Improving photosynthesis, plant productivity and abiotic stress tolerance – current trends and future perspectives

Accepted Manuscript Title: Improving photosynthesis, plant productivity and abiotic stress tolerance – current trends and future perspectives Authors: Beatrycze Nowicka, Joanna Ciura, Renata Szyma´nska, Jerzy Kruk PII: DOI: Reference:

S0176-1617(18)30522-4 https://doi.org/10.1016/j.jplph.2018.10.022 JPLPH 52877

To appear in: Received date: Revised date: Accepted date:

16-8-2018 23-10-2018 24-10-2018

Please cite this article as: Nowicka B, Ciura J, Szyma´nska R, Kruk J, Improving photosynthesis, plant productivity and abiotic stress tolerance – current trends and future perspectives, Journal of Plant Physiology (2018), https://doi.org/10.1016/j.jplph.2018.10.022 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.

Improving photosynthesis, plant productivity and abiotic stress tolerance – current trends and future perspectives Beatrycze Nowickaa, Joanna Ciuraa, Renata Szymańskab, Jerzy Kruka* a

Department of Plant Physiology and Biochemistry, Faculty of Biochemistry, Biophysics and

b

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Biotechnology, Jagiellonian University, Gronostajowa 7, 30-387 Kraków, Poland

Department of Medical Physics and Biophysics, Faculty of Physics and Applied Computer

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Corresponding author:

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[email protected], telephone number: +48 12 664 63 61

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Science, AGH University of Science and Technology, Reymonta 19, 30-059 Kraków, Poland

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E-mail addresses of the other authors: B. Nowicka: [email protected]

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J. Ciura: [email protected]

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R. Szymańska: [email protected]

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Abstract

With unfavourable climate changes and an increasing global population, there is a great need for more productive and stress-tolerant crops. As traditional methods of crop improvement have probably reached their limits, a further increase in the productivity of crops is expected to be possible using genetic engineering. The number of potential genes and metabolic pathways, which when genetically modified could result in improved photosynthesis and

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biomass production, is multiple. Photosynthesis, as the only source of carbon required for the growth and development of plants, attracts much attention is this respect, especially the

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question concerning how to improve CO2 fixation and limit photorespiration. The most promising direction for increasing CO2 assimilation is implementating carbon concentrating mechanisms found in cyanobacteria and algae into crop plants, while hitherto performed experiments on improving the CO2 fixation versus oxygenation reaction catalyzed by Rubisco

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are less encouraging. On the other hand, introducing the C4 pathway into C3 plants is a very

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difficult challenge.

Among other points of interest for increased biomass production is engineering of

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metabolic regulation, certain proteins, nucleic acids or phytohormones. In this respect,

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enhanced sucrose synthesis, assimilate translocation to sink organs and starch synthesis is crucial, as is genetic engineering of the phytohormone metabolism. As abiotic stress tolerance

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is one of the key factors determining crop productivity, extensive studies are being undertaken to develop transgenic plants characterized by elevated stress resistance. This can be

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accomplished due to elevated synthesis of antioxidants, osmoprotectants and protective proteins. Among other promising targets for the genetic engineering of plants with elevated stress resistance are transcription factors that play a key role in abiotic stress responses of

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plants.

In this review, most of the approaches to improving the productivity of plants that are

potentially promising and have already been undertaken are described. In addition to this, the

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limitations faced, potential challenges and possibilities regarding future research are discussed. Keywords: photosynthesis, genetic engineering, biomass, carbon fixation, phytohormones, stress tolerance

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Introduction 1. Strategies for increasing photosynthetic efficiency 1.1. Towards the improvement of the light phase of photosynthesis 1.2. The improvement of carbon fixation in the dark phase of photosynthesis 1.2.1. Manipulation of Rubisco 1.2.2. Carbon concentration mechanisms of cyanobacteria and algae 1.2.3. Carbon concentration mechanisms of C4 and CAM plants

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1.2.4. Other concepts to improve CO2 fixation 1.3. Engineering of photorespiration 1.4. Obstacles and limitations

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2. Transgenic plants for improved biomass production 2.1. RNAs and proteins affecting the growth and development of plants 2.1.1. miRNAs and transcription factors regulating plant growth 2.1.2. Proteins stimulating cell division or expansion

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2.1.3. Changes in the developmental stage and photomorphogenic responses

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2.2. Metabolic regulation

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2.2.1. Modulation of sugar metabolism and transport 2.2.2. Nutrient metabolism

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2.3. Engineering of phytohormones for improved plant productivity 2.4. Other targets for increasing biomass production

3.1. Photooxidative stress

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3. Transgenic plants with elevated resistance to abiotic stresses

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3.2. Drought and salinity stress 3.2.1. Drought stress

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3.2.2. Salinity stress 3.3. Cold stress

3.4. Heat stress and other stresses 4. Why do some plants grow faster than others?

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Future directions

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Introduction

With an increasing global population, shortage of agricultural areas and climate change, there is a high demand for more productive and stress-resistant crops for food and energy purposes. During the second half of the 20th century there was a significant increase in crop yield, which mostly took advantage of new, highly effective cultivars, fertilizers and pesticides (Betti et al., 2016). As a consequence, the yield of the major grain crops increased considerably (Long et

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al., 2006). However, in recent years crop production has increased only slightly and it is predicted that the productivity of the major crop species is approaching the maximal yield that

can be obtained using traditional methods (Betti et al., 2016; Hanson et al., 2016). The further

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increase in crop yield is expected to be achieved by means of genetic engineering (Ort et al.,

2015). Besides the increase in crop yield, due to climate change their resistance to environmental stresses will be the main point of interest for agriculture and plant biotechnology in the near future.

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The main driving force for the growth and biomass production of plants is

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photosynthesis, which supplies the energy and carbon required for the biosynthesis of organic

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compounds necessary for development. Therefore photosynthesis, especially CO2 assimilation, draws most attention in research that could result an improvement of the

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productivity of crops. The strategies undertaken in this area are diverse. There is ongoing research aimed at the discovering natural genetic variation responsible for the increase in

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photosynthetic capacity (Hüner et al., 2016; Nunes-Nesi et al., 2016). The other direction takes advantage of genetic engineering and this approach will be reviewed here. Various

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strategies aimed at enhancing the capacity of photosynthesis have been described, both the concepts concerning the improvement of the light and dark phases of photosynthesis, as well

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as attempts to limit carbon and energy losses during photorespiration. To achieve increased plant productivity other processes could be optimized using genetic engineering methods as well, such as nutrient supply or carbohydrate transport and allocation. Another strategy to be applied is the regulation of plant growth and development by manipulating miRNAs,

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transcription factors (TFs), proteins that participate in the regulation of cell division and expansion, as well as phytohormones. In field conditions, plant productivity is limited by different stress factors, therefore obtaining stress-tolerant plants via genetic engineering is a crucial goal of green biotechnology. Although up to date, many review articles have been published on the use of genetic engineering to improve plant productivity. Nevertheless these articles focused mainly on

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selected aspects (e.g., photosynthesis, carbon fixation, abiotic stress) regarding this issue. In this review we present holistic treatment of the subject, covering a variety of approaches leading to an improvement in plant productivity and their abiotic stress tolerance, with the emphasis on recent achievements in this field. . 1. Strategies for increasing photosynthetic efficiency

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1.1. Towards the improvement of the light phase of photosynthesis

Some of the ideas focus on the enhancement of light absorption or the increase in the

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rate of the photosynthetic electron transfer chain (Fig. 1). Usually, only a narrow range of solar spectrum is used for photosynthesis due to the spectral properties of photosynthetic

pigments. The general trend in the evolution of photosynthetic organisms was to specialize in the absorption at certain wavelengths available in particular ecological niches, rather than to

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widen the absorption spectrum (Hitchcock et al., 2016). Oxygenic phototrophs use two

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photosystems, which both absorb light within a similar range, thus they compete for photons

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(Ort et al., 2015). The idea is to implement bacteriochlorophyll (BChl)-based reaction centers in higher plants in order to create a plant with two types of photosystems, one chlorophyll-

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based (absorbing visible light) and the other absorbing far red and infrared light that relies on Bchl. This would make it possible to increase the spectral range of light absorption (Ort et al.,

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2015). Although this idea is plausible, whether it is possible is a question for the distant future.

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The other fact is that photosynthetic apparatus evolved to maximize light absorption. Thus, when exposed to high-light intensity, photosynthetic organisms absorb more light than

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they can use. Typically, photosynthesis in C3 plants is saturated by ca. 25% of the full sunlight intensity (Ort et al., 2011). When the light intensity is higher than the saturating intensity, photosystems absorb excessive energy that should be dissipated (Ort et al., 2015). Usually, in an open field at full sunlight, the upper leaves absorb more energy than they can use. On the

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other hand, the lower leaves are often exposed to sub-saturating light intensities. Therefore, scientists considered engineering plants with less light-harvesting pigments in the upper leaves. This would improve light penetration into the canopy (Ort et al., 2015). The manipulation of leaf area, orientation and reflectivity was also considered (Drewry et al., 2014). It is supposed that one of the main factors underlying the improved yield of cultivars introduced during “green revolution”, besides the short stature, was improved canopy

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architecture, especially more erect leaves in the upper part of plants. This trait improved light penetration into canopy, resulting in the increased CO2 assimilation rate (Song et al., 2013). The erect leaf phenotype observed in rice osdwarf4-1 mutant was associated with the increase in grain yield (Sakamoto et al., 2006). The investigation of QTL in rice led to the identification of NARROW LEAF1 (NAL1) gene whose product controls leaf blade morphology and vein patterning. This gene shows pleiotropic effects on leaf anatomy, photosynthetic rate per leaf area, spikelet number and grain yield (Hirotsu et al., 2017). The idea of the optimization of light energy distribution and usage within the canopy has been

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called a ‘smart canopy’ concept (Ort et al., 2015). Although the idea deserves some consideration, putting the smart canopy concept into practice using the transgenic approach

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seems to be difficult, if not impossible. The main concepts of improvement of the light phase of photosynthesis have been summarized by Cardona et al. (2018).

In order to provide high light-use efficiency, plants must retain a balance between light conversion in source tissue and light utilisation in sink organs. An imbalance in energy flow

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induces nonphotochemical quenching processes which protect plants and allow them to

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survive, although at the cost of decreased light-use efficiency. One way to overcome this

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obstacle is to enhance sink capacity. This can be accomplished at the level of the Calvin cycle (section 1.2.4), but also by enhancing the assimilate export, which prevents the

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downregulation of photosynthesis by accumulated sugars (section 2.2.1).

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1.2.The improvement of carbon fixation in the dark phase of photosynthesis

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One of the most important factors determining plant productivity is the efficiency of carbon assimilation. All photosynthetic eukaryotes fix CO2 using the Calvin cycle (Hügler and

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Sievert, 2011). However, the properties of the key enzyme of this pathway, ribulose-1,5bisphosphate (RuBP) carboxylase/oxygenase (Rubisco), limit the capacity of carbon fixation. This is mainly due to the fact that Rubisco does not discriminate well between CO2 and O2. Besides the desired reaction of RuBP carboxylation, Rubisco also catalyses a side reaction of

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RuBP oxygenation (Betti et al., 2016; Hagemann and Bauwe, 2016). It was assumed that Rubisco evolved in an anaerobic environment, although a recent hypothesis indicates that the evolution of Rubisco took place under local microoxic conditions (Ślesak et al., 2017). Even after the appearance of oxygenic photosynthesis, for the next 2 Ga the oxygen concentration was low. Therefore, the ancient Rubisco was not primarily selected for suppressing the oxygenation reaction (Erb and Zarzycki, 2016; Hagemann et al., 2016). In the present oxygen-

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rich atmosphere, in C3 plants, which comprise the majority of crop species, every third to fourth molecule of RuBP is oxygenated giving 3-phosphoglycerate and 2-phosphoglycolate (Hagemann and Bauwe, 2016). The latter is an inhibitor of enzymes that participate in photosynthetic carbon metabolism, thus it has to be metabolized. This is achieved via photorespiration that requires significant energy input and leads to the loss of assimilated carbon and nitrogen as CO2 and NH3, respectively (Peterhansel et al., 2013). It is thought that at 25°C the rate of carbon loss due to photorespiration accounts for 25% of the rate of carbon

assimilated carbon per year (Betti et al., 2016; Hagemann and Bauwe, 2016).

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assimilation and globally this process re-liberates into the atmosphere about 29 Gt of

The second constraint is the slow reaction rate of Rubisco, whose turnover number is

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usually between 1 and 10 s-1, while for other enzymes of central metabolism the numbers are

in the range of 50-100 s-1. To compensate for the low activity of Rubisco, plants produce high amount of this enzyme, making up to 50% of the soluble proteins of photosynthetic organisms (Erb and Zarzycki, 2016). This, however, requires high nitrogen investment in Rubisco

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(Whitney et al., 2011a). Therefore, several carbon concentration mechanisms (CCMs) evolved

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in cyanobacteria, algae and land plants to enhance carbon fixation and limit photorespiration

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(Peterhansel et al., 2013).

There are currently three approaches to improve carbon fixation via genetic

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engineering, namely improving the catalytic properties of Rubisco, attempts to introduce CCM into crop plants and engineering of photorespiration (Fig. 1). In the 70’s, Farquhar et al.

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developed a model of plant CO2 assimilation that was later extended and improved (Farquhar et al., 2001). Based on this model it is assumed that critical factors limiting CO2 fixation are

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the CO2 concentration in the chloroplast and balancing the maximal rate of the RuBP regeneration to that of RuBP carboxylation (Hikosaka et al., 2006). These issues have been

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targets of genetic modification, i.e. there have been attempts to introduce CCM into higher plants, to improve Rubisco and to increase the rate of the regeneration phase.

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1.2.1. Manipulation of Rubisco

One of the plausible approaches is to obtain or select Rubisco with improved catalytic properties (Parry et al., 2003). There is a wide range of Rubiscos that occur naturally and differ in their catalytic properties. However, due to the catalytic mechanism of this enzyme, there is an inverse correlation between the catalytic rate and substrate specificity (Erb and Zarzycki, 2016). There are some ways to cope with this limitation. Firstly, the low-specific

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Rubisco with higher turnover rate could be introduced together with CCM providing a favourable CO2/O2 ratio near the catalytic site. Secondly, there are known Rubiscos with higher specificity and acceptable catalytic rates (Galmes et al., 2005). Recent work on the catalytic properties of Rubiscos isolated from eleven diatom species showed noticeable differences in enzyme kinetics. Judging by the lack of correlation between CO2 affinity and maximum rates of carboxylation, which has been observed in other known Rubiscos, it has been suggested that the catalytic mechanism of diatom enzymes differs from those of other

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known photosynthetic eukaryotes (Young et al., 2016). It is known that Rubiscos of some red algae have high selectivity and still relatively high catalytic rates. However, when expressed in higher plants, these enzymes do not assemble properly (Parry et al., 2013).

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Besides studies on natural Rubiscos, selection systems that enable the directed

evolution of these enzymes have been developed. Using this method, it was possible to obtain expression of cyanobacteria-derived Rubisco in E. coli, showing an improved carboxylation turnover rate and CO2 affinity, but with no change in selectivity (Parikh et al., 2006). The

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other system was based on a bio-selection strategy using a Rubisco-deletion (Δrbc) mutant of

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the photosynthetic bacterium Rhodobacter capsulatus (Mueller-Cajar and Whitney, 2008).

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The bacteria were trans-complementated with libraries of randomly mutated Rubisco genes of Synechococcus PCC6301 and screened for photoautotrophic growth. However, Rubisco of

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these mutants displayed little change in catalytic properties when compared to that of the wild type, except for the 50% reduction in the Michaelis constant. This evolution did not allow the

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enzyme with improved catalytic properties as compared to the known natural Rubiscos, to be obtained. Therefore, it is questionable whether this approach could ever be successful in the

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future.

Another approach is site-directed mutagenesis of Rubisco (Parry et al., 2003).

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Exchanging a single amino acid resulted in a higher maximum rate but lower CO2 affinity and vice versa (Whitney et al., 2011b). To date, no significant improvement in the activity and specificity of Rubisco has been achieved using directed mutagenesis (Ort et al., 2015). Engineering transgenic plants with improved Rubisco is a complex issue. The Rubisco

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of higher plants is a hexadecamer containing 8 large catalytic and 8 small regulatory subunits (Tabita et al., 2008). The large subunit is encoded by plastid genome, while the small subunit is encoded by nuclear genome in multiple copies. The individual expression of genes that encode small subunits depends on the environmental conditions and developmental stage (Carmo-Silva et al., 2015). The expression of small and large subunits must be strictly coordinated. The small subunits have to be properly targeted to chloroplasts. Rubisco subunits

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are folded and assembled with the help of chaperonins. It was shown that even a single amino acid substitution may have a significant impact on the functional enzyme folding (Parry et al., 2013). Introducing foreign genes that encode subunits of Rubisco into tobacco resulted in their transcription, but the protein was not translated (Madgwick et al., 2002). Even if heterologous Rubisco subunits are expressed, they do not necessarily assemble into a functional enzyme (Parry et al., 2003; Sharwood et al., 2008). There were also more successful attempts to obtain chimeric Rubisco. The expression of the gene encoding small

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subunit of Rubisco from sorghum increased the catalytic turnover rate of the enzyme in transgenic rice (Ishikawa et al., 2011). Combining large and small Rubisco subunits derived from different species usually leads to reduced affinity, activity and selectivity of hybrid

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enzymes (Wang et al., 2001). Thus, the more promising method is to replace both subunits but this requires both nuclear and chloroplast genomes of a target plant to transform successfully. The other postulated approach is to manipulate the activity of Rubisco activase, an

ATP-dependent enzyme which restores catalytic competence to Rubisco by removing

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inhibitory sugar phosphates from its catalytic sites (Carmo-Silva et al., 2015; Parry et al.,

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2013). It was shown that plant activases are unstable in vitro at temperatures above 30C. The

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replacement of native Rubisco activase with a more thermostable form, obtained using gene shuffling technology, in A. thaliana resulted in plants with a slightly improved photosynthetic

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rate, biomass and seed yield when grown under moderate heat stress (Kurek et al., 2007). Transgenic rice with overexpression of Rubisco activase from barley or maize indeed

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displayed enhanced activation of Rubisco, but the assimilation of CO2 under ambient air decreased. It was shown that the Rubisco content of transgenic plants substantially decreased,

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most probably due to posttranscriptional regulation (Fukayama et al., 2012). These data indicate that manipulating Rubisco is not a very promising way to increase

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CO2 assimilation by Rubisco and the extent to which it discriminates against oxygen, at least in the near future.

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1.2.2. Carbon concentration mechanisms of cyanobacteria and algae

Many photosynthetic organisms, usually those living in water ecosystems, have evolved CCMs based on the concerted action of inorganic carbon uptake systems, enzymes responsible for the reversible conversion of CO2 into carbonate, and subcellular structures, where CO2 concentration is elevated in the vicinity of Rubisco. These structures are called

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carboxysomes in cyanobacteria and pyrenoids in many lineages of eukaryotic algae (Singh et al., 2016). Cyanobacterial CCMs are able to concentrate CO2 up to 1000-fold around the active site of Rubisco, using CO2 but not HCO3- as the substrate. These systems are based on HCO3transporters or membrane bound NAD(P)H-dehydrogenase complexes that convert CO2 to HCO3-. Carbon dioxide is released back from HCO3- in carboxysomes that contain Rubisco, carbonic anhydrase and shell proteins (Cameron et al., 2013; Rae et al., 2013). As there are

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variety of CO2 and HCO3- uptake systems, carboxysome types and carbonic anhydrases, different cyanobacterial species take advantage of various combinations of these CCM elements. Expression of CCM components may depend on growth conditions. For example,

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high-affinity carbon uptake systems are expressed in many cyanobacteria under limited CO 2 availability in the environment (Singh et al., 2016).

Eukaryotic CCMs were found in green and red algae, dinoflagellates, diatoms, as well as in hornworts (Hagemann et al., 2016; Singh et al., 2016). The major operating principle of

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these systems is similar to that of cyanobacteria. Specialized micro-structures, pyrenoids, are

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present in chloroplasts and like cyanobacterial carboxysomes, contain carbonic anhydrase and

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Rubisco (Singh et al., 2016). CCM in diatoms allows effective photosynthesis to be maintained using far less Rubisco than higher plants (Carmo-Silva et al., 2015).

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The advantages of CCMs make the idea of introducing these systems into crop plants a promising approach (Hanson et al., 2016). Besides cyanobacteria, carboxysomes also occur in

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some autotrophic proteobacteria (Cameron et al., 2013). Functional carboxysomes from Halothiobacillus neapolitanus were expressed in E. coli (Bonacci et al., 2012). Engineering

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carboxysomes in eukaryotic organisms seems considerably more challanging. Rubisco from cyanobacterium Synechococcus elongatus was used to replace the native enzyme of tobacco

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(Occhialini et al., 2016). Cyanobacterial Rubiscos operate at higher catalytic rates than those of higher plants, although at the expense of lower affinity and specificity (Whitney et al., 2011a). Therefore, transgenic tobacco, which expresses cyanobacterial Rubisco, but lacks CCM, required an elevated CO2 concentration for growth (Occhialini et al., 2016). The

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transient expression of carboxysome proteins from Synechococcus elongatus fused with plastid transit peptides in Nicotiana benthemiana leads to the formation of organized structures in chloroplasts (Lin et al., 2014). The other element of cyanobacterial CCM, HCO3transporter, was expressed in tobacco (Pengelly et al., 2014). Cyanobacterial bicarbonate transporters were expressed in plant cells and successfully targeted at the chloroplast envelope (Rolland et al., 2016; Uehara et al., 2016). Moreover, ten components of the CCM of

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Chlamydomonas reinhardtii were expressed in tobacco and A. thaliana. In transgenic tobacco all of these components except carbonic anhydrases CAH3 and CAH6 were directed towards the same intracellular locations as in C. reinhardtii. The individual expression of certain inorganic carbon transporters in A. thaliana did not enhance the growth of transgenic plants (Atkinson et al., 2016). The successful expression of algal CCM components in higher plants is promising, but this research is still in a rather early stage and needs to be extended in the future.

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Although these experiments have been not successful in introducing CCMs that could be applied in practice, this is a very promising direction for improving CO2 assimilation in crop plants. The progress of research on introduction of CCM into higher plants has been

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reviewed by Rae et al. (2017).

1.2.3. Carbon concentration mechanisms of C4 and CAM plants

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In higher plants, other carbon concentrating mechanisms have evolved. These are based on

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the development of an additional cycle responsible for fixing inorganic carbon, which does

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not replace the Calvin cycle but enables effective carbon assimilation followed by a release of CO2 under conditions where it can be re-fixed by Rubisco with high efficiency (DePaoli et al.,

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2014; Gowik and Westhoff, 2011). The key reactions of C4 cycle and crassulacean acid metabolism (CAM) are the same. The main difference is that in the C4 plants two carbon

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fixation reactions are separated in space, while CAM plants separate them in time. Separation in space demands functional diversification. Usually this is accompanied by anatomically

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diverse leaf tissue (Gowik and Westhoff, 2011). The majority of C4 plants have developed so called Kranz anatomy, meaning that their photosynthetic tissue is differentiated into

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mesophyll and bundle sheath cells. The mesophyll cells express the key enzyme of the C4 cycle, phosphoenolpyruvate carboxylase, which effectively assimilates HCO3-, a substrate that cannot be used by Rubisco. The malate or aspartate formed is exported to the bundle sheath cells, where it is decarboxylated to pyruvate which is transported back to the mesophyll, while

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the CO2 released is assimilated by Rubisco (Gowik and Westhoff, 2011). While in the chloroplasts of C3 plants, CO2 concentration is below 10 M, in chloroplasts of bundle sheath cells of C4 species, it reaches a concentration of 160 M or higher (Furbank and Hatch, 1987). This allows for efficient CO2 fixation by C4 plants, taking advantage of low substrate-specific Rubisco (Whitney et al., 2011a). As a consequence, less Rubisco is required for efficient photosynthesis and typically the Rubisco content in C4 plants amounts to 10-25% of total 11

soluble proteins (Carmo-Silva et al., 2015). Although the C4 cycle requires additional energy input, it enables more efficient CO2 fixation. The C4 pathway evolved independently in 62 plant lineages, e.g. species important from an agricultural point of view, such as maize and sugar cane (Hanson et al., 2016). However, the majority of crop species, such as wheat, rye and rice are C3 plants. The introduction of the C4 pathway into these species seems to be a promising direction (Fig. 1). Although the number of genes encoding key enzymes and transporters necessary for the C4 pathway is small, introducing the C4 cycle into C3 plants

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seems to be a very difficult task (Covshoff and Hibberd, 2012). Nevertheless, numerous attempts have been undertaken to introduce the C4 pathway into major crops (Peterhansel et

al., 2013). The first efforts focused on engineering transgenic plants, where the C 4 cycle

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would operate in the same cells as the Calvin cycle (Miyao et al., 2011). Although overexpression of C4 enzymes was successful in transgenic rice, it did not result in functional

C4 cultivar being obtained (Taniguchi et al., 2008). In other research on C4 rice, the requirement for morphologic differentiation into a two-compartment structure has been taken

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into consideration (von Caemmerer et al., 2012; Covshoff and Hibberd, 2012). This approach

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demands intensive basic research concerning leaf tissue differentiation. The transcriptomes of

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closely related C4, C3 and C3-C4 intermediate species of the genus Cleome and Flaveria were compared to find genes responsible for the C4 phenotype (Bräutigam et al., 2011; Gowik et

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al., 2011). There are also species where the C4 cycle operates in one type of cells, so-called single-cell C4 plants (Sharpe and Offermann, 2014). Single-cell C4 plants are usually either

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aquatic plants or plants adapted to a dry climate, therefore their physiology and leaf anatomy differs from that of crop plants (Häusler et al., 2002). However, the potential of such

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organisms has been noticed by Gerald Edwards’ group. Recently, they have analyzed the spatial and temporal patterns in the expression of photosynthetic enzymes, as well as the

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structural maturation of chlorenchyma cells in young leaves of two single-cell C4 plants, Bienertia sinuspersici and Suaeda aralocaspica (Koteyeva et al., 2016). Although it was found that all the genes of C4 enzymes are present in C3 species, the

functional C4 photosynthesis requires a considerably higher number of genes to be activated

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(Covshoff and Hibberd, 2012). Developing new model plants for studying the C4 cycle, such as Cleome gynandra and Setaria viridis, could be also beneficial (Brown et al., 2005; Brutnell et al., 2010). It is known that CAM plants produce amounts of biomass comparable to C3 and C4 plants using 20-80% less water. Thus, the idea of introducing CAM metabolism into C3 plants has been considered, especially to improve crop plants grown in a hot and dry climate

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(DePaoli et al., 2014). However, it has to be taken into consideration that CAM plants grow slowly and this approach will most probably not give satisfactory results as far as growth improvement is concerned.

1.2.4. Other concepts to improve CO2 fixation According to Farquhar’s model, the rate of RuBP regeneration is an important factor

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determining the rate of CO2 assimilation. This assumption was confirmed by experiments on transgenic plants with down-regulated expression of Calvin cycle enzymes. Among enzymes

of the regenerative phase the most important is sedoheptulose-1,7-bisphosphatase (SBP), as

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even a small reduction in its content leads to a decrease in photosynthetic capacity and growth

(Raines, 2011). Transgenic tobacco that overexpressed SBP from A. thaliana displayed increased activity of this enzyme and enhanced carbon fixation when compared to the wild type (Lefebvre et al., 2005). On the other hand, an increase in photosynthesis and growth was

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not observed in rice with increased SBP activity when it was grown under optimal conditions

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(Feng et al., 2007).

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It has also been suggested that the Calvin cycle could be replaced with other CO2 fixation pathways (Erb and Zarzycki, 2016). To date, besides the Calvin cycle we know five

acetyl-coenzyme

hydroxypropionate

bicycle,

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pathway,

reductive

tricarboxylic

dicarboxylate/4-hydroxybutyrate

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reductive

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other CO2 assimilation pathways that occur in some bacteria and archaea, namely the acid cycle

cycle,

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and

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hydroxypropionate/4-hydroxybutyrate cycle (Fuchs and Berg, 2014; Hügler and Sievert,

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2011). Most of them are advantageous in terms of energy demand and efficiency when compared to the Calvin cycle (Berg, 2011), although three of them harbour oxygen-sensitive

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enzymes (Hügler and Sievert, 2011). Of the two oxygen-insensitive pathways, i.e. 3hydroxypropionate bicycle and 3-hydroxypropionate/4-hydroxybutyrate cycle, the former was taken into consideration. The enzymes of the 3-hydroxypropionate bicycle from Chloroflexus aurantiacus were expressed in E. coli K12 (Mattozzi et al., 2013) The enzymes of all four

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sub-pathways (bicycle steps) introduced functioned in transformed E. coli, although overexpression of certain enzymes was deleterious to cells (Mattozzi et al., 2013). The most ambitious approach would be to design novel CO2-fixation pathways, but this is to be considered in a distant future (Bar-Even et al., 2010; Erb and Zarzycki, 2016; Ort et al., 2015).

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1.3. Engineering of photorespiration

As previously mentioned, phosphoglycolate formed in the oxygenation reaction of RuBP catalyzed by Rubisco is toxic and has to be metabolized. The reactions of 2-phosphoglycolate recycling, occurring in chloroplasts, peroxisomes, mitochondria and cytosol have been called photorespiration (Betti et al., 2016). Photorespiration consumes much energy and leads to carbon and nitrogen loss,

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therefore limiting this process has been considered as a way to enhance biomass production, mostly through reduction in the loss of assimilated carbon. However, photorespiration interacts with central metabolic pathways and plays multiple roles. It is a sink for an excess of

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reducing power, produced under stress conditions (Betti et al., 2016). There is a direct relationship between the capacity for photorespiratory flux and abiotic stress tolerance (Li and Hu, 2015). Moreover, hydrogen peroxide produced by glycolate oxidase plays a role during the response to pathogens (Rojas et al., 2012) and in signaling pathways leading to

U

programmed cell death (Mateo et al., 2004).

N

The mutants of genes encoding key photorespiratory enzymes cannot grow under

A

ambient air and survive only at elevated CO2 concentration. This has been called ‘photorespiratory phenotype’ (Timm and Bauwe, 2013). The experiments on transgenic potato

M

and rice showed that antisense suppression of photorespiratory enzymes leads to decreased productivity and growth rate (Schjoerring et al., 2006; Xu et al., 2009), while their

ED

overexpression in Arabidopsis and rice leads to an increase in plants’ growth and net photosynthesis (Timm et al., 2012; Wu et al., 2015). Timm and Bauwe (2013) provide

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examples of cross-talk between photorespiration and other processes, such as lipoic acid, folate and H2O2 metabolism, but also state that the exact reasons for the phenotypes of certain

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mutants are still mostly unknown. As a reduction in the photorespiratory rate does not increase plant biomass, other

approaches have been proposed, taking advantage of alternative pathways of 2phosphoglycolate recycling (Fig. 1). Kebeish et al. (2007) introduced the glycolate catabolic

A

pathway from E. coli into Arabidopsis chloroplasts. In this pathway, glycolate is converted to glycerate by heterogeneously expressed glycolate dehydrogenase, glyoxylate carboligase and tartronic semialdehyde reductase. The CO2 released in this pathway can be assimilated by Rubisco. The ‘Kebeish bypass’ was successfully introduced into oilseed crop Camelina sativa, leading to an increase in seed yield and improved growth (Dalal et al., 2015). Potato

14

that expresses glycolate dehydrogenase showed increased shoot biomass and tuber yield (Nölke et al., 2014). Maier et al. (2012) introduced a complete glycolate catabolic pathway into the chloroplasts of A. thaliana, including transgenes for glycolate oxidase, malate synthase and catalase. Malate is oxidized to pyruvate by the chloroplast NADP-malic enzyme and pyruvate is then converted to acetyl-CoA by pyruvate dehydrogenase. The CO2 released in both of these reactions can be fixed by Rubisco. In this approach, ATP-dependent reactions of the

IP T

original photorespiratory pathway and the step of NH3 loss are bypassed. Transgenic plants obtained by both groups showed elevated biomass production but only under short-day conditions (Kebeish et al., 2007; Maier et al., 2012). The third approach was to introduce two

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E. coli enzymes, glyoxylate carboligase and hydroxypyruvate isomerase, so that they could convert glyoxalate into hydroxypyruvate in peroxisomes. This approach should bypass

mitochondrial reactions leading to carbon and nitrogen loss. Using this strategy, transgenic tobacco lines were obtained, but the hydroxypyruvate isomerase was not expressed (de

U

Carvalho et al., 2011).

N

Another approach is also possible, as it is known that there are other routes for 2-

A

phosphoglycolate recycling. For example, some cyanobacteria can convert glyoxylate into glycerate (Betti et al., 2016). However, the expression of cyanobacterial genes that encode

M

enzymes of this pathway and targeting them to peroxisomes of Arabidopsis did not affect its growth and photosynthesis (Hagemann and Bauwe, 2016). On the other hand, transgenic

ED

tobacco and Arabidopsis which overexpress glutamine synthetase, an enzyme responsible for assimilating photorespiratory NH3, displayed a faster growth under photorespiratory

PT

conditions (Zhu et al., 2014). It was also observed that plants overexpressing glutamine

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synthetase are more tolerant to high light and salt stress (Hoshida et al., 2000).

1.4. Obstacles and limitations

There are several points that limit our opportunities to improve photosynthetic efficiency

A

using genetic engineering. Firstly, being a core metabolic process that has evolved over billions of years, photosynthesis is a complex process and highly integrated in the whole metabolism of photosynthetic organisms. Photorespiration intermediates have an impact on the capacity of seemingly unrelated processes, such as nitrate assimilation (Betti et al., 2016). Changing one element disturbs other interactions. Our knowledge concerning the integration of metabolism and regulatory networks is still limited and requires further study.

15

The second limitation is due to the available methodology. As photosynthetic traits are often encoded both in nuclear and plastid genomes, we need efficient methods for transforming both genomes (Ort et al., 2015). Besides, these methods require the introduction of long DNA fragments that encode several proteins. Nuclear transformation strategies face several limitations. The genes introduced are prone to silencing and high expression of transgenes is often not reached (Ort et al., 2015). Knowledge of promoters, terminators, transport signals, centromere and telomere sequences is scarce (Ort et al., 2015). Plastid

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transformation techniques enable one to introduce multiple transgenes with high precision and to achieve high expression levels, but until now transformation protocols have only been

developed for a few species. The plastid transformation of cereals has not yet been successful

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(Ort et al., 2015). Even if the genes were successfully introduced and are expressed, their

products need to be properly folded, transported and in many cases assembled into functional complexes.

Nevertheless, novel technologies that enable precise genetic engineering have been

U

developed, among them CRISPR/Cas9 system (Feng et al., 2014) and a system based on

N

transcription activator-like effector nucleases (TALEN) (Bedell et al., 2012; Li et al., 2012).

A

The assembly of plant mini-chromosomes has opened new possibilities concerning the

M

introduction of a higher number of genes into crop plants (Carlson et al., 2007).

ED

2. Transgenic plants for improved biomass production

Photosynthesis is responsible for introducing organic compounds into plant metabolism, so an

PT

improvement in its capacity should result in increased biomass production. However, there are several other processes which could be manipulated to improve the growth of plants. High

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biomass yield is important for the effective production of biofuels. Nowadays, the main type of biofuel is starch- or sucrose-based ethanol produced from maize and sugarcane, respectively. Another important biofuel is biodiesel derived from oilseeds. These make up the first generation of biofuels, while the second generation relies on the fermentation of

A

lignocellulosic feedstock (Yuan et al., 2008). This approach is considered more beneficial as it is based on agricultural residuals and not on crops that are usually used for food production (Phitsuwan et al., 2013). Moreover, the cell wall may comprise more than 40% of plant dry biomass, indicating that it is a large reservoir of organic compounds (Vogel and Jung, 2001). However, the main problem is that lignocellulosic biomass is resistant to breakdown and expensive pretreatment is necessary to obtain fermentable sugars. Intensive research aimed at

16

decreasing plant cell-wall recalcitrance has been carried out in recent decades (Phitsuwan et al., 2013). Much of the research on enhanced biomass production has been carried out on model plants, mainly A. thaliana (Gonzales et al., 2009), but plants that are important from an agricultural point of view have also been genetically modified. Increased biomass production is a polygenic trait and intensive research into identifying the so called quantitative trait loci (QTL) responsible for higher biomass yield in major crops has been carried out (Fernandez et

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al., 2009; Jakob et al., 2009). The knowledge concerning the QTLs of crop plants may be then used in traditional breeding for crossing selected cultivars, but there is also ongoing research aimed at mapping certain genes, which may then be used for obtaining transgenic plants

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(Salvi and Tuberosa, 2005; Xu, 1997). Such a strategy was used for example to increase

nitrogen use efficiency in maize (Hirel et al., 2011) or rice improvement (Jena and Nissila, 2017).

There are many approaches to the modulation and development of plant growth to

U

obtain more biomass. Growth improvement may be due to enhanced cell division or the

N

formation of larger cells (Gonzalez et al., 2009). However, the positive output in the latter

A

case is questionable, as transgenic plants displaying this trait usually contain more water, while there is no increase in dry biomass production (van Camp, 2005). Increased biomass

M

production can also be obtained via a change in plant architecture, for example promotion of branching or more erect leaves. The latter trait enables plants to grow in high density and thus

ED

a higher yield per ha can be obtained. It improves light penetration into the canopy as well. (Fernandez et al., 2009). There is also the possibility of making plants grow faster, but usually

PT

in this case they enter into the flowering phase earlier and the final size of transgenic plants is similar to that of wild type plants (Safra-Dassa et al., 2006). The other approach is to regulate

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the onset of the generative phase. The delay in flowering usually leads to an increase in vegetative organ biomass due to the assimilates being allocated differently (Sticklen, 2006). This trait could be useful when green parts are the desired product, for example in the case of grasses used for biofuel production where the onset of flowering terminates apical growth

A

(Fernandez et al., 2009). Other approaches focus on the modulation of carbohydrate synthesis and transport, metabolism of macronutrients or phytohormones (Ciura and Kruk, 2018; Ferrante et al., 2017; Sonnewald and Fernie, 2018).

2.1. RNAs and proteins affecting the growth and development of plants

17

2.1.1. miRNAs and transcription factors regulating plant growth

The participation of miRNAs in the regulation of plant development has been the subject of intensive research (Garcia, 2008). The majority of miRNAs regulate plant growth and development by controlling the expression of genes that encode TFs (Fu et al., 2012). It is known that miR396 regulates the expression of the gene encoding GROWTH REGULATING FACTOR 2 (GRF2). A. thaliana synthesizing modified GRF2 protein, which is not silenced

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by miR396, developed larger leaves due to the stimulation of cell proliferation (Rodriguez et al., 2010). Most members of the SQUAMOSA PROMOTER BINDI]NG PROTEIN LIKE

(SPL) transcription factor family are targets of miR156 (Fu et al., 2012). Transgenic A.

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thaliana, which overexpresses miR156b, displayed delayed flowering and weakened apical dominance, which resulted in a substantial increase in the total number of leaves (Schwab et

al., 2005). This miRNA was also overexpressed in switchgrass (Panicum virgatum) (Fu et al., 2012), a C4 grass that has been suggested to be a major perennial species for biomass

U

production in the USA (Yuan et al., 2008). Low overexpression of miR156 precursor caused

N

an increase in biomass yield without a delay in flowering, moderate levels resulted in

A

improved biomass production, but the plants were non-flowering, whereas high levels of this miRNA led to stunted growth in the transgenic plants (Fu et al., 2012). Overexpresion of

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miR164b-resitant OsNAC2 gene, in rice improved plant architecture and caused the significant increase in grain yield (Jiang et al., 2018).

ED

Several experiments concerning the impact of the overexpression of different TFs simultaneous overexpression of genes that encode GRF5 and its interacting protein

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ANGUSTIFOLIA 3 resulted in plants developing larger leaves that contained more cells (Horiguchi et al., 2005), while simultaneous expression of two other members of the GRF

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family, GRF1 and GRF2, led to the development of larger leaves through enhanced cell expansion (Kim et al., 2003). Overexpression of AINTEGUMENTA or ARGOS, proteins involved in signaling upstream of NAC1 (acronym from NAM, ATAF1 and 2, and CUC2) transcription factor, resulted in enhanced cell division and larger organs (Hu et al., 2003;

A

Mizukami and Fischer, 2000). On the other hand, AUXIN RESPONSE FACTOR 2 (ARF2) and protein encoded by rotunda2 gene are TFs that repress plant growth. Mutation of these factors leads to an enhancement of cell expansion and in the case of ARF2, also to increased seed production and delayed senescence (Cnops et al., 2004; Schruff et al., 2006). The overexpression of BIOMASS YIELD 1(BMY1) gene, which encodes a protein belonging to the APETALA2/Ethylene Response Factor family and BIOMASS YIELD 2 (BMY2) gene, which

18

encodes a protein of the Nuclear-Factor Y family in switchgrass resulted in a significant increase in biomass production (Ambavaram et al., 2008). The WFP (WEALTHY FARMER’S PANICLE) gene, which encodes OsSPL14 (SQUAMOSA PROMOTER BINDING PROTEIN-LIKE 14, called also IPA1), has been identified as a gene that regulates panicle branching in rice. Expression of its allele from the cultivar that displayed enhanced panicle branching in the other cultivar led to the promotion of panicle branching and, as a result, an increase in grain yield of transgenic plants (Miura et al., 2010). Much research concerning

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plant TFs focusses on their use in in improving stress tolerance, therefore they were discussed in section 3.

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2.1.2. Proteins stimulating cell division or expansion

Division of cells, which is a prerequisite for organism growth, is strictly regulated by proteins controlling progression of the cell cycle. These proteins were manipulated to investigate their

U

impact on plant growth. Armadillo-BTB Arabidopsis Protein 1 (ABAP1) controls the

N

proliferation rate of cells by limiting DNA replication. A. thaliana with reduced ABAP1

A

expression developed larger leaves with more cells (Masuda et al., 2008). Overexpression of the gene encoding cyclin D2 from A. thaliana in tobacco resulted in a shortening of the G1

M

phase of the cell cycle and as a consequence an increase in the rate of cell division. Transgenic tobacco grew faster, but also started flowering earlier and the final size of the

ED

plants was similar to that of control plants (Cockcroft et al., 2000). Strategies for enhancing cell expansion are usually based on the expression of cell-

PT

wall loosening proteins. For example, the expression of expansin 10 in A. thaliana led to an increase in leaf size due to the formation of larger cells (Cho and Cosgrove, 2000). Attempts

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to obtain overexpression of the gene encoding poplar cellulase in poplar resulted in the transgene being silenced, but overexpression of this gene in A. thaliana was successful. Transgenic plants produced larger rosettes and had more leaves that were larger than those of the wild type (Park et al., 2003). The expression of cellulase from A. thaliana in poplar led to

A

significant phenotypic alterations, such as increased height, leaf size, stem diameter, wood index and dry weight, when compared to the control. However, the measurements were performed on young plants, so it is unknown how this modification affects the fitness of older trees (Shani et al., 2004). Accelerated growth was also observed in tobacco that overexpress cellulase (Levy et al., 2002). Interestingly, the overexpression of novel extensin-like

19

(OsEXTL) gene in rice resulted in the enhancement of lodging resistance by the reduction of cell elongation and the increase in cell wall thickness (Fan et al., 2018).

2.1.3. Changes in the developmental stage and photomorphogenic responses

When the main product is vegetative tissue, a delay in flowering is a promising strategy to improve yield. Overexpression of FLOWERING LOCUS C, an Arabidopsis flowering-time

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gene in tobacco led to a significant delay in the onset of the generative phase and an increase in biomass yield (Salehi et al., 2005). Experiments on the role of three other flowering-time

genes of A. thaliana, SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1),

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FLOWERING LOCUS T (FT) and FRUITFULL (FUL) were carried out. Double mutants of SOC1 and FUL or FT and FUL displayed prolonged, indeterminate activity of the apical meristem and an increase in activity of the vascular cambium. This led to a significant

increase in the vegetative growth of mutants (Melzer et al., 2008). A delay in flowering,

U

accompanied by increased height was also observed in transgenic tobacco that overexpresses

N

the CENTRORADIALIS homologue from Antirrhinum (Amaya et al., 1999).

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The other approach is to delay leaf senescence, prolonging the period when leaves produce photoassimilates. Transgenic tobacco plants with chloroplastic expression of gene

M

encoding acetyl-CoA carboxylase, a key enzyme that regulates the rate of de novo fatty acid biosynthesis in plants, displayed increased fatty acid content in leaves and prolonged leaf

ED

longevity that was accompanied by a twofold increase in seed yield (Madoka et al., 2002). Silencing photomorphogenic responses, such as increased stem elongation, reduced

PT

branching, leaf thickness, chlorophyll synthesis and accelerated leaf senescence, via the manipulation of phytochrome content enables growth at higher densities and thus an increased

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yield. Transgenic tobacco and potato with overexpression of genes that encode phytochrome A and B, respectively, were obtained and yield improvement was found for potato in field trials (Boccalandro et al., 2003). In recent years, knowledge concerning the participation of photoreceptors in plant growth regulation and the control of shade avoidance has been widely

A

extended, and there have been successful attempts to manipulate genes that encode photoreceptors, mostly phytochromes, and auxin-related genes to enhance growth and productivity in crop plants, such as rice, maize, wheat, barley, soybean, tomato and potato (Carriedo et al., 2016; Mawphlang and Kharshiing, 2017).

20

2.2. Metabolic regulation

2.2.1. Modulation of sugar metabolism and transport

An important method for improving yield via genetic engineering is based on the modulation of sugar metabolism or assimilate translocation in plants (Sonnewald and Fernie, 2018). It is known that there is a negative feedback regulation of photosynthesis by its end-products.

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Therefore, enhancing sucrose synthesis in source organs was verified as a strategy for increasing plant production (Chang and Zhu, 2017). The leaf-specific overexpression of gene encoding maize sucrose-phosphate synthase (SPS) in tomato led to earlier fruit maturity and

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higher fruit dry weight when transgenic plants were grown at a low CO2 concentration (Micallef et al., 1995). In search for genes responsible for growth stimulation in rice it was found that plants with faster growth rate showed increased expression of OsSPS1 gene. The other genes identified in these experiments were responsible for NH4+ uptake (Nagai et al.,

U

2016). The simultaneous expression of the three genes encoding enzymes involved in sucrose

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metabolism, i.e. UDP-glucose pyrophosphorylase, sucrose synthase and SPS in tobacco

A

resulted in enhanced growth (Coleman et al., 2010).

The modulation of enzymes directly or indirectly involved in the conversion of

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sucrose to starch was often used to enhance sink strength and make plants allocate more assimilates to organs like seeds or tubers. Downregulation of plastidal adenylate kinase in

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potato resulted in an increase in starch content and tuber yield (Regierer et al., 2002). The rate limiting step in starch synthesis is due to ADP-glucose pyrophosphorylase (AGP) inhibited by

PT

orthophosphate. The introduction of bacterial or modified AGP, which is less sensitive to inhibition, caused an increase in seed yield in maize, potato, wheat and rice (Smidansky et al.,

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2003; Wang et al., 2007). In wheat and rice, not only seeds but also whole plant biomass increased, which is thought to result from a reduction in the feedback inhibition of photosynthesis by sugars (Smidansky et al., 2003). Moreover, stimulation of phloem unloading was achieved using transgenes that encode enzymes responsible for sucrose

A

cleavage at sink organs, i.e. apoplastic invertase and sucrose synthase (Baroja-Fernández et al., 2009; Heyer et al., 2004; Maloney et al., 2015) or transport of sugar phosphates (Zhang et al., 2008). Transgenic tobacco that produces maize pathogenesis-related protein 1 (PR-1; expression of PRms cDNA under 35S promoter) displayed faster growth and increased seed and leaf biomass. It was shown that PR-1 was associated with plasmodesmata in leaves of

21

transgenic tobacco and that its overexpression increased sucrose efflux from leaves and altered photoassimilate partitioning (Murillo et al., 2003). A recent and promising direction for research concerns trehalose-6-phosphate (T6P), which plays a central sugar signaling role in plants regulating sucrose allocation and metabolism (Paul et al., 2017). It was shown that improved photosynthesis increases the yield only when the assimilates are directed to the desired plant organs, such as grains in the case of wheat. It was found that T6P regulates the activity of the feast-famine protein kinase (SnRK1)

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which controls plant metabolism. Binding T6P to SnRK1 reduces its activity and this stimulates anabolic processes, growth and development. On the other hand, low T6P is a

starvation signal that up-regulates sucrose translocation to sinks (Paul et al., 2017).

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Overexpressing rice T6P phosphatase in developing maize ears using a floral promoter led to

an increase in yield (Nuccio et al., 2015). The development of plant-permeable analogues of T6P which release T6P in plant tissue was an important achievement. Applying these precursors to the ears of wheat up-regulates starch synthesis in grains and increases the yield,

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while applying them to vegetative tissue enhances drought recovery (Griffiths et al., 2016).

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The state of the art knowledge concerning source to sink relation and modification in crop

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2.2.2. Nutrient metabolism

A

plants has been recently reviewed by Sonnenwald and Fernie (2018).

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The other approach to improve plant productivity is to increase the availability of key nutrients. Most work in this area of research has focused on enhancing nitrogen assimilation

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(Hirel et al., 2011). Among macroelements, nitrogen is required in the highest amounts, as it is used to synthesize proteins and nucleic acids. World-wide use of nitrogen fertilizers is about

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90 million metric tons and nitrogen fertilizers are a major cost in agricultural production (Bi et al., 2009). The photosynthetic capacity of plants strongly depends on this macronutrient. Proteins participating in photosynthesis, especially Rubisco, consume the majority of leaf nitrogen. There is a correlation between total leaf nitrogen and Rubisco content and a strong

A

linear relationship between nitrogen and chlorophyll content (Evans, 1989). The supply of nitrogen also has a regulatory impact on CO2 assimilation and sugar partitioning (Foyer and Ferrario, 1994). Nitrate ions present in soil, which are the main source of nitrogen for most plant species, are reduced within cells in two-steps by nitrate and nitrite reductases, resulting in the formation of ammonium ions. To examine the impact of the increased activity of nitrate

22

reductase (NR) on plant metabolism, the gene from tobacco was expressed in potato under the control of constitutive 35S promoter. Native NR is inactivated by phosphorylation, but the transgene encoding N-terminal truncated protein cannot be downregulated this way. Transgenic plants displayed an increase in biomass accumulation, especially in tubers (Djennane et al., 2004). There are two pathways for ammonium assimilation into organic compounds. The first is an amination of -ketoglutarate catalyzed by glutamate dehydrogenase. Overexpression of

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the gene encoding this enzyme from E. coli in tobacco led to an increase in biomass production both under controlled conditions and in the field (Ameziane et al., 2000).

However, in most plants ammonium is assimilated into amino acids through the GS-GOGAT

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cycle, named after two enzymes involved in this cycle, glutamine synthetase (GS) and

glutamate synthase (GOGAT) (Chichkova et al., 2001). Overexpression of the gene encoding cytosolic isoform of GS, called GS1, from pine in poplar caused an increase in total soluble proteins, chlorophyll content and growth enhancement (Gallardo et al., 1999). In further

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experiments, poplar that expresses conifer GS1 gene has been grown under natural conditions

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for 3 years and an increase in growth was observed in transgenic trees (Jing et al., 2004).

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Stimulation of growth in transgenic poplar occurred under both low and high nitrate conditions (Man et al., 2005). Transgenic tobacco, overexpressing GS1 from pea in leaf

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mesophyll, displayed an increase in leaf soluble protein, as well as in fresh and dry biomass under nitrogen-limiting and nitrogen-non-limiting conditions (Oliveira et al., 2002).

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Another approach to modulate plant nitrogen metabolism was to overexpress gene encoding barley alanine aminotransferase in rice. Alanine aminotransferase acts downstream

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of the pathway of ammonium assimilation. It catalyzes transfer of NH2 group from glutamine to pyruvate leading to the formation of alanine which is an intercellular nitrogen and carbon

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shuttle. This modification caused an increase in biomass and grain yield of the transgenic plants (Shrawat et al., 2008). The genes which have an impact on plant nitrogen use efficiency (NUE), as well as the strategies for NUE improvement have been reviewed by Li et al.

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(2017).

Besides nitrogen, there have also been attempts to modulate phosphorus metabolism

(Veneklaas, et al., 2012). This macronutrient is necessary for the synthesis of nucleotides, phospholipids and some coenzymes. It is also crucial for ATP synthesis and signal transduction. Plant purple acid phosphatases (PAPs) are thought to mediate phosphorus acquisition and redistribution (Sun et al., 2012). Overexpression of mitochondria- and plastidtargeted A. thaliana PAP2 gene in Arabidopsis caused faster growth, earlier onset of the 23

generative phase, increased seed yield and dry weight. It was observed that transgenic plants displayed increased SPS activity (Sun et al., 2012). The same effect was observed when PAP2 of A. thaliana was overexpressed in Camelina sativa (Zhang et al., 2012).

2.3. Engineering of phytohormones for improved plant productivity

Phytohormones regulate developmental stages of plants and their responses to environmental

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conditions (Fahad et al., 2015; Wani et al., 2016). Therefore, engineering of gibberellins (GA), cytokinins (CK), auxins (Aux), brassinosteroids (BR) and jasmonates (JA) seems to be a promising tool in improving the productivity of plants. In the regulation of the level of

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phytohormones, both their synthetic and catabolic pathways can be targets for the engineering.

Gibberellins are one of the most promising targets that affect plant size and biomass production. The synthesis, catabolism and signaling pathways of GA can be manipulated for

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this purpose (Fernandez et al., 2009). So far, the main biotechnological targets have been GA

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20-oxidases and GA 3-oxidases, catalyzing the last two steps of GA biosynthesis, and GA 2-

A

oxidase, which converts GA to inactive metabolites (Bou-Torrent et al., 2011) (Table 1). Cytokinins, regulating many aspects of plant growth and development, have long been

M

considered to affect plant yield and productivity. The main targets of CK engineering are genes involved in CK synthesis (IPT encoding isopentenyl transferase) and metabolism (CKX

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encoding cytokinin dehydrogenase and the genes of glucosyltrasferases) (Frébort et al., 2011; Zalabák et al., 2013). CK are key factors responsible for regulating plant senescence.

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Delaying the senescence is one of the strategies for improving plants’ yield by extending their lifetime. For the first time, senescence-specific promoter (PSAG12) from Arabidopsis fused with

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the IPT gene, was used for tobacco transformation, which resulted in an increased number of flowers, seed yield, biomass and reduction of leaf and floral senescence (Gan and Amasino, 1995). Since then, SAG12 and other SAG promoters have been widely used in vectors for the transformation of plants. The Senescence Associated Receptor Protein Kinase (PSARK)

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promoter, which is induced by stress and during maturation, is another promoter used successfully in the production of transgenic plants with elevated CK content (Peleg et al., 2011). Examples of transgenic plants with the modified CK levels to improve plant yield and productivity are shown in Table 1. The application of inducible promoters for the conditional expression of CK-biosynthetic genes allows the hormone levels to be controlled without the

24

negative effects on growth and development of plants, caused by a high content of this phytohormone (Peleg and Blumwald, 2011). Auxins regulate a wide variety of growth and developmental processes in plants, including

differentiation

of

vascular

tissues,

apical

dominance,

root

formation,

embryogenesis, phyllotaxis and tropic responses. Genes involved in the biosynthesis of Aux and Aux-related signal transduction have become promising biotechnological targets for modifying plant size and shape, as well as improved yield (Busov et al., 2008). For example,

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the transgenic potato that overexpresses the Arabidopsis AtYUC6 gene, exhibited high-auxin phenotype such as increased height, erect stature, longevity and enhanced drought tolerance (Kim et al., 2013) (Table 1).

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Brassinosteroids are phytohormones of very broad physiological functions (Bartwal et al., 2013). Mutants defective in BR synthesis or signaling show dwarf phenotypes, whereas

increased production of BR can result in higher biomass, plant size and seed yield. These phytohormones have also been found to be involved in adaptive tolerance to environmental

U

stress (Bajguz and Hayat, 2009). Genetic manipulation of BR biosynthesis and signaling

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could allow a significant increase in crop yield through changing both plant metabolism and

A

their stress tolerance (Divi and Krishna, 2009). For example, overexpression of DWF4/DWARF4, encoding steroid 22α-hydroxylase (CYP90B1) − one of the enzymes

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involved in brassinosteroid biosynthesis, in transgenic Arabidopsis resulted in an increase in plant size by 35-47% and seed production up to 59% (Choe et al., 2001). In the case of

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transgenic rice with overexpressed gene that encodes sterol C-22 hydroxylase, an increase in grain yield in the range of 15-44% was observed (Wu et al., 2008) (Table 1).

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Jasmonates (jasmonic acid and its derivatives) are lipid-derived compounds that play a key role in stress responses and developmental processes. These phytohormones are involved

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in physiological responses to wounding, herbivores and pathogen attack, as well as to salinity, drought and cold stress (Wasternack, 2014; Wani et al., 2016). In the transgenic approach, one of the targets is jasmonic acid carboxyl methyltransferase (JMT) which participates in the formation of methyl jasmonate (Table 1). Overexpression of the JMT gene increased tuber

A

yield and size in transgenic potato (Sohn et al., 2011).

2.4. Other targets for increasing biomass production Several processes that follow transcription can be modulated to improve plant growth. Deoxyhypusine synthase (DHS) is an activator of the eukaryotic translation initiation factor 5A that regulates the translocation of mRNA from the nucleus to cytoplasm. Suppression of 25

DHS expression in A. thaliana caused pleiotropic effects, such as increased rosette size and root biomass, as well as a delay in the onset of the flowering phase and delayed leaf senescence (Wang et al., 2003). Further research demonstrated that leaf-specific silencing of DHS expression in A. thaliana enabled growth enhancement without negative effects, such as stunted reproductive growth and reduced seed yield (Duguay et al., 2007). Overexpression of the gene that encodes TOR kinase, which participates in the regulation of translation, resulted in an increase in the cell and organ size of transformed A.

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thaliana (Deprost et al., 2007). EBP1, a protein that plays a role in the regulation of synthesis and assembly of translational machinery, has been postulated to act downstream of TOR

kinase (Deprost et al., 2007; Horvath et al., 2006). A. thaliana overexpressing the EBP1 gene

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from tomato had larger leaves and this effect resulted from stimulating cell division and expansion. The overexpression of potato EBP1 in potato caused an increase in plant size due to the promotion of cell expansion (Horvath et al., 2006).

Protein degradation is another process that has been engineered. A. thaliana plants that

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carry a mutation in the DA1 gene, encoding ubiquitin receptor, had larger leaves and produced

N

more numerous and larger seeds. This is a result of a prolonged cell proliferation time leading

A

to an increase in the number of cells (Li et al., 2008). The mutation in the E3 ubiquitin ligase BIG BROTHER/ENHANCER OF DA1, in the da1 A. thaliana mutant, synergistically

M

enhanced seed and leaf size (Li et al., 2008b).

It is supposed that prohibitins might also be important factors that regulate biomass

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production. These proteins, which are found in nucleus and mitochondria, regulate development and senescence, and are also involved in the response to phytohormones. Plants

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displaying decreased expression of prohibitins showed strong growth inhibition and other abnormalities (Chen et al., 2005).

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One of the key metabolic intermediates is phosphoribosyl pyrophosphate (PRPP), necessary for nucleotide biosynthesis, as well as for the synthesis of His and Trp. The experiments on transgenic A. thaliana and tobacco showed that increased activity of PRPP

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synthetase resulted in a substantial increase in biomass production (Koslovsky et al., 2008). The other promising targets are cystine-rich receptor like kinases (CRK), which take

part in signal perception and transduction (Shiu et al., 2001). The role of CRK5 in senescence and stress response has also been demonstrated. The crk5 mutant plants showed lowered biomass, elevated ROS production or accelerated senescing, while plants overexpressing CRK5 in the mutant background showed increased biomass production (Burdiak et al., 2015).

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3. Transgenic plants with elevated resistance to abiotic stresses

Environmental stress tolerance is one of the key factors determining crop productivity in changing climate conditions, therefore extensive studies are being undertaken to create transgenic plants with elevated abiotic stress resistance. Various abiotic stresses such as excess light, drought, salinity, extreme temperatures, nutrient deficiency, metal toxicity, soil hypoxia (flooded area and compact soil) or UV-B

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radiation result in redox homeostasis being disturbed and the elevated production of reactive oxygen species (ROS), causing oxidative damage to cellular components. The main reason for the increase in ROS generation under stress conditions is that the photosynthetic apparatus is

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very efficient in capturing light, whereas the other processes are more prone to be disturbed

during stress exposure, resulting in an imbalance between light absorption and energy utilisation in metabolism (Hüner et al., 1998). In response to environmental stresses, various enzymatic and non-enzymatic antioxidants are synthesized to counteract the harmful effects

U

of ROS (Foyer and Noctor, 2011; Szymańska et al., 2017).

N

As many abiotic stress factors, like drought, salinity or cold, often induce common

A

effects in plants (e.g. ROS formation, synthesis of osmoprotectants, expression of genes encoding TFs), transgenic plants with elevated levels of antioxidants, osmoprotectants or TFs

M

frequently show increased resistance to a variety of abiotic stresses. The data presented in Table 2 indicate that abiotic stress tolerance of the transgenic

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plants is found in a broad range of stress intensities, from mild to severe stress conditions, as well as in a broad time scale of stress duration, from hours to days in the greenhouse, even to

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whole vegetative season in field experiments. These results are important taking into consideration that for practical application of transgenic crops, the abiotic stress tolerance is

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required in a broad range of stress severity and duration time.

3.1. Photooxidative stress

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Among abiotic stresses, light stress is one of the most important environmental factors limiting the efficiency of photosynthesis and plant productivity (Reddy and Raghavendra, 2006). When absorbed light energy exceeds the capacity for light energy utilization, photosynthetic efficiency is reduced due to quenching mechanisms and ROS formation. Elevated synthesis of antioxidants under these conditions might not provide sufficient protection during prolonged stress. Therefore, engineering plants with increased production of

27

various antioxidants in different cellular compartments is a way to create plants with increased resistance to photo-oxidative stress. There are many examples where the overexpression of various antioxidant enzymes increased photooxidative stress tolerance, using mainly methylviologen to induce ROS production in photosystem I. Among target antioxidant enzymes were various superoxide dismutase (SOD) isoforms (Bowler et al., 1991; Perl et al., 1993; Slooten et al., 1995), ascorbate peroxidase (APX) (Murgia et al., 2004), glutathione peroxidase (GPX) (Yoshimura, 2004), glutathione-S-transferase (GST) (Roxas et al., 1997), catalase (CAT), glutathione

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reductase (GR) and others (Kuźniak, 2002). Transgenic tobacco engineered to accumulate mannitol in chloroplasts was more tolerant to photooxidative stress due to the scavenging of

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hydroxyl radicals by mannitol (Shen et al., 1997). Among non-enzymatic antioxidants, elevated synthesis of ascorbate (Zhang et al., 2011), glutathione (Noctor et al., 1998) and plastoquinol (Ksas et al., 2015) provided increased tolerance of plants to photooxidative stress. Another target in this approach was plastid terminal oxidase (PTOX) which functions

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as an electron sink from photosynthetic electron transport to prevent photooxidative damage

N

under stress conditions. Therefore, PTOX seemed to be a good candidate for engineering

A

stress-tolerant plants, although the PTOX-overexpressing plants that have so far been obtained did not show any increase in stress resistance (Johnson and Stepien, 2016).

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As many other abiotic stresses also cause elevated ROS production, transgenic plants with increased levels of enzymatic antioxidants often show resistance to other stresses, like

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drought, salinity, cold or heat stress (Panda et al., 2014 and ref. therein).

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3.2. Drought and salinity stress

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Drought stress is considered to be the main cause of crop yield loss, causing elevated ROS production and growth inhibition, which is often accompanied by heat or other stresses. Salinity is another major constraint to agriculture causing osmotic and ionic imbalance that perturbs the metabolism and leads to increased ROS production and upregulation of many

A

antioxidant enzymes (Hossain and Dietz, 2016). Under osmotic stress caused by drought, salinity or cold stress, plants accumulate

osmolytes such as proline, sucrose, soluble carbohydrates, betains, trehalose, fructans, sugar alcohols (mannitol, sorbitol), polyamines and protective proteins (dehydrins/LEA proteins). These compounds maintain cell turgor and impose protective effects on proteins under osmotic stress. Among other factors that play a key role in the response of plants to drought

28

and salinity stress are TFs that are also involved in crosstalk among abiotic stress responses, such as drought, cold, salinity and heat (Nakashima et al., 2014, Joshi et al. 2016). One of the major challenges regarding the role of TFs in abiotic stress tolerance is to elucidate the interactions of the most important TFs. This will provide a greater appreciation of the complexity of the gene networks and perhaps identify important hubs for the regulation of these networks. Therefore, both the osomolytes and TFs are the most promising targets for

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engineering stress tolerant crops (Table 2).

3.2.1. Drought stress

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The main target genes whose expression was successfully manipulated in the production of

crops with elevated drought tolerance have been e.g. those of TFs (DREB1/CBF, DREB2, AREB/ABF, bZIP, NAC, MYB, WRKY and others) (Ning et al., 2017; Reddy et al., 2014; Ribichich et al., 2014), transcriptional coregulators (OsSKIPa, OsRIP18) (Hu and Xiong,

U

2014), kinases of signalling pathways (e.g. MAPK, CPK, SOS2, SnRK2), enzymes of

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osmoprotectants synthesis (trehalose, proline, mannitol), enzymes of phytohormone

A

metabolism, dehydrins/LEA proteins, polyamines (Pathak et al., 2014), antioxidant enzymes (Diaz-Vivancos et al., 2016; Roy et al., 2014), aldose reductase (Feher-Juhasz, 2014), ion

M

transporters (Na+/H+ antiporter, V-H+-PPase) or aquaporins (Ayadi et al., 2011; Putpeerawit et al., 2017) (Table 2).

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In particular, DREB (dehydration-responsive element-binding factor of ABAindependent pathways) TFs are promising targets for engineering drought tolerant crops when

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appropriate tissue-specific, drought-inducible promoters are used to avoid undesired side effects. Overexpression of genes encoding DREB/CBF TFs has been reported to enhance

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drought tolerance in transgenic crops of many species, including wheat, peanut, soybean, tobacco and tomato (Hu and Xiong, 2014). On the other hand, DREB2s function in both dehydration and heat shock stress responses (Nakashima et al., 2014). Overexpression of genes that encode NAM, ATAF and CUC (NAC) TFs enhanced drought resistance and salt

A

tolerance in rice under field conditions (Hu et al., 2006). Constitutive overexpression of the genes for the kinase domain of NPK1, a tobacco

MAPK kinase kinase (MAPKKK), in maize resulted in enhanced drought tolerance of transgenic lines at high photosynthesis rates (Shou et al., 2004). When the LOS5/ABA3 gene, coding the key enzyme of ABA biosynthesis, was overexpressed in rice, the transgenic plants showed improved grain yield under drought stress conditions in the field (Xiao et al., 2009).

29

LOS5 also showed a positive effect in improving drought resistance when overexpressed in soybean and cotton (Li et al., 2013; Yue et al., 2012b). Overexpression of a gene encoding 1-pyrroline-5-carboxylate synthetase (P5CS), the rate-limiting enzyme in proline biosynthesis, resulted in improved drought tolerance of transgenic rice (Zhu et al., 1998). Zhang et al. (2014) cloned a MnSOD gene from Tamarix androssowii, an extremely drought-tolerant Chinese shrub, and introduced it into cotton. Under drought stress, transgenic lines produced more proline and soluble sugars and showed a

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higher level of physiological performance and total biomass than control plants (Zhang et al., 2014).

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3.2.2. Salinity stress

Target genes that are of interest for producing transgenic crop plants with elevated salinity resistance are frequently the same as those manipulated for enhanced drought stress tolerance

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(Table 2) (Roy et al., 2014), i.e. genes encoding TFs (DREBs, MYB, NAC) (Reddy et al.,

N

2014; Ribichich et al., 2014), components of signalling pathways (CIPK, MAPK, SnRK2),

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enzymes involved in the synthesis osmoprotectants (trehalose, mannitol, myo-inositol, glycine betaine, proline), dehydrins/LEA proteins (functioning as protectant proteins/chaperons),

M

antioxidant enzymes, polyamines (Pathak et al., 2014) or aquaporins (Ayadi et al., 2011; Liu et al., 2013). Besides the above mentioned, other targets include systems of ion exclusion

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from cells supported by Na+ transporters (SOS - salt overly sensitive, HKT - high affinity potassium transporter, Na+ ATPase) and vacuolar Na+ compartmentation, supported by

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vacuolar Na+/H+ antiporters (NHX) and vacuolar H+ pyrophosphatases (AVP1) (Table 2). For instance, the expression of Atriplex hortensis BALDH gene (betaine aldehyde

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dehydrogenase) in rice increased glycine betaine level and salinity tolerance (Guo et al., 1997). Transgenic plants that overexpress genes that encode antioxidant enzymes, such as GST/GPX, MDAR, APX, SOD, DHAR, CAT (Hossain and Dietz, 2016; Roxas et al., 1997; Roy et al., 2014) or have an elevated content of non-enzymatic antioxidants such as ascorbate

A

(Zhang et al., 2015), showed increased tolerance to salinity. It has been recently shown that the gene of tonoplast intrinsic protein (TIP) isoform

(CsTIP2;1), belonging to aquaporins, is highly expressed in the leaves and roots of citrus plants subjected to salt and drought stress (Martins et al., 2017). Overexpression of this gene in transgenic tobacco increased plant growth under normal, drought and salt stress conditions. Moreover, CsTIP2;1 significantly improved the leaf water and oxidative status,

30

photosynthetic capacity, transpiration rate and water use efficiency of plants subjected to soil drying (Martins et al., 2017). Salinity stress resistance of transgenic plants is often accompanied by resistance to other stresses, such as drought (Bao et al., 2009; Pasapula et al., 2011; Wu et al., 2005) or cold stress (Gao et al., 2009; Holmström et al., 2000). In particular, the increased synthesis of trehalose (Suárez et al., 2009; Garg et al., 2002), CIPK (Wang et al., 2012) or DREB TFs

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(Gao et al., 2009; Joshi et al., 2016) confer broad abiotic stress tolerance.

3.3. Cold stress

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Cold and freezing stress cause similar biochemical responses to those of drought and salt

stress, i.e. increased disturbance of redox homeostasis resulting in the elevated formation of ROS, increased synthesis of enzymatic and non-enzymatic antioxidants, accumulation of osmoprotectants, such as sugars (sucrose, raffinose, stachyose, fructans, trehalose), sugar

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alcohols (sorbitol, ribitol, inositol), aminoacids and their derivatives (proline, glycine betaine),

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dehydrin proteins, heat-shock proteins (HSP) proteins, pathogen-related (PR) proteins, etc.

A

(Janska et al., 2010).

During acclimation to low-temperatures, besides the accumulation of soluble sugars in

M

cells, the content of polyunstaturated fatty acids in membranes increases to maintain the proper membrane fluidity (De Palma et al., 2008). These physiological reactions have been

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used for the metabolic engineering of crops with elevated cold resistance. Overexpression of the plastidal -3 fatty acid desaturase gene, involved in linolenic acid synthesis, in transgenic

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tobacco provided increased chilling tolerance (Kodama et al., 1994). Moreover, overexpression of the gene encoding glycerol-3-phosphate acyl transferase altered the

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unsaturation of fatty acids and conferred chilling tolerance in transgenic plants (Sakamoto et al., 2003; Sui et al., 2007) (Table 2). Other approaches relied on antioxidant enzymes, such as SOD (McKersie et al., 1993;

Sanghera et al., 2011) or synthesis of osmoprotectants, such as glycine betaine (Holmström et

A

al., 2000; Sakamoto and Murata, 1998) or proline (Sanghera et al., 2011). Transgenic rice that expresses the genes of cold shock proteins (CSPs) from bacteria showed improved stress tolerance in the case of a number of abiotic stresses, including cold, heat, and water deficits (Sanghera et al., 2011). Furthermore, RAN1, which belongs to the G-protein family, has been shown to improve cold-tolerance in rice (Xu and Cai, 2014).

31

TFs are promising targets for modifying the cold- and freezing tolerance of crop plants (Sanghera et al., 2011). DREB1/CBF are cold-inducible TFs, whose genes also confer drought- and salt-resistance when overexpressed under proper promoters (Nakashima et al., 2014). This has been shown in Arabidopsis and rice. Plants that overexpress CBF3 show a constitutive accumulation of cold acclimation response (COR) proteins and increased accumulation of both proline and sucrose, developed higher freezing tolerance (Jaglo-Ottosen et al., 1998; Kasuga et al., 1999; Liu et al., 1998). Overexpression of the gene that encodes

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zinc finger protein SCOF-1 resulted in enhanced low temperature tolerance in transgenic Arabidopsis and tobacco (Kim et al., 2001). Recently, the genes of WRKY TFs were shown to

have cold stress-induced expression in Vitis vinifera (Wang et al., 2014). The other examples

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are given in Sanghera et al. (2011), Reddy et al. (2014) and Ribichich et al. (2014).

3.4. Heat stress and other stresses

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Elevated temperature in plants mainly causes protein deactivation. Especially sensitive in this

N

respect is the oxygen-evolving complex (OEC) of photosystem II (Dhir, 2018; Jiang et al.,

A

2006). The thermostability of the OEC of some thermophilic organisms (cyanobacteria, red algae) results from different extrinsic proteins of the OEC found in these organisms (Bricker

M

2012). Therefore, the extrinsic proteins of the OEC could be of potential interest for future research as targets to obtain more thermotolerant crop species. Of photosynthetic electron

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transport components, PQ-pool is strongly affected by heat stress as well (Pshybytko et al., 2008).

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In response to elevated temperatures, plants synthesize HSP that function as chaperons, ensuring proper folding of other proteins, preserving their function under stress

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conditions. It has been demonstrated that overexpression of HSP genes increases the heat tolerance of Arabidopsis and tobacco (Lee and Schoff, 1996; Park and Hong, 2002). Arabidopsis

plants

engineered

to

overproduce

glycine

betaine,

show

increased

thermotolerance (Alia et al., 1998), suggesting that nitrogenous osmoprotectants can play a

A

role in cellular protection against heat stress. It has also been recently shown that Cornus canadensis expressing superoxide reductase gene from the hyperthermophilic archaeon Pyrococcus furiosus shows enhanced heat tolerance (Geng et al., 2016). Among TFs, DREB2s function in both dehydration and heat shock stress responses. DREB2Aca has been shown to improve thermotolerance, in addition to drought tolerance in rice (Sakuma et al., 2006). Overexpression of HsfA1, which encodes the heat stress

32

transcription factor, in tomato plants causes higher thermotolerance (Mishra et. al., 2002). Increased stress resistance was also observed in transgenic wheat and rice with overexpressed HSP genes (Kuang et al., 2017; Kumar et al., 2016; Xiang et al., 2018). Resistance to other abiotic stresses that have been examined using transgenic plants include heavy metal stress, low-light (shading) stress, UV-B stress or nutrient deficit stress (Rathinasabapathi and Kaur, 2006).

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4. Why do some plants grow faster than others?

Among hundreds thousands of higher plant species there is enormous variation in their growth

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rate, biomass production and the age reached. On the one hand, there are species that grow

extremely slowly, like Pinus longeava and related species, Puya raimondii, Welwitschia mirabilis, for example. On the other hand many weeds, bamboo (e.g. Phyllostachys edulis) and plants often used for biomass production (e.g. Salix sp., Miscanthus sp., Paulownia

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elongata x fortunei hybrid - Oxytree) are known to grow very fast. Despite huge progress in

N

understanding many aspects of plant physiology over recent years, we do not have a

A

satisfactory answer to this question. Thorough knowledge of the factors governing the processes responsible for growth rate, size and the age reached of plants would be of crucial

M

significance for research leading to an improvement in the biomass production of crops. One of the most important determinants of plants height and biomass that have been

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suggested are plant hormones such as giberrelins and brassinosteroids. However, it is obvious that to increase the biomass of plants, enhanced CO2 assimilation and energy demand (ATP

PT

production) are required to synthesize new organic compounds necessary as structural components of new cells, tissues and organs. Therefore, the elevated level of phytohormones

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is certainly not the only factor required to increase the growth rate of plants and their biomass. The growth rate of plants is frequently considered in terms of carbon source-sink

limitations (Burnett et al., 2016, White et al., 2016). It could be expected that in the case of annual plants, which grow fast, the carbon supply will be a limiting factor for their growth,

A

while for perennials, which grow more slowly, carbon utilisation will be limiting. However, recent experiments using two barley species (Burnett et al., 2016), one annual and the other perennial, demonstrated that contrary to expectations, the growth of annual barley was sink limited, while the perennial species was more source limited. This example shows that our understanding of the regulatory processes responsible for the growth rate of plants and biomass accumulation are far from being understood and there is much to be explored in this

33

respect. Nevertheless, the sink-source approach indicates the potential factors that affect the growth rate of plants, their yield and biomass production.

Future directions

The data presented demonstrate that a great variety of targets and approaches have been successfully used to increase the productivity and abiotic stress tolerance of plants, although

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many other challenging ideas are yet to be explored. In the area of photosynthesis research, besides increasing the efficiency of light use and photosynthetic electron transport yield, improving carbon assimilation and limiting its

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loss during photorespiration, are the main points to be addressed in future research. The data

accumulated so far indicate that modifications of Rubisco to obtain higher turnover rates and substrate specificity is not a very promising direction for future research. It would be more worthwhile to focus on the introduction of CCM to crop plants, taking advantage of the CO2

U

transporters found in cyanobacteria or green algae. The implementation of CCM based on

N

enzymes of the C4/CAM cycle seems to be considerably more challenging. Engineering CAM

A

metabolism is theoretically less complicated than that of C4 plants, as the primary and secondary CO2 assimilations do not require the transport of metabolites between cells.

M

As far as growth and biomass yield improvement are concerned, the engineering of phytohormones in particular should be an effective target. Besides, other factors that have

ED

been as of yet poorly investigated, like prohibitins or CRK5, should be explored in this respect. For the improvement of abiotic stress tolerance, 'new' osmoprotectants such as proline

PT

betaine and hydroxyproline betaine or polyamines deserve more attention. Recently, emerging roles in crop yield improvement have been demonstrated for microRNA (miRNA) and small

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interfering RNA (siRNA), which have been shown to be involved in various biotic and abiotic stress responses (Kumar, 2014; Khraiwesh et al., 2012). Furthermore, the key role of TFs in stress responses, that have been demonstrated so far, should be explored more thoroughly in terms of their significance for plant productivity and stress resistance. The other direction is

A

the development of stress-dependent and tissue-specific promoters and the testing transgenic plants over a longer time-scale to examine the persistence of transgenes and the performance of transgenic plants under field conditions. Besides, much effort should be directed towards analyzing the traits responsible for the growth rate and biomass production of many wild species known for their fast growth, such as weeds or others. Author contribution statement

34

BN wrote Introduction and chapters 1 and 2, draw Fig. 1. JC wrote chapter 2.3. RS contributed to chapter 3 and Fig. 1. JK designed the work, wrote chapters 3 and 4, 'Future directions' and improved the whole manuscript.

Acknowledgements

This work was supported by the National Centre of Science of Poland, grant number 2015/19/B/NZ9/00422. The Jagiellonian University is a partner of the Leading National

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Research Center (KNOW) supported by the Ministry of Science and Higher Education.

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DvGS2-transgenic Arabidopsis thaliana. Gene 536, 407-415.

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glutamine synthetase gene DvGS2 from Dunaliella viridis and biochemical identification of

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Table 1 Transgenic plants with altered phytohormones metabolism to ameliorate plant productivity. bGLU - -glucosidase, Pl - Phaseolus lunatus, Pv - Phaseolus vulgaris, Agt Agrobacterium tumefaciens, Bc - Brassica campestris, OE - overexpression. Target Gene/promoter, gene/protein regulation

IPT

GA20ox/35S OE GA20ox/35S OE

hybrid aspen

Biemelt et al., 2004 Eriksson et al., 2000

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Tereshonok et al., 2011 Peleg et al., 2011 Bedada et al., 2016

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A

N

Ashikari et al., 2005 barley higher plant Zalewski et productivity al., 2010 PlZOG1/Ubi OE maize growth inhibition, Pineda Rodó increased root mass and et al., 2008 branching, delayed senescence Brassinosteroids DWF4/pAS rice increased grain yield Wu et al., 2008 Ethylene ACS, down-regulation maize increased grain yield Habben et al., under stresses 2014

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ACC synthase

OsCKX2 reduced expression CKX1 silencing

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DWF

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AgtIPT/SARK

Zeatin glucosyltransferase

faster growth, elevated biomass

Cytokinins wheat higher yield and less growth inhibition during flooding rice increased grain yield and improved drought tolerance maize higher grain yield, increased drought tolerance by delayed leaf senescence rice enhanced grain yield

AgtIPT/35S

AgtIPT/SARK

CKX

Reference

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GA20ox

Target plant Effect species Gibberellins tobacco higher biomass

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Table 2 Transgenic plants of elevated resistance to abiotic stresses. Ag - Arthrobacter globiformis, Hv - Hordeum vulgare, Md - Malus domestica, Nt - Nicotiana tabaccum, Pa - Phaseolus aconitifolius, Pv - Phaseolus vulgaris, Agt - Agrobacterium tumefaciens, Bc - Brassica campestris, Le Lycopersicon esculentum, Sc - Sacharomyces cerevisie, So - Spinacia oleracea, OE - overexpression.

DREB

GhDREB/35S OE

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SNAC1/35S OE

wheat

rice

Effect

Transcription factors enhanced tolerance to drought, high salt, and freezing stress enhanced drought resistance and salt tolerance

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NAC

Target plant species

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Gene origin/promoter, regulation

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Target gene/protein

rice

improved cold and salt tolerance

WRKY

GsWRKY20/35S OE

soybean

Y(NF-Y)B

Zm Y(NF-Y)B/actin1 OE

maize

enhanced drought tolerance and yield increased drought tolerance, improved corn yield in the field

A

SNAC2/35S OE

Ion transporters 62

Stress conditions

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water deprivation for 20 d, 6C for 3 d, 2% NaCl for 7 d vegetative stage (hydroponic cultures): 12 d water withholding, 200 mM NaCl for 12 d and 100 mM NaCl for 5 d (mild stress); reproductive stage: (field conditions): severe stress (soil water content ~15%), moderate stress (~28%) 4C for 5 d, 150 mM NaCl for 14 d, 15% PEG6000 for 14 d water withholding for 14 d

Gao et al., 2009

greenhouse: 10 d drought, 3 d full-water recovery, 9 d drought; field: water withholding during late vegetative stage

Nelson et al., 2007

Hu et al., 2006

Hu et al., 2008

Ning et al., 2017

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NHX (Na+/H+ antiporter) SOS1

150 mM NaCl for 7 d

increased salt tolerance

AVP1

AtAVP1/35S OE

cotton

HKT2

HvHKT2;1/35S OE

improved drought- and salt tolerance and increased fibre yield in the field improved salt tolerance

increasing NaCl conc. from Yue et al., 2012a 50-300 mM during 24 d greenhouse: water Pasapula et al., 2011 withholding for 5 d, 200 mM NaCl for 20-30 d; field: rainfed conditions 50 and 100 mM NaCl for 14 Mian et al., 2011 d

Osmoprotectants improved drought and salt tolerance

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Pa P5CS /AIPC (ABA inducible)

rice

codA (choline oxidase)

AgcodA/35S OE

Arabidopsis

enhanced tolerance to salt and cold stress

codA

AgcodA/35S OE

rice

TPS (trehalose-6phosphate synthase)

ScTPS1/rd29A (stress-inducible)

alfalfa

tolerance to salt and cold stress enhanced tolerance to multiple abiotic stresses

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P5CS

barley

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enhanced salt tolerance

AtSOS1/35S OE

poplar hybrid tobacco

APX (ascorbate peroxidase)

AtAPX/35S OE

tobacco

Antioxidant enzymes enhanced tolerance to salt stress and water deficit 63

4 cycles of water withholding for 6 d with 1 d watering intervals, 100 mM NaCl for 5 d 200 mM NaCl for 10 d, 400 mM for up to 48 h; 5C up to 7 d 150 mM for 7 d; 5C up to 2 h water withholding for 5-30 d; 50-300 mM NaCl; 4C for 5 d followed by -5, -10 and -15C for 6,12,48 and 72 h; 37C for 4 h, followed by 40, 45, 50 and 55C for 1 h

Qiao et al., 2011

Zhu et al., 1998

Hayashi et al., 1997

Sakamoto and Murata, 1998 Suarez et al., 2009

0.3 M NaCl up to 8 d; water Badawi et al., 2004 withholding up to 10 d; 10% PEG up to 8 d

I LEA3-1

Os/35S OE

rice

HVA1

Hv/actin1 OE

NPK1 (MAPKKK)

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tobacco

MAPK

OsMAPK5/35S OE

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MDAR AtMDAR1/35S OE (monodehydroascorbate reductase)

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Nt/35S OE

MdCIPK6L/35S OE

SOS2

AtSOS2/LEA3-1 OE

gid1 (gibberellininsensitive dwarf1)

gid1 mutant

ddf1 (dwarf and delayed-flowering 1)

ddf1/35S OE

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CIPK

rice

enhanced tolerance to ozone, salt and osmotic stresses Dehydrins/LEA proteins less yield loss under severe drought stress in field trials increased drought and NaCl tolerance

0.3 M NaCl up to 8 d; 10% PEG up to 6 d

Eltayeb et al., 2007

severe drought stress (soil water content ~18%)

Xiao et al., 2007

water withholding for 5 d, 2 d recovery, followed by second round of water stress; 200 mM NaCl for 10 d, 10 d recovery, followed by 50 mM NaCl for 30 d

Xu et al., 1996

Kinases of signalling pathways maize enhanced drought soil water content was kept tolerance constant at 25% of field capacity rice abiotic stress tolerance 4C for 3 d; water withholding for up to 6 d; 200 mM NaCl for up to 4 d tomato multiple abiotic stress 200 mM NaCl for 18 d; tolerance water withholding for 15 d; 4C for 5 d rice enhanced drought stripping watering, rain-off resistance in field shelter, severe drough stress – water content 15-18% Gibberellins rice dwarf phenotype, 5C for 5 d increased cold stress tolerance Arabidopsis increased tolerance to 170 mM NaCl for 13 d high-salinity stress 64

Shou et al., 2004

Xiong and Yang, 2003

Wang et al., 2012

Xiao et al., 2009

Tanaka et al., 2006

Magome et al., 2004

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cassava

AgtIPT/SARK

rice

AgtIPT/Ghcysp ipt1 3 5 7 mutant

cotton Arabidopsis

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AgtIPT/SAG12

M

IPT

AtCKX1/bGLU OE

improved drought tolerance improved salt tolerance improved salt and drought tolerances

barley

increased tolerance to drought stress

AtCKX/WRKY6, AtCKX/35S OE AtUGT85A5/35S OE

tobacco

AtYUCCA6/SWPA2 Atyuc7-1D mutant

hybrid poplar Arabidopsis

ZEP

MsZEP/35S OE

tobacco

improved drought and heat tolerance enhanced salt stress tolerance Auxins increased drought tolerance enhances drought resistance Abscisic acid drought and salt stress tolerance

NDEC

PvNDEC1/DEX OE

tobacco

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CKX

Cytokinins increased drought tolerance

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YUC

tobacco

drought tolerance

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greenhouse: water deficiency for 4 weeks; field: 5-9 months withholding water for 6-10 d 200 mM NaCl for up to 21 d 200 mM NaCl for 6 d; withholding water for 1or 2 weeks mild stress: limited watering; severe stress: draining off the growing medium in hydroponic cultures for 24 h cessation of watering for 10 d; 40°C for 2 h or 6 h from 100 mM to 300 mM NaCl for 4 weeks

Zhang et al., 2010

water withholding for 6 d

Ke et al., 2015

water withholding for 14 d

Lee et al., 2012

withholding irrigation for 0, 3, 7, and 14 d; 200 mM NaCl for 2 weeks spray with 30 μM DEX in 0.01% (v/v) Tween 20 followeed by withholding irrigation for 7 d

Zhang et al., 2016

Peleg et al., 2011 Liu et al., 2012 Nishiyama et al., 2011 Pospíšilová et al., 2016

Macková et al., 2013 Sun et al., 2013

Qin and Zeevaart, 2002

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cotton

drought tolerance

rice

ACC synthase

acs7 mutant

Arabidopsis

JMT

BcNTR1/ 35S OE

soybean

improved grain yield under drought stress in the field Ethylene increased tolerance to salt, osmotic, and heat stresses Jasmonates drought tolerance

tobacco

Other targets improved cold tolerance 1C for 7 d

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AtLOS5/ superpromoter OE AtLOS5/Actin1P/LE A3-1P OE

Atfad7/35S OE

withholding irrigation for 5 d stripping watering, rain-off shelter, severe drough stress – water content 15-18%

Yue et al., 2012b Xiao et al., 2009

150 mM NaCl for 18 d; 300 Dong et al., 2011 mM mannitol for 86 h; 43C for 3 h withholding irrigation for up Xue et al., 2007 to 6 d Kodama et al., 1994

LeGPAT/35S OE

tomato

improved chilling tolerance

4C for 12 h

Sui et al., 2007

SlVKOR/ 35S OE

tomato

resistance to osmotic stress (salt and drought)

150 mM NaCl or 20% PEG6000 for 3 d

Yu et al., 2016

A

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fad (fatty acid desaturse) GPAT (glycerol-3phosphate acyltransferase) VKOR (vitamin K epoxide reductase)

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M

LOS

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A

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PT

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M

A

Fig. 1. Strategies for improving photosynthesis yield and CO2 utilisation. Target pathways/enzymes that are to be activated are marked in green (upwards arrow), while those to be limited are marked in red (downwards arrow).

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