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To grow or not to grow: A stressful decision for plants
Accepted Manuscript Title: To grow or not to grow: A stressful decision for plants Author: Rudy Dolferus PII: DOI: Reference:
S0168-9452(14)00243-X http://dx.doi.org/doi:10.1016/j.plantsci.2014.10.002 PSL 9061
To appear in:
Plant Science
Received date: Revised date: Accepted date:
4-9-2014 6-10-2014 9-10-2014
Please cite this article as: R. Dolferus, To grow or not to grow: a stressful decision for plants, Plant Science (2014), http://dx.doi.org/10.1016/j.plantsci.2014.10.002 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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To grow or not to grow: a stressful decision for plants
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Agriculture Flagship
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Contents
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Abstract ..................................................................................................3 1. Introduction .......................................................................................4
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1.2. Plant growth and the environment ......................................................................5
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1.3. Can we exploit plant adaptive capacity?.............................................................6
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1.4. The virtue of model plants ..................................................................................7
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1.5. Are domesticated plants different? .....................................................................8
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2. Genetic approaches for improving abiotic stress tolerance.............9
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2.2. Avoidance and escape reactions .......................................................................10
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2.3. Constitutive vs. inducible stress tolerance ........................................................11
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2.4. QTL analysis in the genomics era.....................................................................15
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2.5. Next generation phenotyping methods .............................................................16
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3. Components of abiotic stress responses ..........................................17
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3.2. First things first: establishment of cellular protection ......................................19
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3.3. Taking care of metabolic adjustment................................................................20
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3.4. Do abiotic stress response pathways overlap? ..................................................22
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3.5. Selection for tolerance to multiple abiotic stresses...........................................23
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1.1. Abiotic stresses: definition and impact on agriculture........................................4
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2.1. Field or controlled environment phenotyping?...................................................9
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3.1. The power of transcriptomics ...........................................................................17
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3.6. Transgenic approaches for abiotic stress tolerance...........................................25
4. Coordination of growth responses to abiotic stress........................27 4.1. Do plants have brains? ......................................................................................27 4.2. Growth inhibition responses .............................................................................28 4.3. Growth stimulation responses...........................................................................30 4.4. An old legend born again: auxins .....................................................................32 4.5. Coordination of environmental responses ........................................................33
5. Conclusions.......................................................................................35 Acknowledgements ..............................................................................37 References ............................................................................................38 Figure Legends.....................................................................................59
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Abstract
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Progress in improving abiotic stress tolerance of crop plants using classic breeding
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and selection approaches has been slow. This has generally been blamed on the lack
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of reliable traits and phenotyping methods for stress tolerance. In crops, abiotic stress
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tolerance is most often measured in terms of yield-capacity under adverse weather
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conditions. “Yield” is a complex trait and is determined by growth and developmental
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processes which are controlled by environmental signals throughout the light cycle of
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the plant. The use of model systems has allowed us to gradually unravel how plants
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grow and develop, but our understanding of the flexibility and opportunistic nature of
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plant development and its capacity to adapt growth to environmental cues is still
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evolving. There is genetic variability for the capacity to maintain yield and
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productivity under abiotic stress conditions in crop plants such as cereals.
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Technological progress in various domains has made it increasingly possible to mine
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that genetic variability and develop a better understanding about the basic mechanism
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human nutrition, the cereals.
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of plant growth and abiotic stress tolerance. The aim of this paper is not to give a detailed account of all current research progress, but instead to highlight some of the current research trends that may ultimately lead to strategies for stress-proofing crop species. The focus will be on abiotic stresses that are most often associated with climate change (drought, heat and cold) and those crops that are most important for
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Keywords:
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Abiotic stress/plant development/senescence/hormone regulation/cereals/crop yield
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1. Introduction
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1.1. Abiotic stresses: definition and impact on agriculture
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Plants are immobile and depend on their environment for growth and development.
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This environment is variable and challenges plants with abiotic stress situations
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throughout their life cycle: light (quality and quantity), mineral nutrition (depletion
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and toxicity, salinity), temperature (heat, cold) and water availability (drought,
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flooding). Plant development is therefore flexible and adjustable to the environment.
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During evolution, wild plant species have learned to adapt to their natural
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environment and this has determined their geographical distribution. In agricultural
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environments, crop productivity is usually well controlled by agronomical practices,
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but crop losses due to extreme and unexpected weather events are unavoidable. The
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prospect of having to meet food demands for a 34% increase of the global population
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by 2050 is imminent [1]. Crop yields will need boosting, but the higher frequency and
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intensity of drought, heat and cold spells will also require crops that are better able to
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therefore be based on a thorough understanding of the complexity of plant growth and
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maintain productivity under sub-optimal conditions. The concept of “tolerance” and “sensitivity” of plants to abiotic stress situations can be difficult to measure. In model plants like Arabidopsis, tolerance is often measured as “survival”. In crop species like cereals maintenance of “yield” and “productivity” is for economical reasons more important than “survival”. The criteria to evaluate stress tolerance in crop plants must
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developmental processes that ultimately correlate with maintenance of productivity.
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Unfortunately, this knowledge is still evolving.
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5 Progress in cereal yield improvements has generally been slow and is starting to reach
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a plateau, falling short of the annual yield increases required to meet 2050 food
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demands [2]. In rice and wheat it is estimated that annual rate of yield increase has so
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far been primarily achieved through improved managing practices (mechanisation)
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rather than through breeding and genetic gain [3, 4]. During the last decade significant
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progress has been made in improving our understanding about plant physiology and
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molecular biology and new technologies have placed us now in a better position to
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improve the efficiency of crop breeding. Improved knowledge and advanced new
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technologies may now provide us with an opportunity to improve the speed and
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efficiency of breeding to boost crop yield and abiotic stress tolerance.
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1.2. Plant growth and the environment
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Plants continuously adjust growth and development, growing prolifically when
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conditions are optimal and slowing down, arresting and even reversing growth (e.g.
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abscission, senescence and cell death responses) under sub-optimal conditions - even
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is therefore not surprising that crop productivity attributes (yield, quality) are strongly
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influenced by environmental variability (gene-environment interactions, GxE).
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Consequently, the responsiveness of crop plants to abiotic stresses is equally variable
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and is controlled by complex gene networks with epistatic interactions [5]. In the
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field, crop plants are continuously challenged by a combination of stresses which are
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when conditions are not life-threatening. This bidirectional growth adjustment mechanism is quite remarkable and poorly understood, but it may hold the key for improving abiotic stress tolerance. Plant growth is a measure of environmental input and adaptive capacity to a particular environment; some conditions can be controlled by humans (irrigation, fertilization etc.), but others are at the mercy of the weather. It
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6 often typical for that environment. Breeding activities are usually focused on specific
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target environments, but this approach tends to improve adaptive traits that are
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constitutively present and are relevant for that environment only. This approach may
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have resulted in the loss of genetic variation from current breeding stock that would
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allow the plant to maintain productivity under unexpected and/or more extreme stress
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conditions. To identify germplasm that is better able to maintain productivity under
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more challenging abiotic stress conditions, it will be necessary to increase the
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selection standards and identify germplasm that is able to perform well under stress
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conditions.
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1.3. Can we exploit plant adaptive capacity?
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Plants in general (higher and lower plants) have a staggering capacity to adapt to
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extreme environments and they can be found in most ecosystems of the globe. Some
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grasses and flowering plants can be found on the Antarctic Peninsula [6], resurrection
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plants are adapted to extremely hot and dry conditions [7, 8], while seagrasses are
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stress signalling and metabolic and developmental adaption mechanisms [8, 10].
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Proof-of-concept transgenic approaches can be used to evaluate some of these
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adaptation mechanisms (e.g., cryo- and osmo-protectants) in crop species such as
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cereals. However, this may be difficult to achieve if genes of an entire metabolic
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pathway need to be transferred and it may also compromise important yield and
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land plants that have re-adapted to life in a marine environment, surviving conditions of low light, high salt and anoxia in the sediment [9]. Adaptation of plants to extreme environments requires complex morphological, developmental and metabolic adaptations. Exploring the molecular mechanisms of drought tolerance in resurrection plants and salt tolerance of halophytes has benefited our understanding about abiotic
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7 quality traits. Important morphological and developmental components that contribute
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to abiotic stress tolerance simply cannot be transferred to cereals. Sourcing abiotic
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stress tolerance traits from the available genetic variability in crop species, landraces
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and progenitor species may be a more desirable approach.
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1.4. The virtue of model plants
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A small genome size has been an important criterion for the selection of model plants.
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The simple dicot Arabidopsis has been a workhorse for advancing our understanding
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of various plant biological processes, including plant development and response to
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various abiotic stresses. Comparative genomics is starting to reveal important
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differences between different model systems, suggesting that care is needed when
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extrapolating information from model systems to other plants. For example, some
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genes are missing in Arabidopsis that are present in other plants [11], while other
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genes have diverged and evolved different functions in other plants. The control of
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flowering and flower development differs considerably between eudicots
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has become faster and cheaper, which has made it possible to sequence larger plant
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genomes. In addition to the rice genome, the genome sequences of four other
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cultivated grasses (maize, sorghum, barley and wheat; www.gramene.org) and one
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wild grass (Brachypodium; www.brachypodium.org) are now available, providing a
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wealth of information for comparative genomics studies into the evolution of these
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(Arabidopsis) and monocots (rice, Brachypodium), even though the regulatory genes (e.g. MADS-box genes) identified in Arabidopsis are also present in monocots [1214]. In addition, it has been shown plants that many of the proteins with completely unknown function (POFs; proteins with obscure features) are species-specific and have no homologues in other species [15, 16]. In recent times, sequencing technology
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genomes (synteny, gene loss/conservation, gene divergence). This unstoppable
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progress in sequencing technologies and genomics will ultimately reduce the reliance
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on model systems.
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1.5. Are domesticated plants different?
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Domestication has turned wild ancestor varieties into cultivated crops that have a
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different architecture and look vastly different from their progenitor species (e.g., rice:
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Fig. 1). Selection for desirable traits has affected many plant developmental
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processes, including yield-related traits (seed size and number), seed shattering, seed
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dormancy, photoperiod and flowering time, palatability and overall shape and body
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architecture [17, 18]. Comparative genomics is slowly revealing the effect of
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domestication at the DNA level [19]. Comparison of the wild rice (Oryza rufipogon)
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and cultivated rice (O. sativa japonica) genome sequences reveals significant gene
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loss in the cultivated species [20]. A comparison between domesticated and wild
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tomato revealed genes that underwent positive selection and many genes that showed
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ancestor plants and landraces are often more tolerant to abiotic stresses and this
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genetic variability could be re-introduced in domesticated crops. This process has
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started for cereals such as rice [23] and maize [24] using wide crosses between
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progenitors and interbreeding relatives. In bread wheat, the reconstruction of synthetic
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hexaploids from the respective wild ancestors aims to achieve a similar goal [25].
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shifts in gene expression levels [21]. Some gene deletions, mutations and variation in gene expression may have directly or indirectly affected abiotic stress tolerance. In beans, two DREB2 loci (dehydration-responsive element binding transcription factor) shared high levels of sequence diversity in one bean locus but no variation in the other, suggesting that domestication may have affected one of these genes [22]. Wild
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9 This process can be complicated by the lack of molecular markers for precision
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breeding and the possible introduction of undesirable traits. These problems will be
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discussed in more detail in the following chapter. Comparative genomics could also
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be used to compare adaptation of crop species to abiotic stresses in different
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environments and to compare genetic variability in stress tolerance [26]. The
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difference in growth responses to environmental conditions can also reside in more
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subtle changes in gene functions (e.g., base pair substitutions). Identifying those
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differences will take additional effort.
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2. Genetic approaches for improving abiotic stress tolerance
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2.1. Field or controlled environment phenotyping?
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Controlled environments allow control over occurrence and timing of a stress during
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plant development, as well as its duration and severity. It is also possible to
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investigate the effect of a single abiotic stress at a time. This is a significant advantage
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over field studies, where environmental conditions are typically variable and
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unpredictable. However, field environments remain difficult to simulate in growth chambers, even though technology is improving [27]. Air humidity, variation of light quantity and quality throughout the day (blue and red light enrichments at sunrise and sunset, respectively) control important plant physiological processes, yet are often
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ignored in controlled environments. Additionally, heat load caused by light bulbs can
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sometimes cause heat stress problems [28, 29] and soil drought and frost events are
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extremely hard to simulate in controlled environments. In the field, environmental
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changes that cause stress in plants most often occur over several hours (in the case of
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heat during the day or frosts overnight) or even over several days (in the case of
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10 drought). These gradual changes are difficult to replicate in controlled environments
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and stresses are often imposed abruptly, causing a shock situation by not allowing the
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plant to gradually adapt to the stress. Additionally, growing plants in pots that are too
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small affects root development, which in the case of drought stress affects the severity
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and the speed with which the stress is imposed [30, 31]. Despite these issues,
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controlled environments are the only tool that allows the comparison between
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different stress responses independently and when used with due care and reasonable
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attention, they can help to analyse stress responses in terms of sensitivity of different
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plant developmental stages and effect of treatment duration and severity. This is very
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important for designing phenotyping methods and to make sure that lines with
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different flowering times are stressed at the same developmental stage when
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comparing different lines. Communication with breeders and farmers can identify
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germplasm that performs better/worse in field stress conditions and this material can
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then provide an excellent benchmark to establish “realistic” stress treatment
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conditions that give identical rankings in growth chambers. It is equally important to
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replicate controlled environment results under field conditions.
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flowering time [32, 33]. This is particularly troublesome when screening large
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populations that segregate for flowering time genes. Flowering time is important for
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optimizing grain yield in wheat, as flowering too early can result in cold and frost
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damage and late flowering can result in poor yields due to drought and heat stress [34,
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35]. Manipulating flowering time can also have adverse effects on yield; early-
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2.2. Avoidance and escape reactions Selecting germplasm that is tolerant to abiotic stress under field conditions is compromised by escape or avoidance responses. In wheat, the damage caused by terminal drought can be alleviated by escaping drought through alteration of
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11 maturing varieties have less chance to accumulate biomass compared to late maturing
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varieties, which indirectly affects grain yield in wheat [36]. Plants can also avoid
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stress damage by adapting metabolic activity and growth rate. Accelerated growth
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requires faster metabolism and mobilization of resources, while slowing down
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metabolism and growth saves vital resources for passive survival of abiotic stress
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conditions. Plants can use any of these tactics for survival in a particular environment.
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In rice, ethylene response transcription factors (ERF) play an important role in
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flooding tolerance [37, 38]. The ERF genes SNORKEL1 and 2 are important in deep-
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water rice varieties, where elongation growth and outgrowing rising water levels
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(escape response) is important for longer-term survival and grain production. In
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contrast, another ERF-family member, SUBMERGENCE-1A (SUB1A), is important
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in rice varieties that have to survive occasional short-term submergence and flooding
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by transiently keeping growth and metabolic activity quiescent. Analysis of the
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molecular basis indicates that the plant hormone ethylene plays an important role in
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regulating elongation growth under stress conditions. The example of flooding
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tolerance in rice illustrates the importance of regulating plant growth rate and
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2.3. Constitutive vs. inducible stress tolerance
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Selection for yield-related traits in field environments has dominated crop breeding.
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Traits such as growth vigour, biomass accumulation, harvest index (reproductive
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biomass), stem carbohydrate levels, tiller number, plant height, water use and
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metabolic activity under stress conditions. Avoidance and escape reactions generally provide protection against abiotic stress through adjustment of growth rate and developmental processes. Understanding the molecular basis of these processes is important for understanding abiotic stress tolerance.
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12 transpiration efficiency, carbon isotope discrimination and root depth are important in
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cereal breeding. These traits, together with improved management practises, have
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improved vegetative growth of cereal crops, resulting in higher yield and productivity
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[32, 33, 39-41]. Interestingly, for Australian wheat the yield gain was found to be
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proportionally higher in the driest years compared to the better years even though
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those traits were not specifically targeting drought conditions [4]. This illustrates that
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yield-based traits that boost vegetative growth, biomass accumulation and water use
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efficiency generally benefit plant growth and resilience and contribute to higher yields
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under abiotic stress conditions [3-5, 41, 42]. However, unexpected and more extreme
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abiotic stress conditions still result in massive yield penalties, indicating that growth
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vigour and biomass accumulation does not necessarily result in a better capacity to
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maintain that yield potential when growth conditions during reproductive
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development are not favourable [5]. It is clear that an additional tolerance mechanism
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is needed to convert or maintain the yield potential generated during the vegetative
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stage to successful reproductive development and grain productivity. Sensitivity of
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crops to various abiotic stresses are usually associated with phenotypes that are
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compromised as growth repression saves resources for later growth when conditions
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have returned to normal [43]. Even when this occurs, yield can never be recovered
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because it is too late in the growing season and previously established biomass and
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productivity has been lost. In many crops, growth repression can be an exaggeration
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indicative of growth arrest, generally including leaf senescence or cell death, severe tissue necrosis (e.g., frosts and salinity), stomatal closure and arrest of photosynthesis [5]. At the reproductive stage, pollen sterility and abortion of grain development are similar growth repression phenotypes that cause major yield losses in cereals. Under shorter-duration or unexpected stress periods, survival of the plant is often not
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13 or an overly sensitive response to stress conditions. There may therefore be an
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opportunity for increasing the threshold level at which growth repression takes place
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in response to stresses, in order to maintain growth and productivity for as long as
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possible. Interestingly, the two flooding tolerance mechanisms described earlier for
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rice (section 2.2: growth acceleration versus metabolic quiescence) may be more
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widely applicable for other abiotic stresses and the molecular understanding of
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flooding tolerance may stimulate research on other abiotic stresses. An intriguing
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question is whether avoidance and escape strategies should also be seen as part of the
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plants overall strategy to tolerate abiotic stresses.
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To identify crops that maintain growth and yield potential under adverse growth
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conditions it is necessary to complement constitutively expressed yield traits with
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traits that are induced and specifically expressed under stress conditions. Identifying
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more stress-induced traits will have a positive effect for breeding stress-tolerant crops,
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but also for improving our understanding of the underlying physiological and
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molecular mechanism. Under stress conditions, plants require mechanisms to protect
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(irrigated, rain-fed, rainout shelter plots to compare water stress conditions) [44].
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However, controlled environments offer significant advantages if precision-
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phenotyping is required (see section 2.1). Leaf senescence is a stress-induced
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phenotype and has received a lot of attention as a stress-induced trait. Selecting for
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their cellular machinery, metabolic adaptations and their capacity to sustain growth and development (see section 3). Selection for stress-inducible traits is more difficult to achieve, considering the unpredictability of field conditions and interference of avoidance and escape reactions. Field plots can be selected to target certain abiotic stresses (drought, heat, frost) or can be artificially modified to create stress conditions
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14 delayed foliar senescence (stay-green) and maintenance of stomatal conductance,
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transpiration and photosynthesis during stress conditions are relatively easy
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phenotypes to score [45]. Significant improvements in drought tolerance have resulted
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from proof-of-concept transgenic approaches manipulating cytokinin levels,
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confirming that this trait contributes to stress tolerance [46]. Leaf rolling is another
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distinctive and easy to score heat and drought-induced phenotype. Reduction in leaf
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area prevents transpiration and water loss and genetic variation for leaf rolling is
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available in wheat and rice. However, leaf rolling does not always correlate with
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drought tolerance, suggesting that it could be an escape rather than tolerance
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mechanism [47, 48]. Osmotic adjustment is an inducible drought adaptation
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mechanism that maintains leaf water potential through the synthesis of osmotically
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active substances [44, 50]. Osmotic adjustment delays leaf senescence and leaf
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rolling, maintains stomatal conductance and turgor pressure, thereby sustaining
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growth under drought conditions [51]. Despite its importance, osmotic adjustment has
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so far remained a difficult trait to phenotype [52]. Many abiotic stresses cause pollen
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sterility and loss of fertility and grain yield in cereals [53, 54]. A phenotyping method
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building up a higher yield potential, stress-inducible traits are essential to sustain that
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higher yield potential under adverse environmental conditions to maintain growth and
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reproductive development.
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for cold and drought-induced pollen sterility was established using controlled environments [55, 56] and the plant hormone abscisic acid (ABA) was shown to play a role in stress-induced pollen abortion [53, 57, 58]. Stress-inducible traits are less likely to have negative effects on productivity of crops under non-stress conditions. While yield traits that improve vegetative plant growth and development contribute to
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2.4. QTL analysis in the genomics era
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Identifying genetic variation for abiotic stress tolerance in crops requires the tedious
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and laborious process of establishing linkage maps using DNA-based molecular
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markers: restriction fragment length polymorphism (RFLP), amplified fragment
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length polymorphism (AFLP), random amplification of polymorphic DNA (RAPD),
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cleaved amplified polymorphic sequences (CAPS) and simple sequence repeat (SSR,
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microsatellite) markers. In the last decade, the shift to high-throughput technologies
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such as Diversity Arrays (DArT; [59]) and Single Nucleotide Polymorphism markers
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(SNP; [60]) has made the construction of high density genomic maps easier. The
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identification of SNP markers was boosted by the availability of the genome sequence
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for many crop species. 160,000 SNPs were identified in the non-repetitive genome
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fraction of 20 different rice varieties [61]. The availability of annotated genome
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sequences and accurate high density SNP maps makes it easier to identify candidate
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genes within QTL (Quantitative Trait Loci) regions [61, 62] and the lowering in
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sequencing costs has made it possible to carry out genotyping by sequencing (GBS),
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which further facilitates fine-mapping QTL [63]. Genome-wide association studies
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(GWAS, [64]) also benefit from high density SNP maps and can be used for mapping abiotic stress tolerance loci. In wheat, the development of multi-parent advanced inter-cross populations (MAGIC) provides a powerful tool for mapping QTL [65].
Abiotic stress tolerance is typically controlled by a large number of QTL with
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epistatic interactions and low phenotypic contribution and heritability. A
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comprehensive overview of QTL for various abiotic stress-related traits can be
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accessed at the Gramene and Plant Stress websites (archive.gramene.org/qtl/;
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www.plantstress.com/files/qtls_for_ resistance.htm). Abiotic stress QTL mapping and
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16 genomic selection (GS) has so far not led to markers for routine use in marker-
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assisted selection (MAS) for abiotic stress tolerance [41, 66, 67]. With the bottleneck
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of genotyping removed, mapping of abiotic stress tolerance loci will depend on the
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availability of reliable traits for phenotyping. The case of salinity tolerance in rice is a
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good example that QTL analysis can lead to identification of candidate genes
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provided that reliable phenotyping methods are available [68].
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2.5. Next generation phenotyping methods
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Considering the difficulties involved in direct selection for abiotic stress tolerance in
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field or controlled environments, shifting from “observable” to molecular or
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secondary traits that are highly correlated with abiotic stress tolerance, may improve
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reliability of phenotyping procedures [69]. Our understanding about the physiological
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and molecular basis of stress responses has improved and technological progress in
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the last decade has provided opportunities for high-throughput phenotyping.
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Metabolomics is a promising technology that can now be used at a scale that is
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used to quantitatively and qualitatively evaluate components of cellular protection.
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Hormone measurements can be used as indicators of developmental responses in
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sensitive and tolerant germplasm (senescence or growth). Proteomics can also be used
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for phenotyping abiotic stress responses, but protein expression profiling can be
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technically more challenging (e.g., resolution limits of two-dimensional
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compatible with population screening and mQTL mapping. This technology was used to identify genes controlling several metabolites and quality-related traits [70-72], but can also be used to map mQTL for metabolite changes associated with abiotic stresses [73, 74]. Measuring diagnostic metabolites can be informative about the physiological state of plant tissues in response to drought, heat and cold and metabolomics can be
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17 electrophoresis and detection limits of mass spectrometry) and is harder to adapt for
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high throughput screening [75]. The development in recent years of various digital
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imaging technologies has added even more opportunities for phenotyping [67, 76].
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Non-destructive imaging can measure canopy properties that contribute to biomass
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accumulation, as well as stress-related traits (photosynthesis, transpiration and leaf
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senescence). This technology can be applied for high-throughput screening under
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field or controlled environments [77-79]. New generation phenotyping technologies
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are powerful but require some knowledge about the molecular and physiological basis
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of abiotic stress phenotypes and the questions to be addressed.
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3. Components of abiotic stress responses
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3.1. The power of transcriptomics
414
While GxE interactions are considered problematic and something to avoid in plant
415
breeding, molecular biologists have used differential gene expression of stress-treated
416
versus unstressed plant material as a standard method to study abiotic stress
418 419 420 421
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responses. In the recent decade, large-scale transcriptome analyses using microarrays and more recently new generation sequencing technologies (RNA-seq) have proven to be a powerful tool for identifying genes and cellular processes that are affected by abiotic stresses [80]. A massive amount of transcriptome information for different stresses and plant species is currently available in public databases.
422 423
Transcriptome information is starting to reveal how plants respond to various abiotic
424
stresses, but the full potential is still unexplored [81]. Currently, about 40% of the
425
proteins encoded by a eukaryotic genome have an unknown function [82]. It is
Page 17 of 65
18 estimated that between 18 and 38% of the eukaryotic proteome consists of proteins
427
without any defined domain or motif [15]. Interestingly, when comparing the
428
Arabidopsis and rice proteins with totally unknown features (POFs) nearly half were
429
found to be species-specific and had no homolog in the other genome [16].
430
Obviously, identifying the function of these proteins will require species-specific
431
studies and this will be a major challenge. Finding the exact physiological function for
432
members of large gene families (e.g., transcription factors) can also be a complicated
433
and time-consuming process. In model plants such as Arabidopsis and rice, insertion
434
mutagenesis using T-DNA and transposons can be used to identify gene functions and
435
support the gene annotation process. In rice, about 60.49% of the nuclear genes have
436
been tagged with T-DNA or Tos17 transposon insertions [83], but the functional
437
characterization of these insertion mutants remains a major effort. In addition, the
438
function of some genes for which the insertion mutant phenotype is lethal cannot be
439
investigated. Another limitation is gene redundancy and lack of a clear phenotype for
440
some mutations. Over-expression and RNAi technology can also be used to reveal the
441
function of candidate genes in plants that can be transformed. Transcriptome analysis
446
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447
triggering early developmental responses, are likely to be present all the time and
448
simply require activation by upstream signals (e.g., phosphorylation). Identifying
449
those genes will require more fundamental approaches, ideally using model systems
450
in the first place (e.g., using mutagenesis approaches).
442 443 444 445
needs support from other technologies to speed up the identification of unknown gene functions. A systems biology approach combining transcriptomics with proteomics and metabolomics can help this process [84, 85]. It is also important to realize that transcriptomics focuses on differentially expressed genes, while some genes that play an important role in the early stress signal perception and transduction events, or those
Page 18 of 65
19
3.2. First things first: establishment of cellular protection
452
Bacteria, yeast and animals have a general cellular stress response mechanism that
453
protects essential macromolecules (DNA, proteins and lipids) against oxidative stress
454
and removes damaged cells using a cell death response. The conservation of this
455
response in different life forms suggests that it is an ancient protection mechanism
456
against general stress situations. The minimal cellular stress response proteome
457
consists of 44 proteins with known function, including molecular chaperones (e.g.
458
heat shock proteins), various enzymes that repair DNA damage and various proteins
459
that protect against oxidative stress and reactive oxygen species (ROS), such as
460
superoxide dismutase and glutathione antioxidant defence pathway proteins [86].
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Plants also activate a cellular protection mechanism in response to various stresses.
463
Little is known about macromolecule protection in plants, but chaperone proteins (e.g.
464
heat shock proteins) are induced by all abiotic stresses and their importance is
465
illustrated by the fact that an Escherichia coli gene encoding a cold shock protein that
466
functions as RNA chaperone can significantly improve tolerance to multiple stresses
468 469 470 471
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(cold, drought, heat) in transgenic rice and maize [87]. The transformation of light into chemical energy during photosynthesis and the mitochondrial electron transport chain produce damaging free radicals [88]. Regulation of intracellular redox homeostasis has been shown to control important metabolic pathways such as photosynthesis [89, 90] and is also important for regulating root and leaf
472
developmental processes [91, 92]. Superoxide, hydrogen peroxide and hydroxyl
473
radical production is induced in response to abiotic and biotic stresses and results in
474
activation of genes encoding ROS-detoxifying enzymes [93, 94]. Active oxygen
475
species such as hydrogen peroxide are generally considered as local and systemic
Page 19 of 65
20 signals in response to various stress situations [95, 96]. This indicates that plants may
477
have turned this early stress defence mechanism into a systemic warning signal to
478
protect different plant parts. Some oxidative stress-related genes are expressed in cells
479
associated with the vascular bundles [97], which is compatible with a systemic
480
signalling function of ROS [98-100]. Resistance to the ROS-generating herbicide
481
paraquat in Conyza bonariensis is correlated with a highly expressed constitutive
482
ROS detoxification system and cross-tolerance to environmental oxidants [101, 102].
483
Paraquat resistance in wheat and barley has been correlated with tolerance to water
484
stress and paraquat treatment has been evaluated as a screening system for abiotic
485
stress tolerance [103, 104]. Overexpression of peroxidase, catalase, superoxide
486
reductase and superoxide dismutase in transgenic plants has resulted in improved
487
tolerance to cold, drought, salinity and heat stress [105-108], while an ascorbate
488
deficient mutant in Arabidopsis caused a stress-sensitive phenotype [109]. Cellular
489
protection in plants may also function as an intracellular and systemic signal to
490
regulate developmental processes. As a stress defence mechanism it may be essential
491
for all other aspects of the stress response to function and it could therefore act as an
493 494 495
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“enabling” mechanism that needs to be activated before other aspects of stress responses (biotic and abiotic) can be established (Fig. 2).
3.3. Taking care of metabolic adjustment
496
Changes in plant growth and development under abiotic stress conditions must be
497
associated with metabolic activity to provide the energy required to establish the
498
response. Firstly, the altered cellular environment requires changes in the cellular
499
machinery to be put in place; adaptations of translation initiation and protein folding
500
are commonly observed in stress-induced transcriptomes [110, 111]. Then, specially
Page 20 of 65
21 adapted metabolic proteins are induced early in the stress response (Fig. 2). Many
502
abiotic stresses shut down photosynthesis, while photosynthates are a crucial source
503
of energy. Sugars are transported from source to sink tissues via the phloem and are
504
important signals for growth and development, as well as response to various abiotic
505
stresses. Sugar signalling and metabolism are therefore tightly linked to growth
506
responses [112]. ABA regulates stomatal conductance and photosynthetic activity,
507
causing vegetative growth retardation. This has been shown to contribute to
508
vegetative stage abiotic stress tolerance, but this growth repression also has a negative
509
effect on reproductive processes [113]. Abiotic stresses repress the sucrose cleaving
510
enzyme cell wall invertase in anthers, preventing hexose supply for pollen
511
development and causing pollen sterility. ABA accumulation was shown to directly or
512
indirectly repress cell wall invertase expression. Tolerant wheat and rice germplasm
513
displayed different anther ABA homeostasis, maintaining lower ABA levels than
514
sensitive lines in response to cold and drought stress [55-57, 113]. Sugars and ABA
515
are known to regulate ethylene and senescence responses [114]. Sugars are an
516
important growth signal in plants and are therefore tightly connected with the decision
521
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501
522
osmotic stresses such as drought, cold and salt stress and are tightly integrated with
523
signalling pathways for sugars, essential nutrients (nitrogen) and various hormones
524
[118-120]. The yeast SnRK (Sucrose non-fermenting related kinase) related protein
525
kinases KIN10 and KIN11 play a central role in coordinating sugar, stress and
517 518 519 520
to grow or repress growth and respond to abiotic stress (Fig. 2). The glycolytic enzyme hexokinase (HXK) is a cellular sugar sensor that cross-talks to several phytohormones [115]. Other cellular components involved in regulation of metabolism in plants show some similarity to yeast. The Mitogen-Activated Protein Kinase (MAPK) [116, 117] and the Salt Overly Sensitive (SOS) pathways respond to
Page 21 of 65
22 developmental signals with metabolic pathways, activating gene expression via bZIP
527
transcription factors [121, 122]. The General Control Non-repressible related protein
528
kinase (GCN-2) phosphorylates translation initiation factor 2 (eIF2α) and is able to
529
sense free amino acid levels, respond to osmotic stresses and control protein synthesis
530
[123, 124]. Both SnRK1 and GCN-2 regulate nitrate reductase and nitrogen
531
metabolism [120, 121]. Further research is required to establish how this complex
532
metabolic regulation mechanism is controlled by environmental stimuli. The
533
conservation of the kinases that regulate fundamental metabolic pathways between
534
plants, yeast and animals illustrates their evolutionary importance.
an
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535
3.4. Do abiotic stress response pathways overlap?
537
It has been demonstrated that treatment with one abiotic stress can provide “cross-
538
tolerance” or “hardening” to other stresses, including biotic stresses [125, 126]. Pre-
539
treatment of plants with the stress hormone ABA has a similar effect [127-129]. This
540
already suggests that there must be some functional overlap in the signalling and
545
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536
546
pollen fertility, induction of osmo-protectants by drought, cold and salinity) are also
547
shared by different stresses. Communication between sink and source tissues is
548
especially important under abiotic stress conditions when growth can be limited by
549
available resources. To fully understand the impact of abiotic stresses on plant growth
541 542 543 544
response pathways of abiotic stresses. Osmotic stresses (drought, cold, salinity, heat) involve ABA and are therefore expected to share common components. Furthermore, transcriptome analyses have confirmed that early macromolecule and oxidative stress protection is recruited by most stresses and is a general stress response (Fig. 2). Some developmental and metabolic responses (e.g., growth adaptation, leaf senescence,
Page 22 of 65
23 550
it is essential to further unravel the relationships between metabolism and
551
developmental processes.
552 Due to gene redundancy, different gene copies encoding proteins with the same
554
function can be activated under different stresses, suggesting that overlap between
555
different stresses could be larger at the protein level than at the transcript level. In
556
economical terms, it seems logical that plants will share the response to the initial
557
threat and mount stress-specific responses once the general response has created the
558
environment to make this possible (Fig. 2). A shared initial stress response may not
559
require many genes and some may have so far remained undetected in differential
560
gene expression studies. Regulation at the protein level, such as targeted protein
561
degradation using the ubiquitin proteasome, is commonly used by plant hormones to
562
regulate downstream developmental signalling [130]. It is therefore possible that a
563
rather small - but critically important - part of the overlap between different abiotic
564
stress responses has so far escaped detection.
cr
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553
570
arrest is taken in this early response mechanism and it is an important factor for
571
determining productivity and abiotic stress tolerance in crops. Selection for adaptation
572
to specific environments and productivity traits has affected many developmental
573
properties and may also have modified the early response mechanism to stress (Fig.
574
2). Selection against seed dormancy may have affected homeostasis of hormones that
566 567 568
3.5. Selection for tolerance to multiple abiotic stresses Genetic diversity for abiotic stress tolerance is more likely to occur in the early response mechanism than in the stress-specific responses that depend on the initial response (Fig. 2). The decision to continue growth or induce senescence and growth
Page 23 of 65
24 play a role in stress tolerance (ABA, GA). Adaptation to seasonal conditions and
576
different environments in cereals has modified important growth processes such as
577
duration of photosynthesis, adaptation to day-length and altered rate of leaf
578
senescence, which may also have changed the interaction between plant hormones
579
(ethylene, cytokinins). The stay-green trait has therefore been thought of as a potential
580
domestication trait [45, 131]. Analysis of stay-green QTL (e.g., sorghum) could lead
581
to positional cloning and identification of new genes involved in this process [45,
582
132].
us
cr
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575
an
583
In nature, frequent exposure to a combination of stresses may have selected a shared
585
genetic adaptation mechanism to those stresses. This may be the case for heat and
586
drought stress which often occur at the same time in field conditions [126, 133]. It
587
therefore makes sense to select germplasm that is tolerant to more than one abiotic
588
stress [126], especially since different abiotic stress responses may already share a
589
common initial response mechanism (Fig. 2). Germplasm that establishes the initial
590
response successfully may also be better able to establish a stress-specific response
595
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584
596
wheat lines that are tolerant to multiple abiotic stresses individually (drought, heat,
597
shading and cold). QTL mapping using this tolerant germplasm can also be used to
598
identify overlapping general stress-response QTL, as well as QTL that are specific for
599
different stresses. Obtaining high levels of abiotic stress tolerance may ultimately
591 592 593 594
(Fig. 2). However, selecting germplasm that is tolerant to more than one stress using the combination of those stresses may be difficult to achieve because of quantitative and qualitative differences in tolerance to the combination of stresses and the difficulty to choose physiologically relevant selection conditions for the combination of stresses. We are currently using a step-wise selection procedure to first identify
Page 24 of 65
25 require combining both general stress response and stress-specific QTL. However, for
601
some traits it may be difficult to obtain tolerance to a combination of stresses; some
602
traits for drought (stomata closed to prevent water loss) and heat stress (open stomata
603
to reduce leaf temperature) are mutually exclusive [126].
604
ip t
600
3.6. Transgenic approaches for abiotic stress tolerance
606
It is common practice in molecular biology to use proof-of-concept transgenic
607
approaches (over-expression, RNAi) to evaluate candidate genes for their effect on
608
abiotic stress tolerance. Many genes have indeed been shown to improve abiotic stress
609
tolerance ([134]; see Plant Stress website for a comprehensive listing:
610
www.plantstress.com/ files/abiotic-stress_gene.htm). These include transcription and
611
regulatory factors, osmo-protectants, hormone and oxidative stress-related genes,
612
molecular chaperones, transporters and various metabolic genes. Abiotic stress
613
tolerance for most of these genes was evaluated under controlled environment or
614
glasshouse conditions, using model systems such as Arabidopsis or tobacco and some
619
Ac ce p
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605
620
tolerance may also be a contributing factor; in model plants tolerance is usually
621
measured as survival under vegetative stage stresses, while in crops maintenance of
622
productivity during reproductive stage stresses is important [136, 137]. The choice of
623
promoter to drive transgene expression is also important. Strong constitutive
624
promoters lead to ectopic expression of a transgene, potentially causing adverse
615 616 617 618
were also evaluated in cereals (rice, wheat, barley, maize). Relatively few transgenic lines have so far made any impact for improving field abiotic stress tolerance [135]. Potential explanations are that the field environment is much harsher, transgenes only partially improve the abiotic stress response or they improve response to one stress and not a combination of stresses. Differences in evaluation criteria for abiotic stress
Page 25 of 65
26 secondary effects on crop productivity. CBF/DREB transcription factors can improve
626
osmotic stress tolerance but result in stunted growth when using constitutive
627
promoters [138]; plants look normal when a strong drought-inducible promoter is
628
used that expresses the transgene only when required [139]. The quantitative and
629
qualitative properties of the promoter driving a transgene may be particularly critical
630
in the case of transcription factors, hormone metabolic and signal transduction genes.
631
Using Arabidopsis as a model system it may be extremely difficult or impossible to
632
fully evaluate and predict potential adverse effects in crop species [139]. In the case
633
of multigene families it is often difficult to find out which gene to use for
634
transformation. For instance, only a few aquaporin gene family members are affected
635
by stress and lead to improvement of drought tolerance in transgenic plants [140]. For
636
large transcription factor families, trial and error approaches can identify which gene
637
has a positive effect on stress tolerance [141]. Some transgenic approaches may result
638
in morphologically different plants where stress phenotypes are simply delayed (e.g.,
639
smaller leaf area reduce transpiration under drought), giving transgenics an unfair
640
advantage [142]. Manipulation of cytokinin levels using a stress-induced promoter led
645
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625
646
multiple stresses (cold, drought and heat) in field experiments [88], suggesting that
647
focusing on the manipulation of the top of the stress signalling cascade using general
648
stress responsive genes may yield positive results.
641 642 643 644
to delayed senescence and improved drought tolerance in rice under glasshouse conditions [143]. It is possible that these transgenic lines may also perform well under field drought conditions, considering the field experience with stay-green plants. Interestingly, transgenic rice and maize plants expressing an E. coli cold shock protein
that acts as RNA chaperone in cellular protection resulted in improved tolerance to
649
Page 26 of 65
27
4. Coordination of growth responses to abiotic stress
651
4.1. Do plants have brains?
652
How are the early responses to abiotic stresses orchestrated by signals from the
653
environment? Higher animals are mobile and react to stress by escaping
654
environmental challenges. The brain processes environmental signals via the central
655
nervous system and regulates this mobility and escape reaction. The flexibility of
656
plant development in response to environmental change indicates that they have an
657
efficient systemic signalling mechanism that coordinates and orchestrates the
658
response to adverse environmental conditions. The plant vascular system bears some
659
resemblance to an animal central nervous system, sparking some speculation that
660
plants have a cellular communication mechanism similar to animals [144]. Specific
661
proteins known to play a role as neurotransmitters in animals (e.g., glutamate
662
receptors, 14-3-3 proteins) are also encoded in plant genomes but they acquired
663
different functions when plants evolved into multicellular organisms. The vascular
664
system plays an important role in coordinating growth and development between the
666 667 668 669
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665
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650
different plant parts [145], but the signalling mechanism is vastly different to that of animals. Plants have evolved their own systemic signals to drive growth and development (Fig. 2). Being photosynthetic organisms, they use photosynthates and the capacity to produce sugars as a resource signal for growth. They also adapted reactive oxygen species as a signal for abiotic stress. Plants have evolved their own
670
hormone signals, which are totally unlike animal hormones, to signal developmental
671
and growth responses. An emerging theme in plant biology is the observation that
672
many genes involved in hormone synthesis and signalling, e.g. those involved in ABA
673
synthesis and signalling [146, 58], are expressed in vascular parenchyma cells. This
Page 27 of 65
28 allows rapid signal perception and distribution via the vascular system, similar to a
675
nervous system but at a slower pace. Environmental signals can therefore be sensed in
676
any plant part and quickly spread throughout the plant, suggesting that plants have
677
essentially obviated the need for a central nervous system. Despite its importance, the
678
signal transmitting function of the vascular system still needs to be unravelled [147].
679
Understanding of how the signals (hormones, ROS, metabolites) themselves work is
680
gradually emerging. Auxins can be transported all over the plant using directional
681
efflux carriers and long-distance transporters and tissue-specific response mechanisms
682
make it possible to mount different auxin responses in different plant parts [148].
683
These different plant parts are pre-programmed to react differently to plant hormone
684
signals, explaining how environmental signals can have different but coordinated
685
responses. Hormonal signals therefore form an important link between the
686
environment and developmental processes. Plant evolution and global diversity is
687
testimony that plants have evolved efficient systems to manage and adapt to
688
environmental challenges.
cr
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693
Ac ce p
689
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674
694
development and have been implicated in abiotic stress responses. A lot of progress
695
has been made in recent years in understanding their function. Plant hormones can be
696
growth-retarding (ABA, ethylene, jasmonic acid) or growth-promoting (auxin,
697
gibberellic acid, cytokinin). Two recently discovered plant hormones, brassinosteroids
698
[149] and strigolactones [150] act in conjunction with auxins and can be classified as
690 691 692
4.2. Growth inhibition responses The key to understanding abiotic stress tolerance resides in understanding the plant’s capacity to accelerate/maintain or repress growth. Interaction between plant hormones must play an important role in this phenomenon. Most plant hormones play a role in
Page 28 of 65
29 growth promoting hormones, while salicylic acid functions in plant defence responses
700
to pathogens [151]. The stress hormone ABA is implicated in stomatal closure and
701
regulation of plant water balance, which impairs photosynthesis and restricts growth
702
[113]. ABA levels are up-regulated in response to osmotic stresses (drought, cold,
703
salinity) and heat stress. Higher ABA levels improve stress tolerance at the vegetative
704
level, but there is a compromise at the reproductive level. QTL analysis in maize
705
indicated that lines with higher root ABA levels had lower grain yield [152] and our
706
own work demonstrated that lower ABA levels in stressed anthers was correlated with
707
better cold and drought tolerance, as well as maintenance of anther sink strength in
708
rice [58]. The ABA signalling pathway interacts with other hormones and sugar
709
signalling via the SnRK network [98, 123]. ABA’s restriction of photosynthesis and
710
photosynthate allocation to sink tissues may help in shorter periods of abiotic stress,
711
but is destructive under longer term stress conditions such as terminal drought. The
712
opposing effect of ABA on vegetative and reproductive structures indicates that it is
713
important to understand the effect of abiotic stress during plant development. The
714
success of transgenic approaches for manipulation of abiotic stress tolerance will
719
Ac ce p
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cr
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699
720
tapetum [153, 154]. External application and stress-induced accumulation of ABA
721
results in senescence, but the role of ABA in this process is still unclear. ABA may
722
interact with the oxidative stress response that protects against senescence [155], but
723
may also cause senescence via interaction with ethylene. The role of ethylene in
715 716 717 718
depend on carefully targeting the control of ABA homeostasis to particular tissues and growth stages.
Growth repression under abiotic stress conditions is associated with induction of leaf senescence (Fig. 3) or programmed cell death responses in tissues such as the anther
Page 29 of 65
30 inducing leaf senescence and inhibition of root elongation has been well investigated.
725
Antisense repression of ethylene biosynthesis inhibits senescence, and the limitation
726
of ethylene production has in many cases resulted in improved abiotic stress tolerance
727
[156]. Ethylene can induce the biosynthesis of the growth-promoting hormone auxin
728
in a tissue-specific manner [157]. The role of ethylene can therefore also be growth-
729
promoting; low light (etiolation) and shading conditions cause elongation growth in
730
shading-sensitive plants [158]. Ethylene is therefore in a unique position to control
731
plant developmental processes: it can act as an inhibitor of growth, but also as a
732
growth promoter (Fig. 4).
an
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724
733
Jasmonic acid can also induce senescence. In Arabidopsis, jasmonate-induced
735
senescence involves induction of the transcription factor WRKY57, which is
736
repressed by the growth hormone auxin [159]. In addition, jasmonate induces
737
expression of ICE (Inducer of CBF Expression), thereby promoting freezing tolerance
738
in Arabidopsis [160]. Ethylene and jasmonate can regulate each other’s homeostasis
739
via feedback regulation, producing a fine balance between growth repression
743
Ac ce p
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734
744
Cytokinins counteract the effect of ethylene, preventing senescence and stimulating
745
sugar metabolism and sink strength. Over-expression of the cytokinin biosynthetic
746
gene isopentenyl transferase has been used to produce plants that show delayed
747
senescence (stay-green trait), increased biomass production and improved stress
748
tolerance [45, 131]. However, the stay-green trait is not always associated with
740 741 742
(jasmonic acid) and growth stimulation (ethylene).
4.3. Growth stimulation responses The growth hormone group of cytokinins plays a role in controlling cell division.
Page 30 of 65
31 749
increased yield and productivity [131], suggesting that increased cytokinin levels
750
benefit vegetative growth but not reproductive development.
751 Gibberellins (GA) play a crucial role in the promotion of plant elongation growth. In
753
the absence of GA, elongation growth is restrained by DELLA nuclear proteins. In the
754
presence of GA, DELLA proteins bind to the GA-GID1 receptor complex, targeting it
755
for degradation by the ubiquitin-26S proteasome and thereby activating GA signalling
756
and elongation growth [161]. Some DELLA mutants are unable to bind the GA-GID1
757
complex, causing it to escape proteasome degradation. This suppresses elongation
758
growth, causing a semi-dwarf phenotype. Other DELLA mutants abolish its
759
repression activity, resulting in a tall stature (slender); these mutants are also male
760
sterile, suggesting that DELLA proteins play a role in pollen development [162].
761
Mutations in GA biosynthesis genes and DELLA proteins with a semi-dwarf
762
phenotype increase yield in cereals and have formed the basis of the Green
763
Revolution [163]. However, some GA-insensitive dwarf mutants in wheat (reduced
764
height; Rht) also have reduced pollen viability, which has been associated with
769
Ac ce p
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752
770
CBF1 was shown to induce DELLA gene expression and activate GA catabolic genes,
771
causing growth repression [168, 169]. Stress-induced accumulation of ABA
772
antagonizes GA action by controlling DELLA activity [170]. In addition, DELLA
773
proteins play a role in mounting a protective response to oxidative stress [169, 171].
765 766 767 768
reduced tolerance to abiotic stresses such as heat and drought [162, 164]. Interestingly, the growth-stimulation of GA can be counteracted by environmental stresses and hormones such as ethylene and auxins, which affect the growth restraining activity of DELLA proteins [165-167]. In Arabidopsis, the CBF/DREB cold-inducible transcription factors activate cold acclimation and freezing tolerance.
Page 31 of 65
32 774
The DELLA proteins obviously form a hub of hormonal and environmental
775
interactions that determine continuation or repression of growth in function of
776
environmental cues [172].
ip t
777
4.4. An old legend born again: auxins
779
Auxins were the first plant hormone to be discovered. The growth-promoting
780
properties of auxins have gained increasing prominence in recent years because of
781
their role in regulating development and response to abiotic stress. Auxins are
782
synthesized in the shoot apical meristem and are transported to neighbouring tissues
783
and over longer distances using efflux carriers and polar transporters respectively.
784
Auxins stimulate root growth and other tissue-specific responses throughout the plant
785
such as leaf and fruit senescence [148]. In Arabidopsis this requires cross-talk with
786
jasmonic acid signalling and the transcription factor WRKY57 [161, 173, 174].
us
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M
d
One of the oldest known effects of auxins is the control of apical dominance and
793
Ac ce p
788
te
787
cr
778
794
have a role in stamen development and are actively synthesized in the anther,
795
controlling pollen development and anther dehiscence [178]. Apical dominance may
796
play an important role in promoting reproductive development and grain yield in
797
cereals. Auxins are synthesized in the anthers towards maturity where they play a role
798
in anther senescence [178, 179]. At the start of reproductive development in cereals
789 790 791 792
shoot branching (tillering in cereals). Cutting the main stem of a plant removes the apical meristem where auxins are made, resulting in increased branching. The branching response involves interaction with strigolactone and requires adequate sugar supply to support axillary bud outgrowth [175, 176]. It has been demonstrated that auxin treatment improves fertility in heat-stressed barley plants [177]. Auxins
Page 32 of 65
33 the shoot apex where auxins are synthesized changes into a flowering meristem. It
800
then develops into a spike containing the reproductive organs. The presence of auxin
801
biosynthesis in the floral organs at this stage might signify that apical dominance is
802
controlled by the reproductive structures. This function may be essential to direct
803
resources to the reproductive structures for seed production rather than investing them
804
in further vegetative growth. Abiotic stresses in cereals cause pollen sterility in
805
sensitive lines, resulting in increased tillering after the stress period (Fig. 3). This may
806
reflect the loss in apical dominance as a result of pollen sterility. An intriguing aspect
807
of auxins is that they regulate some aspects of plant development such as lateral root
808
development synergistically with ethylene and other hormones, while for some
809
aspects both hormones act antagonistically [180]. Recent progress in understanding
810
plant hormone action is illustrating the complexity of cross-talk between different
811
plant hormones and the importance of controlling hormone homeostasis.
812
Understanding the intricacies of these interactions is important to unravel how genetic
813
variability in the network can affect how plants adapt to environmental change.
cr
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d
te
818
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814
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in photomorphogenesis. Phytochromes respond to darkness (etiolation) and changes
820
in the red to far-red light ratio, which warns the plant about competing vegetation
821
(shade avoidance) [158]. Phytochromes control many growth processes from seed
822
germination to reproductive development and they are well known to modulate biotic
823
and abiotic stress responses [181].The activated form of phytochrome moves to the
815 816 817
4.5. Coordination of environmental responses Progress made in unravelling how plants react to low light conditions provided a clue as to how environmental signals regulate plant growth. Phytochrome photoreceptors react to changes in the ratio between red and far-red light and play an important role
Page 33 of 65
34 nucleus and forms a complex with members of the basic helix-loop-helix (bHLH)
825
transcription factors, the Phytochrome Interacting Factors (PIF). PIFs interact with
826
DELLA proteins; in the absence of GA, DELLA proteins bind to PIFs, preventing
827
them from regulating their target genes. In the presence of GA, DELLA proteins are
828
degraded, PIFs become functional and elongation growth is activated [161, 182, 183]
829
(Fig. 4). PIF transcription factors also activate auxin biosynthesis and their own
830
expression is controlled by the circadian clock; the Arabidopsis bZIP transcription
831
factor Hy5 (Elongated Hypocotyl) promotes photomorphogenesis by antagonizing PIF
832
action and the RING-motif E3 ligase COP1 (Constitutive Morphogenic) inhibits Hy5.
833
This pathway also influences CBF function and freezing tolerance [184]. PIFs form in
834
combination with DELLA proteins a hub for the integration of signals from various
835
hormones [183, 185-187], day-length [184, 188], light quality [158, 184], as well as
836
sugars [189] (Fig. 4). Light quality is also important for the induction of CBF
837
transcription factors and activation of cold and frost tolerance [190, 191] and PIFs
838
play a role in regulating expression of DREB transcription factors that are required for
839
drought responses [183]. Low red to far-red ratios lead to increased levels of ethylene
844
Ac ce p
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an
us
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converge into a single, complicated signalling hub that orchestrates plant growth
846
responses. This environmental response hub may explain why one abiotic stress can
847
improve the response to other stresses (section 3.4).
840 841 842 843
[158], which affects the stability of the DELLA proteins [165] (Fig. 4). Induction of the ERF transcription factor SUB1A under flooding conditions prevents elongation growth by increasing DELLA levels, thereby inhibiting GA-mediated elongation growth [37, 38]. The PIF transcription factors also mediate cross-talk with ROS signalling [193]. These findings demonstrate how different environmental stimuli
848
Page 34 of 65
35
5. Conclusions
850
In the last decade important progress has been made using model plants in
851
understanding how plants grow and develop and how they respond to changes in the
852
environment. This know-how is still fragmentary and needs to be extended to crop
853
plants. In important crop species such as cereals, it is important to maintain
854
productivity under abiotic stress conditions during the reproductive stage. Some crop
855
plants appear to overreact and switch to growth arrest too quickly, even when survival
856
is not immediately under threat. One way of improving stress tolerance and grain
857
productivity in cereals would be to increase the threshold level at which plants switch
858
from promotion to arrest of growth. At the vegetative stage, the stay-green trait has
859
achieved this by selecting for delayed senescence. Maybe an equivalent of the stay-
860
green trait is required to protect the reproductive stage and grain formation in cereals.
861
Seed production itself is a stress survival mechanism; seed can survive prolonged
862
stress conditions in dehydrated state and this guarantees the plant’s next generation.
863
This potential may have been lost from crop plants, but genetic diversity to
864
reintroduce this trait may still be available in breeding lines, landraces or wild
866 867 868 869
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an
M
d
te
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progenitor species. This material can also be used to further improve our understanding of the hormonal interactions that control growth.
A lesson could be learned from flooding tolerance research, which showed that both growth arrest and acceleration can be beneficial – depending on the circumstances.
870
This response requires ethylene and ERF transcription factors. The molecular basis of
871
how flooding tolerance interacts with the environmental response hub can serve as a
872
guideline for other abiotic stresses. Response to shading also shares some of the hub
873
components used by flooding stress. Importantly, the example of flooding stress
Page 35 of 65
36 indicates that avoidance and/or escape reactions should not necessarily be treated as
875
different or independent from true tolerance responses. The common denominator is
876
“growth regulation”. It is crucial that we learn to understand how plants regulate
877
growth in function of environmental restraints; this may lead to strategies to
878
manipulate the threshold levels to switch from growth arrest to maintenance of
879
growth. Crop plants such as cereals, combined with current technologies, can help us
880
to reach that level of understanding.
cr
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874
us
881
Having a single regulatory hub to integrate all environmental responses and regulate
883
plant growth and development makes a lot of sense, but a lot of questions still need to
884
be answered. We need to get a better understanding about systemic signalling and the
885
relationship between vegetative and reproductive growth. During the stage of
886
flowering and seed production, a plant behaves quite differently from a plant during
887
vegetative growth. Even though there is a shared response system to the environment,
888
growth signals still need to be relayed to different plant parts and the effect in
889
different plant parts can be interpreted very differently. For instance, nitrogen
894
Ac ce p
te
d
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an
882
895
environment. The use of Green Revolution genes in cereals has shown that reducing
896
stem elongation growth using semi-dwarf genes benefits grain yield, but there is a
897
trade-off in terms of abiotic stress tolerance and pollen fertility. Some semi-dwarf
898
mutations affect the function of DELLA proteins in the central hub controlling growth
890 891 892 893
application can stimulate vegetative growth and repress reproductive development. In cereals, grain yield depends on successful interaction between both vegetative and reproductive growth. While management, agronomy and breeding practices have focused a lot on the vegetative establishment phase of cereals, relatively little is known about the control of reproductive development and its interaction with the
Page 36 of 65
37 and abiotic stress responses (Fig. 4). This raises the question whether high yield and
900
high abiotic stress tolerance are compatible – or not. There is a strong need to fully
901
understand the function of the central environmental response hub (e.g., role of PIF
902
family members, identification of still unknown components), but the use of model
903
systems only may not allow us to achieve this and genetic variation in crop species
904
should be included in these studies. Analysing this genetic variation using new
905
generation genotyping and phenotyping technologies has vastly improved and
906
identification of candidate stress tolerance genes is made easier using genomics.
907
Proof-of-function transgenic approaches may also lead to identification of genes that
908
can be used for stress-proofing cereals.
M
909
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us
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The technological revolution of the last decade has provided renewed hope for
911
improving abiotic stress tolerance in crops such as cereals, but it is clear that this
912
effort will increasingly require close interaction between plant scientists of different
913
disciplines, including bioinformaticians and engineers.
te
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d
910
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of cited references in this review paper has been limited by journal policy. The author
920
apologises to those authors whose publications were not cited in this paper.
915 916 917
Acknowledgements
R.D. is supported by grants from the Grains Research and Development corporation (GRDC, grants CSP00130, CSP00143 and CSP00175). The author thanks Jane Edlington and Holly Staniford for their help in preparing the manuscript. The number
921
Page 37 of 65
38 922
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Figure Legends Figure 1: Effect of domestication in rice. Oryza rufipogon (top panel) is
1417
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1418
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1419
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Figure 2: Proposed components of abiotic stress responses in plants.
1422
Early responses to abiotic stress are likely to be general stress responses: cellular
1423
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1424
hormonal changes that lead to developmental responses. Genetic variation in crop
1425
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1426
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1427
growth, with negative yield consequences. Other germplasm is more resilient and
1429 1430 1431 1432
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will maintain growth and productivity as much as possible. The latter phenotype will require successful interaction between the different early responses to establish stress-specific responses. Genetic variation can occur at different levels of the response pathway. QTL (stars with letter “Q”) in different parts of the general stress response will affect response to different abiotic stresses. QTL in
1433
the stress-specific responses are predicted to only affect response to a particular
1434
stress. Targeting the genetic variation in the general stress response could be more
1435
successful, but may require additional QTL in the stress-specific responses. QTL
1436
for stress-specific responses may have negative effects for other stresses.
Page 59 of 65
60 1437 Figure 3: Effect of drought stress at the reproductive stage in wheat. Drought
1439
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1440
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1441
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1442
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1443
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Figure 4: Simplified schematic representation of the components involved in the
1446
environmental response module that controls plant growth, based on the shade
1447
avoidance response pathway in Arabidopsis. The PIF and DELLA proteins are
1448
central regulators of growth and environmental responses in plants.
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61 Abiotic stresses affect yield and productivity of crop plants. Stress tolerance in crops correlates with maintenance of growth and productivity. Early stress-responsive genes control growth responses Selection strategies should use stress-induced traits and focus on early general stress response. Plant hormone interactions control development and abiotic stress tolerance.
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Page 61 of 65
Ac ce pt e
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Figure(s)
Figure 1
Page 62 of 65
ip t
Q
Q Q
Oxidative Stress Q
Metabolism
Q
Q
Development Q
Q
Q
Growth
an
Senescence
M
Light Stress
Q
Temperature Q Stress
Water Stress
Others
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Environmental Signals
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Phytochrome
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Circadian Clock
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Stress-specific response
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S0168-9452(14)00243-X http://dx.doi.org/doi:10.1016/j.plantsci.2014.10.002 PSL 9061
To appear in:
Plant Science
Received date: Revised date: Accepted date:
4-9-2014 6-10-2014 9-10-2014
Please cite this article as: R. Dolferus, To grow or not to grow: a stressful decision for plants, Plant Science (2014), http://dx.doi.org/10.1016/j.plantsci.2014.10.002 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
1 1 2 3
Review:
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To grow or not to grow: a stressful decision for plants
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Agriculture Flagship
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GPO Box 1600
Canberra ACT 2601 Australia
Tel: +61-2-62465010
E-mail: [email protected]
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Contents
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Abstract ..................................................................................................3 1. Introduction .......................................................................................4
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1.2. Plant growth and the environment ......................................................................5
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1.3. Can we exploit plant adaptive capacity?.............................................................6
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1.4. The virtue of model plants ..................................................................................7
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1.5. Are domesticated plants different? .....................................................................8
31 32
2. Genetic approaches for improving abiotic stress tolerance.............9
33
2.2. Avoidance and escape reactions .......................................................................10
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2.3. Constitutive vs. inducible stress tolerance ........................................................11
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2.4. QTL analysis in the genomics era.....................................................................15
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2.5. Next generation phenotyping methods .............................................................16
37 38
3. Components of abiotic stress responses ..........................................17
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3.2. First things first: establishment of cellular protection ......................................19
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3.3. Taking care of metabolic adjustment................................................................20
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3.4. Do abiotic stress response pathways overlap? ..................................................22
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3.5. Selection for tolerance to multiple abiotic stresses...........................................23
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1.1. Abiotic stresses: definition and impact on agriculture........................................4
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2.1. Field or controlled environment phenotyping?...................................................9
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3.1. The power of transcriptomics ...........................................................................17
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3.6. Transgenic approaches for abiotic stress tolerance...........................................25
4. Coordination of growth responses to abiotic stress........................27 4.1. Do plants have brains? ......................................................................................27 4.2. Growth inhibition responses .............................................................................28 4.3. Growth stimulation responses...........................................................................30 4.4. An old legend born again: auxins .....................................................................32 4.5. Coordination of environmental responses ........................................................33
5. Conclusions.......................................................................................35 Acknowledgements ..............................................................................37 References ............................................................................................38 Figure Legends.....................................................................................59
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3 55
Abstract
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Progress in improving abiotic stress tolerance of crop plants using classic breeding
58
and selection approaches has been slow. This has generally been blamed on the lack
59
of reliable traits and phenotyping methods for stress tolerance. In crops, abiotic stress
60
tolerance is most often measured in terms of yield-capacity under adverse weather
61
conditions. “Yield” is a complex trait and is determined by growth and developmental
62
processes which are controlled by environmental signals throughout the light cycle of
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the plant. The use of model systems has allowed us to gradually unravel how plants
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grow and develop, but our understanding of the flexibility and opportunistic nature of
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plant development and its capacity to adapt growth to environmental cues is still
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evolving. There is genetic variability for the capacity to maintain yield and
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productivity under abiotic stress conditions in crop plants such as cereals.
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Technological progress in various domains has made it increasingly possible to mine
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that genetic variability and develop a better understanding about the basic mechanism
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human nutrition, the cereals.
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of plant growth and abiotic stress tolerance. The aim of this paper is not to give a detailed account of all current research progress, but instead to highlight some of the current research trends that may ultimately lead to strategies for stress-proofing crop species. The focus will be on abiotic stresses that are most often associated with climate change (drought, heat and cold) and those crops that are most important for
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Keywords:
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Abiotic stress/plant development/senescence/hormone regulation/cereals/crop yield
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1. Introduction
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1.1. Abiotic stresses: definition and impact on agriculture
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Plants are immobile and depend on their environment for growth and development.
83
This environment is variable and challenges plants with abiotic stress situations
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throughout their life cycle: light (quality and quantity), mineral nutrition (depletion
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and toxicity, salinity), temperature (heat, cold) and water availability (drought,
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flooding). Plant development is therefore flexible and adjustable to the environment.
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During evolution, wild plant species have learned to adapt to their natural
88
environment and this has determined their geographical distribution. In agricultural
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environments, crop productivity is usually well controlled by agronomical practices,
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but crop losses due to extreme and unexpected weather events are unavoidable. The
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prospect of having to meet food demands for a 34% increase of the global population
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by 2050 is imminent [1]. Crop yields will need boosting, but the higher frequency and
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intensity of drought, heat and cold spells will also require crops that are better able to
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therefore be based on a thorough understanding of the complexity of plant growth and
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maintain productivity under sub-optimal conditions. The concept of “tolerance” and “sensitivity” of plants to abiotic stress situations can be difficult to measure. In model plants like Arabidopsis, tolerance is often measured as “survival”. In crop species like cereals maintenance of “yield” and “productivity” is for economical reasons more important than “survival”. The criteria to evaluate stress tolerance in crop plants must
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developmental processes that ultimately correlate with maintenance of productivity.
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Unfortunately, this knowledge is still evolving.
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5 Progress in cereal yield improvements has generally been slow and is starting to reach
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a plateau, falling short of the annual yield increases required to meet 2050 food
105
demands [2]. In rice and wheat it is estimated that annual rate of yield increase has so
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far been primarily achieved through improved managing practices (mechanisation)
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rather than through breeding and genetic gain [3, 4]. During the last decade significant
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progress has been made in improving our understanding about plant physiology and
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molecular biology and new technologies have placed us now in a better position to
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improve the efficiency of crop breeding. Improved knowledge and advanced new
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technologies may now provide us with an opportunity to improve the speed and
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efficiency of breeding to boost crop yield and abiotic stress tolerance.
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1.2. Plant growth and the environment
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Plants continuously adjust growth and development, growing prolifically when
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conditions are optimal and slowing down, arresting and even reversing growth (e.g.
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abscission, senescence and cell death responses) under sub-optimal conditions - even
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is therefore not surprising that crop productivity attributes (yield, quality) are strongly
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influenced by environmental variability (gene-environment interactions, GxE).
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Consequently, the responsiveness of crop plants to abiotic stresses is equally variable
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and is controlled by complex gene networks with epistatic interactions [5]. In the
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field, crop plants are continuously challenged by a combination of stresses which are
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when conditions are not life-threatening. This bidirectional growth adjustment mechanism is quite remarkable and poorly understood, but it may hold the key for improving abiotic stress tolerance. Plant growth is a measure of environmental input and adaptive capacity to a particular environment; some conditions can be controlled by humans (irrigation, fertilization etc.), but others are at the mercy of the weather. It
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6 often typical for that environment. Breeding activities are usually focused on specific
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target environments, but this approach tends to improve adaptive traits that are
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constitutively present and are relevant for that environment only. This approach may
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have resulted in the loss of genetic variation from current breeding stock that would
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allow the plant to maintain productivity under unexpected and/or more extreme stress
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conditions. To identify germplasm that is better able to maintain productivity under
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more challenging abiotic stress conditions, it will be necessary to increase the
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selection standards and identify germplasm that is able to perform well under stress
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conditions.
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1.3. Can we exploit plant adaptive capacity?
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Plants in general (higher and lower plants) have a staggering capacity to adapt to
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extreme environments and they can be found in most ecosystems of the globe. Some
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grasses and flowering plants can be found on the Antarctic Peninsula [6], resurrection
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plants are adapted to extremely hot and dry conditions [7, 8], while seagrasses are
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stress signalling and metabolic and developmental adaption mechanisms [8, 10].
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Proof-of-concept transgenic approaches can be used to evaluate some of these
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adaptation mechanisms (e.g., cryo- and osmo-protectants) in crop species such as
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cereals. However, this may be difficult to achieve if genes of an entire metabolic
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pathway need to be transferred and it may also compromise important yield and
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land plants that have re-adapted to life in a marine environment, surviving conditions of low light, high salt and anoxia in the sediment [9]. Adaptation of plants to extreme environments requires complex morphological, developmental and metabolic adaptations. Exploring the molecular mechanisms of drought tolerance in resurrection plants and salt tolerance of halophytes has benefited our understanding about abiotic
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7 quality traits. Important morphological and developmental components that contribute
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to abiotic stress tolerance simply cannot be transferred to cereals. Sourcing abiotic
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stress tolerance traits from the available genetic variability in crop species, landraces
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and progenitor species may be a more desirable approach.
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1.4. The virtue of model plants
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A small genome size has been an important criterion for the selection of model plants.
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The simple dicot Arabidopsis has been a workhorse for advancing our understanding
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of various plant biological processes, including plant development and response to
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various abiotic stresses. Comparative genomics is starting to reveal important
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differences between different model systems, suggesting that care is needed when
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extrapolating information from model systems to other plants. For example, some
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genes are missing in Arabidopsis that are present in other plants [11], while other
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genes have diverged and evolved different functions in other plants. The control of
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flowering and flower development differs considerably between eudicots
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has become faster and cheaper, which has made it possible to sequence larger plant
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genomes. In addition to the rice genome, the genome sequences of four other
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cultivated grasses (maize, sorghum, barley and wheat; www.gramene.org) and one
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wild grass (Brachypodium; www.brachypodium.org) are now available, providing a
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wealth of information for comparative genomics studies into the evolution of these
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(Arabidopsis) and monocots (rice, Brachypodium), even though the regulatory genes (e.g. MADS-box genes) identified in Arabidopsis are also present in monocots [1214]. In addition, it has been shown plants that many of the proteins with completely unknown function (POFs; proteins with obscure features) are species-specific and have no homologues in other species [15, 16]. In recent times, sequencing technology
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genomes (synteny, gene loss/conservation, gene divergence). This unstoppable
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progress in sequencing technologies and genomics will ultimately reduce the reliance
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on model systems.
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1.5. Are domesticated plants different?
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Domestication has turned wild ancestor varieties into cultivated crops that have a
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different architecture and look vastly different from their progenitor species (e.g., rice:
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Fig. 1). Selection for desirable traits has affected many plant developmental
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processes, including yield-related traits (seed size and number), seed shattering, seed
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dormancy, photoperiod and flowering time, palatability and overall shape and body
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architecture [17, 18]. Comparative genomics is slowly revealing the effect of
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domestication at the DNA level [19]. Comparison of the wild rice (Oryza rufipogon)
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and cultivated rice (O. sativa japonica) genome sequences reveals significant gene
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loss in the cultivated species [20]. A comparison between domesticated and wild
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tomato revealed genes that underwent positive selection and many genes that showed
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ancestor plants and landraces are often more tolerant to abiotic stresses and this
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genetic variability could be re-introduced in domesticated crops. This process has
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started for cereals such as rice [23] and maize [24] using wide crosses between
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progenitors and interbreeding relatives. In bread wheat, the reconstruction of synthetic
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hexaploids from the respective wild ancestors aims to achieve a similar goal [25].
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shifts in gene expression levels [21]. Some gene deletions, mutations and variation in gene expression may have directly or indirectly affected abiotic stress tolerance. In beans, two DREB2 loci (dehydration-responsive element binding transcription factor) shared high levels of sequence diversity in one bean locus but no variation in the other, suggesting that domestication may have affected one of these genes [22]. Wild
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9 This process can be complicated by the lack of molecular markers for precision
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breeding and the possible introduction of undesirable traits. These problems will be
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discussed in more detail in the following chapter. Comparative genomics could also
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be used to compare adaptation of crop species to abiotic stresses in different
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environments and to compare genetic variability in stress tolerance [26]. The
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difference in growth responses to environmental conditions can also reside in more
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subtle changes in gene functions (e.g., base pair substitutions). Identifying those
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differences will take additional effort.
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2. Genetic approaches for improving abiotic stress tolerance
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2.1. Field or controlled environment phenotyping?
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Controlled environments allow control over occurrence and timing of a stress during
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plant development, as well as its duration and severity. It is also possible to
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investigate the effect of a single abiotic stress at a time. This is a significant advantage
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over field studies, where environmental conditions are typically variable and
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unpredictable. However, field environments remain difficult to simulate in growth chambers, even though technology is improving [27]. Air humidity, variation of light quantity and quality throughout the day (blue and red light enrichments at sunrise and sunset, respectively) control important plant physiological processes, yet are often
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ignored in controlled environments. Additionally, heat load caused by light bulbs can
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sometimes cause heat stress problems [28, 29] and soil drought and frost events are
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extremely hard to simulate in controlled environments. In the field, environmental
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changes that cause stress in plants most often occur over several hours (in the case of
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heat during the day or frosts overnight) or even over several days (in the case of
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10 drought). These gradual changes are difficult to replicate in controlled environments
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and stresses are often imposed abruptly, causing a shock situation by not allowing the
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plant to gradually adapt to the stress. Additionally, growing plants in pots that are too
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small affects root development, which in the case of drought stress affects the severity
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and the speed with which the stress is imposed [30, 31]. Despite these issues,
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controlled environments are the only tool that allows the comparison between
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different stress responses independently and when used with due care and reasonable
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attention, they can help to analyse stress responses in terms of sensitivity of different
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plant developmental stages and effect of treatment duration and severity. This is very
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important for designing phenotyping methods and to make sure that lines with
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different flowering times are stressed at the same developmental stage when
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comparing different lines. Communication with breeders and farmers can identify
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germplasm that performs better/worse in field stress conditions and this material can
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then provide an excellent benchmark to establish “realistic” stress treatment
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conditions that give identical rankings in growth chambers. It is equally important to
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replicate controlled environment results under field conditions.
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flowering time [32, 33]. This is particularly troublesome when screening large
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populations that segregate for flowering time genes. Flowering time is important for
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optimizing grain yield in wheat, as flowering too early can result in cold and frost
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damage and late flowering can result in poor yields due to drought and heat stress [34,
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35]. Manipulating flowering time can also have adverse effects on yield; early-
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2.2. Avoidance and escape reactions Selecting germplasm that is tolerant to abiotic stress under field conditions is compromised by escape or avoidance responses. In wheat, the damage caused by terminal drought can be alleviated by escaping drought through alteration of
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11 maturing varieties have less chance to accumulate biomass compared to late maturing
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varieties, which indirectly affects grain yield in wheat [36]. Plants can also avoid
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stress damage by adapting metabolic activity and growth rate. Accelerated growth
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requires faster metabolism and mobilization of resources, while slowing down
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metabolism and growth saves vital resources for passive survival of abiotic stress
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conditions. Plants can use any of these tactics for survival in a particular environment.
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In rice, ethylene response transcription factors (ERF) play an important role in
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flooding tolerance [37, 38]. The ERF genes SNORKEL1 and 2 are important in deep-
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water rice varieties, where elongation growth and outgrowing rising water levels
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(escape response) is important for longer-term survival and grain production. In
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contrast, another ERF-family member, SUBMERGENCE-1A (SUB1A), is important
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in rice varieties that have to survive occasional short-term submergence and flooding
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by transiently keeping growth and metabolic activity quiescent. Analysis of the
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molecular basis indicates that the plant hormone ethylene plays an important role in
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regulating elongation growth under stress conditions. The example of flooding
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tolerance in rice illustrates the importance of regulating plant growth rate and
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2.3. Constitutive vs. inducible stress tolerance
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Selection for yield-related traits in field environments has dominated crop breeding.
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Traits such as growth vigour, biomass accumulation, harvest index (reproductive
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biomass), stem carbohydrate levels, tiller number, plant height, water use and
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metabolic activity under stress conditions. Avoidance and escape reactions generally provide protection against abiotic stress through adjustment of growth rate and developmental processes. Understanding the molecular basis of these processes is important for understanding abiotic stress tolerance.
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12 transpiration efficiency, carbon isotope discrimination and root depth are important in
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cereal breeding. These traits, together with improved management practises, have
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improved vegetative growth of cereal crops, resulting in higher yield and productivity
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[32, 33, 39-41]. Interestingly, for Australian wheat the yield gain was found to be
281
proportionally higher in the driest years compared to the better years even though
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those traits were not specifically targeting drought conditions [4]. This illustrates that
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yield-based traits that boost vegetative growth, biomass accumulation and water use
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efficiency generally benefit plant growth and resilience and contribute to higher yields
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under abiotic stress conditions [3-5, 41, 42]. However, unexpected and more extreme
286
abiotic stress conditions still result in massive yield penalties, indicating that growth
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vigour and biomass accumulation does not necessarily result in a better capacity to
288
maintain that yield potential when growth conditions during reproductive
289
development are not favourable [5]. It is clear that an additional tolerance mechanism
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is needed to convert or maintain the yield potential generated during the vegetative
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stage to successful reproductive development and grain productivity. Sensitivity of
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crops to various abiotic stresses are usually associated with phenotypes that are
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compromised as growth repression saves resources for later growth when conditions
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have returned to normal [43]. Even when this occurs, yield can never be recovered
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because it is too late in the growing season and previously established biomass and
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productivity has been lost. In many crops, growth repression can be an exaggeration
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indicative of growth arrest, generally including leaf senescence or cell death, severe tissue necrosis (e.g., frosts and salinity), stomatal closure and arrest of photosynthesis [5]. At the reproductive stage, pollen sterility and abortion of grain development are similar growth repression phenotypes that cause major yield losses in cereals. Under shorter-duration or unexpected stress periods, survival of the plant is often not
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13 or an overly sensitive response to stress conditions. There may therefore be an
303
opportunity for increasing the threshold level at which growth repression takes place
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in response to stresses, in order to maintain growth and productivity for as long as
305
possible. Interestingly, the two flooding tolerance mechanisms described earlier for
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rice (section 2.2: growth acceleration versus metabolic quiescence) may be more
307
widely applicable for other abiotic stresses and the molecular understanding of
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flooding tolerance may stimulate research on other abiotic stresses. An intriguing
309
question is whether avoidance and escape strategies should also be seen as part of the
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plants overall strategy to tolerate abiotic stresses.
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To identify crops that maintain growth and yield potential under adverse growth
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conditions it is necessary to complement constitutively expressed yield traits with
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traits that are induced and specifically expressed under stress conditions. Identifying
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more stress-induced traits will have a positive effect for breeding stress-tolerant crops,
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but also for improving our understanding of the underlying physiological and
317
molecular mechanism. Under stress conditions, plants require mechanisms to protect
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(irrigated, rain-fed, rainout shelter plots to compare water stress conditions) [44].
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However, controlled environments offer significant advantages if precision-
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phenotyping is required (see section 2.1). Leaf senescence is a stress-induced
326
phenotype and has received a lot of attention as a stress-induced trait. Selecting for
318 319 320 321
their cellular machinery, metabolic adaptations and their capacity to sustain growth and development (see section 3). Selection for stress-inducible traits is more difficult to achieve, considering the unpredictability of field conditions and interference of avoidance and escape reactions. Field plots can be selected to target certain abiotic stresses (drought, heat, frost) or can be artificially modified to create stress conditions
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14 delayed foliar senescence (stay-green) and maintenance of stomatal conductance,
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transpiration and photosynthesis during stress conditions are relatively easy
329
phenotypes to score [45]. Significant improvements in drought tolerance have resulted
330
from proof-of-concept transgenic approaches manipulating cytokinin levels,
331
confirming that this trait contributes to stress tolerance [46]. Leaf rolling is another
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distinctive and easy to score heat and drought-induced phenotype. Reduction in leaf
333
area prevents transpiration and water loss and genetic variation for leaf rolling is
334
available in wheat and rice. However, leaf rolling does not always correlate with
335
drought tolerance, suggesting that it could be an escape rather than tolerance
336
mechanism [47, 48]. Osmotic adjustment is an inducible drought adaptation
337
mechanism that maintains leaf water potential through the synthesis of osmotically
338
active substances [44, 50]. Osmotic adjustment delays leaf senescence and leaf
339
rolling, maintains stomatal conductance and turgor pressure, thereby sustaining
340
growth under drought conditions [51]. Despite its importance, osmotic adjustment has
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so far remained a difficult trait to phenotype [52]. Many abiotic stresses cause pollen
342
sterility and loss of fertility and grain yield in cereals [53, 54]. A phenotyping method
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building up a higher yield potential, stress-inducible traits are essential to sustain that
349
higher yield potential under adverse environmental conditions to maintain growth and
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reproductive development.
343 344 345 346
for cold and drought-induced pollen sterility was established using controlled environments [55, 56] and the plant hormone abscisic acid (ABA) was shown to play a role in stress-induced pollen abortion [53, 57, 58]. Stress-inducible traits are less likely to have negative effects on productivity of crops under non-stress conditions. While yield traits that improve vegetative plant growth and development contribute to
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15
2.4. QTL analysis in the genomics era
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Identifying genetic variation for abiotic stress tolerance in crops requires the tedious
354
and laborious process of establishing linkage maps using DNA-based molecular
355
markers: restriction fragment length polymorphism (RFLP), amplified fragment
356
length polymorphism (AFLP), random amplification of polymorphic DNA (RAPD),
357
cleaved amplified polymorphic sequences (CAPS) and simple sequence repeat (SSR,
358
microsatellite) markers. In the last decade, the shift to high-throughput technologies
359
such as Diversity Arrays (DArT; [59]) and Single Nucleotide Polymorphism markers
360
(SNP; [60]) has made the construction of high density genomic maps easier. The
361
identification of SNP markers was boosted by the availability of the genome sequence
362
for many crop species. 160,000 SNPs were identified in the non-repetitive genome
363
fraction of 20 different rice varieties [61]. The availability of annotated genome
364
sequences and accurate high density SNP maps makes it easier to identify candidate
365
genes within QTL (Quantitative Trait Loci) regions [61, 62] and the lowering in
366
sequencing costs has made it possible to carry out genotyping by sequencing (GBS),
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which further facilitates fine-mapping QTL [63]. Genome-wide association studies
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(GWAS, [64]) also benefit from high density SNP maps and can be used for mapping abiotic stress tolerance loci. In wheat, the development of multi-parent advanced inter-cross populations (MAGIC) provides a powerful tool for mapping QTL [65].
Abiotic stress tolerance is typically controlled by a large number of QTL with
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epistatic interactions and low phenotypic contribution and heritability. A
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comprehensive overview of QTL for various abiotic stress-related traits can be
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accessed at the Gramene and Plant Stress websites (archive.gramene.org/qtl/;
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www.plantstress.com/files/qtls_for_ resistance.htm). Abiotic stress QTL mapping and
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16 genomic selection (GS) has so far not led to markers for routine use in marker-
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assisted selection (MAS) for abiotic stress tolerance [41, 66, 67]. With the bottleneck
379
of genotyping removed, mapping of abiotic stress tolerance loci will depend on the
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availability of reliable traits for phenotyping. The case of salinity tolerance in rice is a
381
good example that QTL analysis can lead to identification of candidate genes
382
provided that reliable phenotyping methods are available [68].
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2.5. Next generation phenotyping methods
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Considering the difficulties involved in direct selection for abiotic stress tolerance in
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field or controlled environments, shifting from “observable” to molecular or
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secondary traits that are highly correlated with abiotic stress tolerance, may improve
388
reliability of phenotyping procedures [69]. Our understanding about the physiological
389
and molecular basis of stress responses has improved and technological progress in
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the last decade has provided opportunities for high-throughput phenotyping.
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Metabolomics is a promising technology that can now be used at a scale that is
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used to quantitatively and qualitatively evaluate components of cellular protection.
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Hormone measurements can be used as indicators of developmental responses in
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sensitive and tolerant germplasm (senescence or growth). Proteomics can also be used
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for phenotyping abiotic stress responses, but protein expression profiling can be
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technically more challenging (e.g., resolution limits of two-dimensional
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compatible with population screening and mQTL mapping. This technology was used to identify genes controlling several metabolites and quality-related traits [70-72], but can also be used to map mQTL for metabolite changes associated with abiotic stresses [73, 74]. Measuring diagnostic metabolites can be informative about the physiological state of plant tissues in response to drought, heat and cold and metabolomics can be
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17 electrophoresis and detection limits of mass spectrometry) and is harder to adapt for
403
high throughput screening [75]. The development in recent years of various digital
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imaging technologies has added even more opportunities for phenotyping [67, 76].
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Non-destructive imaging can measure canopy properties that contribute to biomass
406
accumulation, as well as stress-related traits (photosynthesis, transpiration and leaf
407
senescence). This technology can be applied for high-throughput screening under
408
field or controlled environments [77-79]. New generation phenotyping technologies
409
are powerful but require some knowledge about the molecular and physiological basis
410
of abiotic stress phenotypes and the questions to be addressed.
an
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3. Components of abiotic stress responses
413
3.1. The power of transcriptomics
414
While GxE interactions are considered problematic and something to avoid in plant
415
breeding, molecular biologists have used differential gene expression of stress-treated
416
versus unstressed plant material as a standard method to study abiotic stress
418 419 420 421
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responses. In the recent decade, large-scale transcriptome analyses using microarrays and more recently new generation sequencing technologies (RNA-seq) have proven to be a powerful tool for identifying genes and cellular processes that are affected by abiotic stresses [80]. A massive amount of transcriptome information for different stresses and plant species is currently available in public databases.
422 423
Transcriptome information is starting to reveal how plants respond to various abiotic
424
stresses, but the full potential is still unexplored [81]. Currently, about 40% of the
425
proteins encoded by a eukaryotic genome have an unknown function [82]. It is
Page 17 of 65
18 estimated that between 18 and 38% of the eukaryotic proteome consists of proteins
427
without any defined domain or motif [15]. Interestingly, when comparing the
428
Arabidopsis and rice proteins with totally unknown features (POFs) nearly half were
429
found to be species-specific and had no homolog in the other genome [16].
430
Obviously, identifying the function of these proteins will require species-specific
431
studies and this will be a major challenge. Finding the exact physiological function for
432
members of large gene families (e.g., transcription factors) can also be a complicated
433
and time-consuming process. In model plants such as Arabidopsis and rice, insertion
434
mutagenesis using T-DNA and transposons can be used to identify gene functions and
435
support the gene annotation process. In rice, about 60.49% of the nuclear genes have
436
been tagged with T-DNA or Tos17 transposon insertions [83], but the functional
437
characterization of these insertion mutants remains a major effort. In addition, the
438
function of some genes for which the insertion mutant phenotype is lethal cannot be
439
investigated. Another limitation is gene redundancy and lack of a clear phenotype for
440
some mutations. Over-expression and RNAi technology can also be used to reveal the
441
function of candidate genes in plants that can be transformed. Transcriptome analysis
446
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447
triggering early developmental responses, are likely to be present all the time and
448
simply require activation by upstream signals (e.g., phosphorylation). Identifying
449
those genes will require more fundamental approaches, ideally using model systems
450
in the first place (e.g., using mutagenesis approaches).
442 443 444 445
needs support from other technologies to speed up the identification of unknown gene functions. A systems biology approach combining transcriptomics with proteomics and metabolomics can help this process [84, 85]. It is also important to realize that transcriptomics focuses on differentially expressed genes, while some genes that play an important role in the early stress signal perception and transduction events, or those
Page 18 of 65
19
3.2. First things first: establishment of cellular protection
452
Bacteria, yeast and animals have a general cellular stress response mechanism that
453
protects essential macromolecules (DNA, proteins and lipids) against oxidative stress
454
and removes damaged cells using a cell death response. The conservation of this
455
response in different life forms suggests that it is an ancient protection mechanism
456
against general stress situations. The minimal cellular stress response proteome
457
consists of 44 proteins with known function, including molecular chaperones (e.g.
458
heat shock proteins), various enzymes that repair DNA damage and various proteins
459
that protect against oxidative stress and reactive oxygen species (ROS), such as
460
superoxide dismutase and glutathione antioxidant defence pathway proteins [86].
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Plants also activate a cellular protection mechanism in response to various stresses.
463
Little is known about macromolecule protection in plants, but chaperone proteins (e.g.
464
heat shock proteins) are induced by all abiotic stresses and their importance is
465
illustrated by the fact that an Escherichia coli gene encoding a cold shock protein that
466
functions as RNA chaperone can significantly improve tolerance to multiple stresses
468 469 470 471
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(cold, drought, heat) in transgenic rice and maize [87]. The transformation of light into chemical energy during photosynthesis and the mitochondrial electron transport chain produce damaging free radicals [88]. Regulation of intracellular redox homeostasis has been shown to control important metabolic pathways such as photosynthesis [89, 90] and is also important for regulating root and leaf
472
developmental processes [91, 92]. Superoxide, hydrogen peroxide and hydroxyl
473
radical production is induced in response to abiotic and biotic stresses and results in
474
activation of genes encoding ROS-detoxifying enzymes [93, 94]. Active oxygen
475
species such as hydrogen peroxide are generally considered as local and systemic
Page 19 of 65
20 signals in response to various stress situations [95, 96]. This indicates that plants may
477
have turned this early stress defence mechanism into a systemic warning signal to
478
protect different plant parts. Some oxidative stress-related genes are expressed in cells
479
associated with the vascular bundles [97], which is compatible with a systemic
480
signalling function of ROS [98-100]. Resistance to the ROS-generating herbicide
481
paraquat in Conyza bonariensis is correlated with a highly expressed constitutive
482
ROS detoxification system and cross-tolerance to environmental oxidants [101, 102].
483
Paraquat resistance in wheat and barley has been correlated with tolerance to water
484
stress and paraquat treatment has been evaluated as a screening system for abiotic
485
stress tolerance [103, 104]. Overexpression of peroxidase, catalase, superoxide
486
reductase and superoxide dismutase in transgenic plants has resulted in improved
487
tolerance to cold, drought, salinity and heat stress [105-108], while an ascorbate
488
deficient mutant in Arabidopsis caused a stress-sensitive phenotype [109]. Cellular
489
protection in plants may also function as an intracellular and systemic signal to
490
regulate developmental processes. As a stress defence mechanism it may be essential
491
for all other aspects of the stress response to function and it could therefore act as an
493 494 495
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“enabling” mechanism that needs to be activated before other aspects of stress responses (biotic and abiotic) can be established (Fig. 2).
3.3. Taking care of metabolic adjustment
496
Changes in plant growth and development under abiotic stress conditions must be
497
associated with metabolic activity to provide the energy required to establish the
498
response. Firstly, the altered cellular environment requires changes in the cellular
499
machinery to be put in place; adaptations of translation initiation and protein folding
500
are commonly observed in stress-induced transcriptomes [110, 111]. Then, specially
Page 20 of 65
21 adapted metabolic proteins are induced early in the stress response (Fig. 2). Many
502
abiotic stresses shut down photosynthesis, while photosynthates are a crucial source
503
of energy. Sugars are transported from source to sink tissues via the phloem and are
504
important signals for growth and development, as well as response to various abiotic
505
stresses. Sugar signalling and metabolism are therefore tightly linked to growth
506
responses [112]. ABA regulates stomatal conductance and photosynthetic activity,
507
causing vegetative growth retardation. This has been shown to contribute to
508
vegetative stage abiotic stress tolerance, but this growth repression also has a negative
509
effect on reproductive processes [113]. Abiotic stresses repress the sucrose cleaving
510
enzyme cell wall invertase in anthers, preventing hexose supply for pollen
511
development and causing pollen sterility. ABA accumulation was shown to directly or
512
indirectly repress cell wall invertase expression. Tolerant wheat and rice germplasm
513
displayed different anther ABA homeostasis, maintaining lower ABA levels than
514
sensitive lines in response to cold and drought stress [55-57, 113]. Sugars and ABA
515
are known to regulate ethylene and senescence responses [114]. Sugars are an
516
important growth signal in plants and are therefore tightly connected with the decision
521
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501
522
osmotic stresses such as drought, cold and salt stress and are tightly integrated with
523
signalling pathways for sugars, essential nutrients (nitrogen) and various hormones
524
[118-120]. The yeast SnRK (Sucrose non-fermenting related kinase) related protein
525
kinases KIN10 and KIN11 play a central role in coordinating sugar, stress and
517 518 519 520
to grow or repress growth and respond to abiotic stress (Fig. 2). The glycolytic enzyme hexokinase (HXK) is a cellular sugar sensor that cross-talks to several phytohormones [115]. Other cellular components involved in regulation of metabolism in plants show some similarity to yeast. The Mitogen-Activated Protein Kinase (MAPK) [116, 117] and the Salt Overly Sensitive (SOS) pathways respond to
Page 21 of 65
22 developmental signals with metabolic pathways, activating gene expression via bZIP
527
transcription factors [121, 122]. The General Control Non-repressible related protein
528
kinase (GCN-2) phosphorylates translation initiation factor 2 (eIF2α) and is able to
529
sense free amino acid levels, respond to osmotic stresses and control protein synthesis
530
[123, 124]. Both SnRK1 and GCN-2 regulate nitrate reductase and nitrogen
531
metabolism [120, 121]. Further research is required to establish how this complex
532
metabolic regulation mechanism is controlled by environmental stimuli. The
533
conservation of the kinases that regulate fundamental metabolic pathways between
534
plants, yeast and animals illustrates their evolutionary importance.
an
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535
3.4. Do abiotic stress response pathways overlap?
537
It has been demonstrated that treatment with one abiotic stress can provide “cross-
538
tolerance” or “hardening” to other stresses, including biotic stresses [125, 126]. Pre-
539
treatment of plants with the stress hormone ABA has a similar effect [127-129]. This
540
already suggests that there must be some functional overlap in the signalling and
545
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536
546
pollen fertility, induction of osmo-protectants by drought, cold and salinity) are also
547
shared by different stresses. Communication between sink and source tissues is
548
especially important under abiotic stress conditions when growth can be limited by
549
available resources. To fully understand the impact of abiotic stresses on plant growth
541 542 543 544
response pathways of abiotic stresses. Osmotic stresses (drought, cold, salinity, heat) involve ABA and are therefore expected to share common components. Furthermore, transcriptome analyses have confirmed that early macromolecule and oxidative stress protection is recruited by most stresses and is a general stress response (Fig. 2). Some developmental and metabolic responses (e.g., growth adaptation, leaf senescence,
Page 22 of 65
23 550
it is essential to further unravel the relationships between metabolism and
551
developmental processes.
552 Due to gene redundancy, different gene copies encoding proteins with the same
554
function can be activated under different stresses, suggesting that overlap between
555
different stresses could be larger at the protein level than at the transcript level. In
556
economical terms, it seems logical that plants will share the response to the initial
557
threat and mount stress-specific responses once the general response has created the
558
environment to make this possible (Fig. 2). A shared initial stress response may not
559
require many genes and some may have so far remained undetected in differential
560
gene expression studies. Regulation at the protein level, such as targeted protein
561
degradation using the ubiquitin proteasome, is commonly used by plant hormones to
562
regulate downstream developmental signalling [130]. It is therefore possible that a
563
rather small - but critically important - part of the overlap between different abiotic
564
stress responses has so far escaped detection.
cr
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553
570
arrest is taken in this early response mechanism and it is an important factor for
571
determining productivity and abiotic stress tolerance in crops. Selection for adaptation
572
to specific environments and productivity traits has affected many developmental
573
properties and may also have modified the early response mechanism to stress (Fig.
574
2). Selection against seed dormancy may have affected homeostasis of hormones that
566 567 568
3.5. Selection for tolerance to multiple abiotic stresses Genetic diversity for abiotic stress tolerance is more likely to occur in the early response mechanism than in the stress-specific responses that depend on the initial response (Fig. 2). The decision to continue growth or induce senescence and growth
Page 23 of 65
24 play a role in stress tolerance (ABA, GA). Adaptation to seasonal conditions and
576
different environments in cereals has modified important growth processes such as
577
duration of photosynthesis, adaptation to day-length and altered rate of leaf
578
senescence, which may also have changed the interaction between plant hormones
579
(ethylene, cytokinins). The stay-green trait has therefore been thought of as a potential
580
domestication trait [45, 131]. Analysis of stay-green QTL (e.g., sorghum) could lead
581
to positional cloning and identification of new genes involved in this process [45,
582
132].
us
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575
an
583
In nature, frequent exposure to a combination of stresses may have selected a shared
585
genetic adaptation mechanism to those stresses. This may be the case for heat and
586
drought stress which often occur at the same time in field conditions [126, 133]. It
587
therefore makes sense to select germplasm that is tolerant to more than one abiotic
588
stress [126], especially since different abiotic stress responses may already share a
589
common initial response mechanism (Fig. 2). Germplasm that establishes the initial
590
response successfully may also be better able to establish a stress-specific response
595
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584
596
wheat lines that are tolerant to multiple abiotic stresses individually (drought, heat,
597
shading and cold). QTL mapping using this tolerant germplasm can also be used to
598
identify overlapping general stress-response QTL, as well as QTL that are specific for
599
different stresses. Obtaining high levels of abiotic stress tolerance may ultimately
591 592 593 594
(Fig. 2). However, selecting germplasm that is tolerant to more than one stress using the combination of those stresses may be difficult to achieve because of quantitative and qualitative differences in tolerance to the combination of stresses and the difficulty to choose physiologically relevant selection conditions for the combination of stresses. We are currently using a step-wise selection procedure to first identify
Page 24 of 65
25 require combining both general stress response and stress-specific QTL. However, for
601
some traits it may be difficult to obtain tolerance to a combination of stresses; some
602
traits for drought (stomata closed to prevent water loss) and heat stress (open stomata
603
to reduce leaf temperature) are mutually exclusive [126].
604
ip t
600
3.6. Transgenic approaches for abiotic stress tolerance
606
It is common practice in molecular biology to use proof-of-concept transgenic
607
approaches (over-expression, RNAi) to evaluate candidate genes for their effect on
608
abiotic stress tolerance. Many genes have indeed been shown to improve abiotic stress
609
tolerance ([134]; see Plant Stress website for a comprehensive listing:
610
www.plantstress.com/ files/abiotic-stress_gene.htm). These include transcription and
611
regulatory factors, osmo-protectants, hormone and oxidative stress-related genes,
612
molecular chaperones, transporters and various metabolic genes. Abiotic stress
613
tolerance for most of these genes was evaluated under controlled environment or
614
glasshouse conditions, using model systems such as Arabidopsis or tobacco and some
619
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605
620
tolerance may also be a contributing factor; in model plants tolerance is usually
621
measured as survival under vegetative stage stresses, while in crops maintenance of
622
productivity during reproductive stage stresses is important [136, 137]. The choice of
623
promoter to drive transgene expression is also important. Strong constitutive
624
promoters lead to ectopic expression of a transgene, potentially causing adverse
615 616 617 618
were also evaluated in cereals (rice, wheat, barley, maize). Relatively few transgenic lines have so far made any impact for improving field abiotic stress tolerance [135]. Potential explanations are that the field environment is much harsher, transgenes only partially improve the abiotic stress response or they improve response to one stress and not a combination of stresses. Differences in evaluation criteria for abiotic stress
Page 25 of 65
26 secondary effects on crop productivity. CBF/DREB transcription factors can improve
626
osmotic stress tolerance but result in stunted growth when using constitutive
627
promoters [138]; plants look normal when a strong drought-inducible promoter is
628
used that expresses the transgene only when required [139]. The quantitative and
629
qualitative properties of the promoter driving a transgene may be particularly critical
630
in the case of transcription factors, hormone metabolic and signal transduction genes.
631
Using Arabidopsis as a model system it may be extremely difficult or impossible to
632
fully evaluate and predict potential adverse effects in crop species [139]. In the case
633
of multigene families it is often difficult to find out which gene to use for
634
transformation. For instance, only a few aquaporin gene family members are affected
635
by stress and lead to improvement of drought tolerance in transgenic plants [140]. For
636
large transcription factor families, trial and error approaches can identify which gene
637
has a positive effect on stress tolerance [141]. Some transgenic approaches may result
638
in morphologically different plants where stress phenotypes are simply delayed (e.g.,
639
smaller leaf area reduce transpiration under drought), giving transgenics an unfair
640
advantage [142]. Manipulation of cytokinin levels using a stress-induced promoter led
645
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625
646
multiple stresses (cold, drought and heat) in field experiments [88], suggesting that
647
focusing on the manipulation of the top of the stress signalling cascade using general
648
stress responsive genes may yield positive results.
641 642 643 644
to delayed senescence and improved drought tolerance in rice under glasshouse conditions [143]. It is possible that these transgenic lines may also perform well under field drought conditions, considering the field experience with stay-green plants. Interestingly, transgenic rice and maize plants expressing an E. coli cold shock protein
that acts as RNA chaperone in cellular protection resulted in improved tolerance to
649
Page 26 of 65
27
4. Coordination of growth responses to abiotic stress
651
4.1. Do plants have brains?
652
How are the early responses to abiotic stresses orchestrated by signals from the
653
environment? Higher animals are mobile and react to stress by escaping
654
environmental challenges. The brain processes environmental signals via the central
655
nervous system and regulates this mobility and escape reaction. The flexibility of
656
plant development in response to environmental change indicates that they have an
657
efficient systemic signalling mechanism that coordinates and orchestrates the
658
response to adverse environmental conditions. The plant vascular system bears some
659
resemblance to an animal central nervous system, sparking some speculation that
660
plants have a cellular communication mechanism similar to animals [144]. Specific
661
proteins known to play a role as neurotransmitters in animals (e.g., glutamate
662
receptors, 14-3-3 proteins) are also encoded in plant genomes but they acquired
663
different functions when plants evolved into multicellular organisms. The vascular
664
system plays an important role in coordinating growth and development between the
666 667 668 669
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650
different plant parts [145], but the signalling mechanism is vastly different to that of animals. Plants have evolved their own systemic signals to drive growth and development (Fig. 2). Being photosynthetic organisms, they use photosynthates and the capacity to produce sugars as a resource signal for growth. They also adapted reactive oxygen species as a signal for abiotic stress. Plants have evolved their own
670
hormone signals, which are totally unlike animal hormones, to signal developmental
671
and growth responses. An emerging theme in plant biology is the observation that
672
many genes involved in hormone synthesis and signalling, e.g. those involved in ABA
673
synthesis and signalling [146, 58], are expressed in vascular parenchyma cells. This
Page 27 of 65
28 allows rapid signal perception and distribution via the vascular system, similar to a
675
nervous system but at a slower pace. Environmental signals can therefore be sensed in
676
any plant part and quickly spread throughout the plant, suggesting that plants have
677
essentially obviated the need for a central nervous system. Despite its importance, the
678
signal transmitting function of the vascular system still needs to be unravelled [147].
679
Understanding of how the signals (hormones, ROS, metabolites) themselves work is
680
gradually emerging. Auxins can be transported all over the plant using directional
681
efflux carriers and long-distance transporters and tissue-specific response mechanisms
682
make it possible to mount different auxin responses in different plant parts [148].
683
These different plant parts are pre-programmed to react differently to plant hormone
684
signals, explaining how environmental signals can have different but coordinated
685
responses. Hormonal signals therefore form an important link between the
686
environment and developmental processes. Plant evolution and global diversity is
687
testimony that plants have evolved efficient systems to manage and adapt to
688
environmental challenges.
cr
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693
Ac ce p
689
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674
694
development and have been implicated in abiotic stress responses. A lot of progress
695
has been made in recent years in understanding their function. Plant hormones can be
696
growth-retarding (ABA, ethylene, jasmonic acid) or growth-promoting (auxin,
697
gibberellic acid, cytokinin). Two recently discovered plant hormones, brassinosteroids
698
[149] and strigolactones [150] act in conjunction with auxins and can be classified as
690 691 692
4.2. Growth inhibition responses The key to understanding abiotic stress tolerance resides in understanding the plant’s capacity to accelerate/maintain or repress growth. Interaction between plant hormones must play an important role in this phenomenon. Most plant hormones play a role in
Page 28 of 65
29 growth promoting hormones, while salicylic acid functions in plant defence responses
700
to pathogens [151]. The stress hormone ABA is implicated in stomatal closure and
701
regulation of plant water balance, which impairs photosynthesis and restricts growth
702
[113]. ABA levels are up-regulated in response to osmotic stresses (drought, cold,
703
salinity) and heat stress. Higher ABA levels improve stress tolerance at the vegetative
704
level, but there is a compromise at the reproductive level. QTL analysis in maize
705
indicated that lines with higher root ABA levels had lower grain yield [152] and our
706
own work demonstrated that lower ABA levels in stressed anthers was correlated with
707
better cold and drought tolerance, as well as maintenance of anther sink strength in
708
rice [58]. The ABA signalling pathway interacts with other hormones and sugar
709
signalling via the SnRK network [98, 123]. ABA’s restriction of photosynthesis and
710
photosynthate allocation to sink tissues may help in shorter periods of abiotic stress,
711
but is destructive under longer term stress conditions such as terminal drought. The
712
opposing effect of ABA on vegetative and reproductive structures indicates that it is
713
important to understand the effect of abiotic stress during plant development. The
714
success of transgenic approaches for manipulation of abiotic stress tolerance will
719
Ac ce p
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cr
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699
720
tapetum [153, 154]. External application and stress-induced accumulation of ABA
721
results in senescence, but the role of ABA in this process is still unclear. ABA may
722
interact with the oxidative stress response that protects against senescence [155], but
723
may also cause senescence via interaction with ethylene. The role of ethylene in
715 716 717 718
depend on carefully targeting the control of ABA homeostasis to particular tissues and growth stages.
Growth repression under abiotic stress conditions is associated with induction of leaf senescence (Fig. 3) or programmed cell death responses in tissues such as the anther
Page 29 of 65
30 inducing leaf senescence and inhibition of root elongation has been well investigated.
725
Antisense repression of ethylene biosynthesis inhibits senescence, and the limitation
726
of ethylene production has in many cases resulted in improved abiotic stress tolerance
727
[156]. Ethylene can induce the biosynthesis of the growth-promoting hormone auxin
728
in a tissue-specific manner [157]. The role of ethylene can therefore also be growth-
729
promoting; low light (etiolation) and shading conditions cause elongation growth in
730
shading-sensitive plants [158]. Ethylene is therefore in a unique position to control
731
plant developmental processes: it can act as an inhibitor of growth, but also as a
732
growth promoter (Fig. 4).
an
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724
733
Jasmonic acid can also induce senescence. In Arabidopsis, jasmonate-induced
735
senescence involves induction of the transcription factor WRKY57, which is
736
repressed by the growth hormone auxin [159]. In addition, jasmonate induces
737
expression of ICE (Inducer of CBF Expression), thereby promoting freezing tolerance
738
in Arabidopsis [160]. Ethylene and jasmonate can regulate each other’s homeostasis
739
via feedback regulation, producing a fine balance between growth repression
743
Ac ce p
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734
744
Cytokinins counteract the effect of ethylene, preventing senescence and stimulating
745
sugar metabolism and sink strength. Over-expression of the cytokinin biosynthetic
746
gene isopentenyl transferase has been used to produce plants that show delayed
747
senescence (stay-green trait), increased biomass production and improved stress
748
tolerance [45, 131]. However, the stay-green trait is not always associated with
740 741 742
(jasmonic acid) and growth stimulation (ethylene).
4.3. Growth stimulation responses The growth hormone group of cytokinins plays a role in controlling cell division.
Page 30 of 65
31 749
increased yield and productivity [131], suggesting that increased cytokinin levels
750
benefit vegetative growth but not reproductive development.
751 Gibberellins (GA) play a crucial role in the promotion of plant elongation growth. In
753
the absence of GA, elongation growth is restrained by DELLA nuclear proteins. In the
754
presence of GA, DELLA proteins bind to the GA-GID1 receptor complex, targeting it
755
for degradation by the ubiquitin-26S proteasome and thereby activating GA signalling
756
and elongation growth [161]. Some DELLA mutants are unable to bind the GA-GID1
757
complex, causing it to escape proteasome degradation. This suppresses elongation
758
growth, causing a semi-dwarf phenotype. Other DELLA mutants abolish its
759
repression activity, resulting in a tall stature (slender); these mutants are also male
760
sterile, suggesting that DELLA proteins play a role in pollen development [162].
761
Mutations in GA biosynthesis genes and DELLA proteins with a semi-dwarf
762
phenotype increase yield in cereals and have formed the basis of the Green
763
Revolution [163]. However, some GA-insensitive dwarf mutants in wheat (reduced
764
height; Rht) also have reduced pollen viability, which has been associated with
769
Ac ce p
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752
770
CBF1 was shown to induce DELLA gene expression and activate GA catabolic genes,
771
causing growth repression [168, 169]. Stress-induced accumulation of ABA
772
antagonizes GA action by controlling DELLA activity [170]. In addition, DELLA
773
proteins play a role in mounting a protective response to oxidative stress [169, 171].
765 766 767 768
reduced tolerance to abiotic stresses such as heat and drought [162, 164]. Interestingly, the growth-stimulation of GA can be counteracted by environmental stresses and hormones such as ethylene and auxins, which affect the growth restraining activity of DELLA proteins [165-167]. In Arabidopsis, the CBF/DREB cold-inducible transcription factors activate cold acclimation and freezing tolerance.
Page 31 of 65
32 774
The DELLA proteins obviously form a hub of hormonal and environmental
775
interactions that determine continuation or repression of growth in function of
776
environmental cues [172].
ip t
777
4.4. An old legend born again: auxins
779
Auxins were the first plant hormone to be discovered. The growth-promoting
780
properties of auxins have gained increasing prominence in recent years because of
781
their role in regulating development and response to abiotic stress. Auxins are
782
synthesized in the shoot apical meristem and are transported to neighbouring tissues
783
and over longer distances using efflux carriers and polar transporters respectively.
784
Auxins stimulate root growth and other tissue-specific responses throughout the plant
785
such as leaf and fruit senescence [148]. In Arabidopsis this requires cross-talk with
786
jasmonic acid signalling and the transcription factor WRKY57 [161, 173, 174].
us
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d
One of the oldest known effects of auxins is the control of apical dominance and
793
Ac ce p
788
te
787
cr
778
794
have a role in stamen development and are actively synthesized in the anther,
795
controlling pollen development and anther dehiscence [178]. Apical dominance may
796
play an important role in promoting reproductive development and grain yield in
797
cereals. Auxins are synthesized in the anthers towards maturity where they play a role
798
in anther senescence [178, 179]. At the start of reproductive development in cereals
789 790 791 792
shoot branching (tillering in cereals). Cutting the main stem of a plant removes the apical meristem where auxins are made, resulting in increased branching. The branching response involves interaction with strigolactone and requires adequate sugar supply to support axillary bud outgrowth [175, 176]. It has been demonstrated that auxin treatment improves fertility in heat-stressed barley plants [177]. Auxins
Page 32 of 65
33 the shoot apex where auxins are synthesized changes into a flowering meristem. It
800
then develops into a spike containing the reproductive organs. The presence of auxin
801
biosynthesis in the floral organs at this stage might signify that apical dominance is
802
controlled by the reproductive structures. This function may be essential to direct
803
resources to the reproductive structures for seed production rather than investing them
804
in further vegetative growth. Abiotic stresses in cereals cause pollen sterility in
805
sensitive lines, resulting in increased tillering after the stress period (Fig. 3). This may
806
reflect the loss in apical dominance as a result of pollen sterility. An intriguing aspect
807
of auxins is that they regulate some aspects of plant development such as lateral root
808
development synergistically with ethylene and other hormones, while for some
809
aspects both hormones act antagonistically [180]. Recent progress in understanding
810
plant hormone action is illustrating the complexity of cross-talk between different
811
plant hormones and the importance of controlling hormone homeostasis.
812
Understanding the intricacies of these interactions is important to unravel how genetic
813
variability in the network can affect how plants adapt to environmental change.
cr
us
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d
te
818
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814
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799
819
in photomorphogenesis. Phytochromes respond to darkness (etiolation) and changes
820
in the red to far-red light ratio, which warns the plant about competing vegetation
821
(shade avoidance) [158]. Phytochromes control many growth processes from seed
822
germination to reproductive development and they are well known to modulate biotic
823
and abiotic stress responses [181].The activated form of phytochrome moves to the
815 816 817
4.5. Coordination of environmental responses Progress made in unravelling how plants react to low light conditions provided a clue as to how environmental signals regulate plant growth. Phytochrome photoreceptors react to changes in the ratio between red and far-red light and play an important role
Page 33 of 65
34 nucleus and forms a complex with members of the basic helix-loop-helix (bHLH)
825
transcription factors, the Phytochrome Interacting Factors (PIF). PIFs interact with
826
DELLA proteins; in the absence of GA, DELLA proteins bind to PIFs, preventing
827
them from regulating their target genes. In the presence of GA, DELLA proteins are
828
degraded, PIFs become functional and elongation growth is activated [161, 182, 183]
829
(Fig. 4). PIF transcription factors also activate auxin biosynthesis and their own
830
expression is controlled by the circadian clock; the Arabidopsis bZIP transcription
831
factor Hy5 (Elongated Hypocotyl) promotes photomorphogenesis by antagonizing PIF
832
action and the RING-motif E3 ligase COP1 (Constitutive Morphogenic) inhibits Hy5.
833
This pathway also influences CBF function and freezing tolerance [184]. PIFs form in
834
combination with DELLA proteins a hub for the integration of signals from various
835
hormones [183, 185-187], day-length [184, 188], light quality [158, 184], as well as
836
sugars [189] (Fig. 4). Light quality is also important for the induction of CBF
837
transcription factors and activation of cold and frost tolerance [190, 191] and PIFs
838
play a role in regulating expression of DREB transcription factors that are required for
839
drought responses [183]. Low red to far-red ratios lead to increased levels of ethylene
844
Ac ce p
te
d
M
an
us
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824
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converge into a single, complicated signalling hub that orchestrates plant growth
846
responses. This environmental response hub may explain why one abiotic stress can
847
improve the response to other stresses (section 3.4).
840 841 842 843
[158], which affects the stability of the DELLA proteins [165] (Fig. 4). Induction of the ERF transcription factor SUB1A under flooding conditions prevents elongation growth by increasing DELLA levels, thereby inhibiting GA-mediated elongation growth [37, 38]. The PIF transcription factors also mediate cross-talk with ROS signalling [193]. These findings demonstrate how different environmental stimuli
848
Page 34 of 65
35
5. Conclusions
850
In the last decade important progress has been made using model plants in
851
understanding how plants grow and develop and how they respond to changes in the
852
environment. This know-how is still fragmentary and needs to be extended to crop
853
plants. In important crop species such as cereals, it is important to maintain
854
productivity under abiotic stress conditions during the reproductive stage. Some crop
855
plants appear to overreact and switch to growth arrest too quickly, even when survival
856
is not immediately under threat. One way of improving stress tolerance and grain
857
productivity in cereals would be to increase the threshold level at which plants switch
858
from promotion to arrest of growth. At the vegetative stage, the stay-green trait has
859
achieved this by selecting for delayed senescence. Maybe an equivalent of the stay-
860
green trait is required to protect the reproductive stage and grain formation in cereals.
861
Seed production itself is a stress survival mechanism; seed can survive prolonged
862
stress conditions in dehydrated state and this guarantees the plant’s next generation.
863
This potential may have been lost from crop plants, but genetic diversity to
864
reintroduce this trait may still be available in breeding lines, landraces or wild
866 867 868 869
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us
an
M
d
te
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849
progenitor species. This material can also be used to further improve our understanding of the hormonal interactions that control growth.
A lesson could be learned from flooding tolerance research, which showed that both growth arrest and acceleration can be beneficial – depending on the circumstances.
870
This response requires ethylene and ERF transcription factors. The molecular basis of
871
how flooding tolerance interacts with the environmental response hub can serve as a
872
guideline for other abiotic stresses. Response to shading also shares some of the hub
873
components used by flooding stress. Importantly, the example of flooding stress
Page 35 of 65
36 indicates that avoidance and/or escape reactions should not necessarily be treated as
875
different or independent from true tolerance responses. The common denominator is
876
“growth regulation”. It is crucial that we learn to understand how plants regulate
877
growth in function of environmental restraints; this may lead to strategies to
878
manipulate the threshold levels to switch from growth arrest to maintenance of
879
growth. Crop plants such as cereals, combined with current technologies, can help us
880
to reach that level of understanding.
cr
ip t
874
us
881
Having a single regulatory hub to integrate all environmental responses and regulate
883
plant growth and development makes a lot of sense, but a lot of questions still need to
884
be answered. We need to get a better understanding about systemic signalling and the
885
relationship between vegetative and reproductive growth. During the stage of
886
flowering and seed production, a plant behaves quite differently from a plant during
887
vegetative growth. Even though there is a shared response system to the environment,
888
growth signals still need to be relayed to different plant parts and the effect in
889
different plant parts can be interpreted very differently. For instance, nitrogen
894
Ac ce p
te
d
M
an
882
895
environment. The use of Green Revolution genes in cereals has shown that reducing
896
stem elongation growth using semi-dwarf genes benefits grain yield, but there is a
897
trade-off in terms of abiotic stress tolerance and pollen fertility. Some semi-dwarf
898
mutations affect the function of DELLA proteins in the central hub controlling growth
890 891 892 893
application can stimulate vegetative growth and repress reproductive development. In cereals, grain yield depends on successful interaction between both vegetative and reproductive growth. While management, agronomy and breeding practices have focused a lot on the vegetative establishment phase of cereals, relatively little is known about the control of reproductive development and its interaction with the
Page 36 of 65
37 and abiotic stress responses (Fig. 4). This raises the question whether high yield and
900
high abiotic stress tolerance are compatible – or not. There is a strong need to fully
901
understand the function of the central environmental response hub (e.g., role of PIF
902
family members, identification of still unknown components), but the use of model
903
systems only may not allow us to achieve this and genetic variation in crop species
904
should be included in these studies. Analysing this genetic variation using new
905
generation genotyping and phenotyping technologies has vastly improved and
906
identification of candidate stress tolerance genes is made easier using genomics.
907
Proof-of-function transgenic approaches may also lead to identification of genes that
908
can be used for stress-proofing cereals.
M
909
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us
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The technological revolution of the last decade has provided renewed hope for
911
improving abiotic stress tolerance in crops such as cereals, but it is clear that this
912
effort will increasingly require close interaction between plant scientists of different
913
disciplines, including bioinformaticians and engineers.
te
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d
910
919
of cited references in this review paper has been limited by journal policy. The author
920
apologises to those authors whose publications were not cited in this paper.
915 916 917
Acknowledgements
R.D. is supported by grants from the Grains Research and Development corporation (GRDC, grants CSP00130, CSP00143 and CSP00175). The author thanks Jane Edlington and Holly Staniford for their help in preparing the manuscript. The number
921
Page 37 of 65
38 922
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Figure Legends Figure 1: Effect of domestication in rice. Oryza rufipogon (top panel) is
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Figure 2: Proposed components of abiotic stress responses in plants.
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Early responses to abiotic stress are likely to be general stress responses: cellular
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1426
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1427
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1429 1430 1431 1432
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will maintain growth and productivity as much as possible. The latter phenotype will require successful interaction between the different early responses to establish stress-specific responses. Genetic variation can occur at different levels of the response pathway. QTL (stars with letter “Q”) in different parts of the general stress response will affect response to different abiotic stresses. QTL in
1433
the stress-specific responses are predicted to only affect response to a particular
1434
stress. Targeting the genetic variation in the general stress response could be more
1435
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1436
for stress-specific responses may have negative effects for other stresses.
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Figure 4: Simplified schematic representation of the components involved in the
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avoidance response pathway in Arabidopsis. The PIF and DELLA proteins are
1448
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61 Abiotic stresses affect yield and productivity of crop plants. Stress tolerance in crops correlates with maintenance of growth and productivity. Early stress-responsive genes control growth responses Selection strategies should use stress-induced traits and focus on early general stress response. Plant hormone interactions control development and abiotic stress tolerance.
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