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Engineering Improved Photosynthesis in the Era of Synthetic Biology
Journal Pre-proof Engineering Improved Photosynthesis in the Era of Synthetic Biology Willian Batista-Silva, Paula da Fonseca-Pereira, Auxiliadora Oliveira Martins, Agustín Zsögön, Adriano Nunes-Nesi, Wagner L. Araújo PII:
S2590-3462(20)30013-4
DOI:
https://doi.org/10.1016/j.xplc.2020.100032
Reference:
XPLC 100032
To appear in:
PLANT COMMUNICATIONS
Please cite this article as: Batista-Silva, W., da Fonseca-Pereira, P., Martins, A.O., Zsögön, A., NunesNesi, A., Araújo, W.L., Engineering Improved Photosynthesis in the Era of Synthetic Biology, PLANT COMMUNICATIONS (2020), doi: https://doi.org/10.1016/j.xplc.2020.100032. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. 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. © 2020
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Engineering Improved Photosynthesis in the Era of Synthetic Biology
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Willian Batista-Silva1#, Paula da Fonseca-Pereira1#, Auxiliadora Oliveira
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Martins1, Agustín Zsögön1, Adriano Nunes-Nesi1, and Wagner L. Araújo1*
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Authors Affiliations
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1
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Departamento de Biologia Vegetal, Universidade Federal de Viçosa, 36570-
900, Viçosa, Minas Gerais, Brazil
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#
These authors contributed equally to this work
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Running title: Improving Photosynthesis through Synthetic Biology
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Short summary:
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We summarize here the progress on the emerging field of synthetic biology
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applied to photosynthesis. We further discuss recent strategies used for
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manipulating photosynthetic efficiency and their potential biotechnological
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applications.
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* Corresponding author
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Wagner L. Araújo
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Departamento de Biologia Vegetal
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Universidade Federal de Viçosa
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36570-900, Viçosa, Minas Gerais, Brazil
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E-mail: [email protected]
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Tel.:+55 31 3612 5358
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1
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ABSTRACT
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Much attention has been given to the enhancement of photosynthesis as a
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strategy for the optimization of crop productivity. As traditional plant breeding is
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most likely reaching a plateau, there is a timely need to accelerate
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improvements in photosynthetic efficiency by means of novel tools and
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biotechnological solutions. The emerging field of synthetic biology offers the
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potential for building completely novel pathways in predictable directions and,
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thus, addresses the global requirements for higher yields expected to occur in
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the 21st century. Here we discuss the recent advances and current challenges
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of engineering improved photosynthesis in the era of synthetic biology toward
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optimized utilization of solar energy and carbon sources to optimize the
45
production of food, fibre and fuel.
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Keywords: photosynthesis; synthetic biology; genetic engineering; yield
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improvement; targeted manipulation
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2
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The need for increased photosynthesis in crops
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Photosynthesis is the main driving force for plant growth and biomass
55
production and, as such, considered as a cornerstone of human civilization (Ort
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et al., 2015; Orr et al., 2017; Simkin et al., 2019). Notably, most attention in
57
research that could result in an improvement of the productivity of crops has
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been directed to photosynthesis (Nowicka et al., 2018). Moreover, the
59
accelerated growth of global population and the uncertainties derived from
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global climate change make the enhancement of photosynthetic efficiency of
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paramount importance to ensure food security over the coming decades
62
(National Academies of Sciences, Engineering and Medicine, 2019) and an
63
exciting opportunity to address the challenge of sustainable yield increases
64
required to meet future food demand (Foyer et al., 2017; Éva et al., 2019;
65
Fernie and Yan, 2019).
66
Until recently, it was generally believed that plant photosynthesis had
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already been optimized during evolution to perform at its optimum, and thus it
68
could not be further improved (Leister, 2012). However, research efforts toward
69
better understanding of the photosynthetic process have actually demonstrated
70
that photosynthesis in terrestrial plants can be considered remarkably inefficient
71
(Ort et al., 2015; Éva et al., 2019). As a consequence, a range of opportunities
72
aimed at enhancing the photosynthetic capacity have been proposed (Orr et al.,
73
2017; Nowicka et al., 2018; Nowicka, 2019; Kubis and Bar-Even, 2019) and
74
promising results have been obtained. If successfully transferred to crops, these
75
results would enable agriculture to keep pace with the exponential demand for
76
increased yield from growing human population (Shih, 2018; Éva et al., 2019).
77
The strategies aimed at enhancing crop yield have changed over time.
78
From the onset of crop domestication and the very beginning of agriculture until
79
the current state of global agriculture, humankind has learned to improve crops
80
in order to fulfil its evolving needs (Pouvreau et al., 2018; Fernie and Yan,
81
2019). In the past, particularly in the second half of the 20th century, during the
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so-called ‘Green Revolution’, traditional plant breeding strategies, in conjunction
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with greater inputs of fertilizers, pesticides and water, provided a rapid and
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significant increase in crop yield, especially for cereals (Betti et al., 2016;
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Nowicka et al., 2018; Éva et al., 2019). As a result, large increases in the yield
86
of the staple crops were achieved (Long et al., 2006; Nowicka et al., 2018). 3
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However, yield improvements for several major crops are either slowing or
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stagnating (Long et al., 2015). Furthermore, it is predicted that the productivity
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of the major crop species is approaching the highest yield that can be obtained
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using traditional breeding methods (Betti et al., 2016; Hanson et al., 2016;
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Nowicka et al., 2018). Therefore, there is a timely need to accelerate our
92
understanding of the mechanisms controlling photosynthetic and associated
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processes in response to the environment to allow higher photosynthesis for
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increased biomass production and yield (Long et al., 2015; Vavitsas et al.,
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2019). However, according with Leister (2019), few, if any, increases in crop
96
yield have been attained through increases in photosynthetic rate.
97
As traditional methods of crop improvement are probably reaching a
98
plateau, further increases in the productivity of crops must be obtained by
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means of novel tools and technological solutions (Ort et al., 2015; Nowicka et
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al., 2018; Simkin et al., 2019). Much of the ongoing research has aimed at
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identifying natural genetic variation responsible for increased photosynthetic
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capacity (Hüner et al., 2016; Nunes-Nesi et al., 2016). However, the limited
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genetic variation that is naturally found in the enzymes and photosynthesis
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related processes, especially for major crops, hampers the task of optimizing
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photosynthesis (Ort et al., 2015; Dann and Leister, 2017). Such challenges can
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potentially be overcome using genetic engineering in conjunction with
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systems/synthetic biology and computational modelling strategies as part of a
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new Green Revolution (Long et al., 2015; Wallace et al., 2018; Fernie and Yan,
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2019). Instead of exchanging single components, synthetic biology tools can
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engineer and redesign entire processes to overcome the challenges that cannot
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be easily solved using existing systems (Weber and Bar-Even, 2019).
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Our aim here is to provide an overview of the current state and the
113
prospects for engineering improved photosynthesis and plant productivity in the
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era of synthetic biology. To this end, we summarize recently identified strategies
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for manipulating photosynthetic efficiency and further discuss their potential
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application for plant biomass production and crop yield, as well as for producing
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valuable and highly-demanded compounds in vivo to address the global
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requirements for higher yields expected to occur in the 21st century.
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Photosynthesis as a target for synthetic biology strategies 4
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Oxygenic photosynthesis is the process in which plants and other
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phototrophs use solar energy to fix carbon dioxide (CO2) into carbohydrates,
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releasing oxygen (O2) as a by-product through a series of reactions occurring in
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the thylakoid membranes (photochemical reactions) and in the chloroplast
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stroma (carbon-fixing and reducing reactions). In the photochemical reactions,
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the absorbed light energy oxidizes water to O2 and drives a series of reduction-
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oxidation (redox) reactions in which electrons flow through several specialized
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compounds, ultimately reducing NADP+ to NADPH, with the concomitant
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generation of ATP during the electron transfer from water to NADP+ (Nielsen et
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al., 2013). The resulting high energy compounds, NAPDH and ATP, are used to
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power the Calvin-Benson cycle (CBC) allowing the assimilation and reduction of
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CO2 into trioses phosphate, which are then stored in the chloroplast as starch or
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exported by the phloem in the form of sucrose to support growth and
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metabolism of sink tissues and organs.
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At least three kinds of photosynthesis namely C3, C4, and crassulacean
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acid metabolism (CAM) are found in plants based on a set of characteristics,
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such as the identity of the first molecule produced upon CO2 fixation,
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photorespiratory rate and natural habitat (Moses, 2019). The central enzyme of
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the
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(RuBisCO), catalyses the carboxylation reaction of RuBP (CO2 fixation) to form
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two molecules of 3-phosphoglycerate (3PGA) in the first step of the C3
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photosynthetic carbon reduction cycle (Moses, 2019). Because carboxylation
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and oxygenation occur within the same active site of the RuBisCO, in all
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photosynthetic organisms, and the enzyme does not discriminate well between
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CO2 and O2, the concentration ratio of CO2 to O2 in the vicinity of RuBisCO
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determines the efficiency of CO2 fixation (Betti et al., 2016; Hagemann and
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Bauwe, 2016; Nölke et al., 2019).
CBC,
ribulose-1,5-bisphosphate
(RuBP)
carboxylase/oxygenase
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The majority of the plants (~85%), including major crops like wheat
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(Triticum aestivum), rice (Oryza sativa), and soybean (Glycine max) have a C3-
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type metabolism (Stitt; Moses, 2019). In contrast to C3, in which oxygenase
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activity of RuBisCO causes a significant waste of resources, some plant
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species, as well as cyanobacteria and algae, have evolved carbon
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concentration mechanisms (CCMs) to favour the carboxylase activity of
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RuBisCO and thus limit their photorespiratory rates known as C4 and CAM 5
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photosynthesis (Peterhänsel et al., 2013; Long et al., 2016; Nowicka et al.,
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2018; Nölke et al., 2019). By contrast, C3 plants maximize CO2 capture by
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maintaining high stromal RubisCO concentrations (up to 50% of leaf total
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protein), at the cost of relatively higher rates of photorespiration and lower
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water-use efficiency (WUE) (Raines, 2011; Orr et al., 2017; Rae et al., 2017). In
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consequence, most of the efforts to optimize photosynthesis have been directed
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toward the introduction of desired metabolic pathways of either CAM or C4
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photosynthesis into C3 plants (Orr et al., 2017; Weber and Bar-Even, 2019).
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Considering that the number of genes and metabolic routes bearing a
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potential for improved photosynthesis and biomass production is high (Orr et al.,
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2017; Nowicka et al., 2018), targeted manipulation based on engineering
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principles have been extensively used to modify and optimize photosynthesis
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and, thus, facilitate the management of such complexity. Synthetic biology
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offers a promising interdisciplinary approach to integrate the principles of
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molecular
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computational tools to modify an existent organism or to artificially create novel
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life forms for different purposes (South et al., 2018; Stewart et al., 2018),
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including the improvement of photosynthesis. Thus, within the next sections, we
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will shed light on the challenges, advances and prospects for the applicability of
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synthetic biology concepts, from an integrated and holistic perspective, to
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multitargeted manipulations of the photosynthetic machinery.
biology
with
biochemical
engineering
in
conjunction
with
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Approaches to optimize light reactions of photosynthesis
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Photosynthesis is the only known biological process capable of using the
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energy derived from light to produce chemical energy for the synthesis of
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complex carbon compounds. As shown in Figure 1, light-dependent reactions of
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land plant photosynthesis consist of two photochemical complexes, called
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photosystems I and II (PSI and PSII), which operate in series and are spatially
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separated in the thylakoid and lamella membranes (Éva et al., 2019). PSI and
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PSII work in conjunction with their respective light-absorbing antenna systems,
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LHCI and LHCII, and are connected to each other by an electron-transport
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chain (ETC)(Amthor, 2010). While the light-absorbing pigments of the antenna
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complex are responsible for collecting the light and physically transferring the 6
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energy, specialized chlorophyll molecules associated with the reaction center
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complex transduce the energy from the light and use it for the photochemical
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reactions leading to the long-term chemical energy storage.
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In view of the complexity and the importance of light reactions of
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photosynthesis, it is not surprising that not only an efficient and robust
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apparatus but also flexibility in the responses to changing environmental
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conditions is required (Kramer et al., 2004). This fact aside, many scholars have
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argued that overall plant photosynthesis is remarkably inefficient, since many
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drawbacks have been identified within this system (Kornienko et al., 2018; Éva
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et al., 2019; Moses, 2019). To begin with, less than half of the average solar
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spectrum
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photosynthetically active fraction of 400-740 nm) can be used to drive oxygenic
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photosynthesis in plants (Moses, 2019). Secondly, the theoretical efficiency of
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solar energy conversion into biomass by natural photosynthesis is considered
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low (maximum of 4.6 and 6% for C3 and C4 plants, respectively; 1–2% typical
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for crops and 0.1% for most other plants) (Zhu et al., 2008b; Zhu et al., 2010)
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Thirdly, PSII is highly susceptible to photoinhibition at high light intensity
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(Nishiyama et al., 2011; Liu et al., 2019), possibly due to the evolutionary origin
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of photosynthesis in prokaryotes, initially in marine conditions (i.e., low- light)
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and in the absence of oxygen (Leister, 2012; Éva et al., 2019). Therefore, the
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many losses known to occur from light absorption to photochemical events and
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beyond provide the necessary room for improvement of the plant photosynthetic
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light reactions.
incident
on
the
earth’s
surface
(corresponding
to
the
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Several approaches aiming at increasing the efficiency to process the
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influx of energy by the photosynthetic apparatus, thus mitigating energy losses
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during photosynthesis, have been proposed (Blankenship et al., 2011; Orr et al.,
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2017). Significant increases in growth rates were recently obtained in tobacco
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by accelerating recovery from photoprotection by means of an improved non-
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photochemical quenching (NPQ) (Kromdijk et al., 2016a). Furthermore, different
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recent approaches have emerged as alternatives to improve photosynthesis
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based on changes in NPQ (Murchie and Niyogi, 2011; Harada et al., 2019) as
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well as on the regulation of the cytochrome b6f complex and its related proteins
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PsbS and Rieske FeS subunit (Shikanai, 2014; Ermakova et al., 2019a). Apart
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from the alterations in NPQ or cytochrome b6f complex, two main ideas 7
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suggested to optimize light-use efficiency (LUE) by plants are (i) the expansion
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of the light absorption spectrum to capture more of the available light and (ii) the
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reduction of antenna size of the photosystems (Terao and Katoh, 1996; Ort et
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al., 2011; Bielczynski et al., 2019). In this respect, a promising strategy would
227
be the use of bacteriochlorophylls found in anoxygenic photosynthetic
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organisms, which have absorption maxima that extend out to the far-red region
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(~1100 nm), to engineer one of the photosystems, thus expanding the visible
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light spectrum of plant photosynthetic apparatus (Blankenship et al., 2011; Ort
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et al., 2015; Orr et al., 2017). Alternatively, chlorophylls and bacteriochlorophylls
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could also be combined in the same organism (Leister, 2019a). On the other
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hand, reducing the size of the antenna could be a feasible approach to extend
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the absorption spectrum without favouring saturation effects (Blankenship et al.,
235
2011).
236
The temptation to modify core photosynthetic proteins has generally led
237
to undesired effects, as expertly reviewed elsewhere (Leister, 2019b). For
238
instance, exchanges of conserved individual photosynthetic proteins from either
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cyanobacterial PSI (PsaA) or PSII (D1, CP43, CP47, and PsbH) by their plant
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counterparts caused side effects such as slower growth (Nixon et al., 1991),
241
loss of photoautotrophy (Carpenter et al., 1993; Vermaas et al., 1996), higher
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light sensitivity (Chiaramonte et al., 1999), lower chlorophyll content
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(Chiaramonte et al., 1999), impaired photoautotrophic growth and drastically
244
reduced chlorophyll-phycocyanin ratio (Viola et al., 2014; Leister, 2019b).
245
Hence, single mutations or replacements of core photosynthetic proteins will not
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be probably enough to increase the photosynthetic performance owing to the
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multiple interactions of the photosynthetic machinery, which evolved over
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billions of years and is locked in a “frozen metabolic state” (Gimpel et al., 2016;
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Leister, 2019a; Leister, 2019b).
250
In view of the highly integrated nature of the photosynthetic machinery,
251
the transfer of entire photosynthetic multiprotein complexes from different
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species seems to be a more promising approach than the exchange of
253
individual photosynthetic proteins (Leister, 2019b). The first successful
254
demonstration of a whole photosynthetic complex being exchanged was made
255
by Gimpel et al., 2016. Six subunits of the entire PSII core of C. reinhardtii were
256
replaced by a single synthetic construct that contained the orthologous genes 8
257
from two other green algae (Volvox carteri or Scenedesmus obliquus) (Gimpel
258
et al., 2016). Despite their photoautotrophic growth, the resulting strains
259
exhibited lower photosynthetic efficiency and lower levels of the heterologous
260
proteins in comparison with those proteins they were replacing (Gimpel et al.,
261
2016; Leister, 2019b). These results suggest that the aforementioned synthetic
262
exchange might have disturbed interactions with other PSII proteins in the
263
transgenic strains (Gimpel et al., 2016). Therefore, it might be mandatory to not
264
only exchange the core subunits, but also the supplementary proteins that
265
physically and/or physiologically interact with the core photosynthetic proteins.
266
However, whether this approach is feasible in practice is still a matter of debate
267
and a target of future engineering and optimization efforts (Nowicka et al., 2018;
268
Leister, 2019a).
269
Several recent synthetic biology studies have endeavoured to insert
270
photosynthetic proteins into host species which lack the related homologs
271
(Tognetti et al., 2006; Chida et al., 2007; Tognetti et al., 2007; Blanco et al.,
272
2011; Yamamoto et al., 2016). Promising results were obtained by the
273
introduction of the algal cytochrome c6 protein in the photosynthetic ETC of
274
Arabidopsis (Chida et al., 2007) and of tobacco (Yadav et al., 2018) (Figure 1).
275
In both cases, photosynthetic rates and growth were higher in the transgenic
276
lines (Chida et al., 2007; Yadav et al., 2018). In addition, improved pigment
277
contents and WUE were observed when the Cyt c6 from the green macroalgae
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Ulva fasciata was overexpressed in tobacco (Yadav et al., 2018). Therefore, the
279
overexpression of the heterologous Cyt c6 protein is a promising approach
280
toward delivering step change advancement in crop productivity by means of
281
synthetic biology.
282
In addition to the improvement of photosynthesis for higher biomass,
283
synthetic biology efforts have also been proposed to modify the photosynthetic
284
apparatus to redirect metabolic energy towards the production of desired
285
compounds (Mellor et al., 2019; Russo et al., 2019). P450s are a large and
286
diverse family of redox enzymes wide-spread across the kingdoms (Mellor et
287
al., 2019). Owing to their involvement in extreme versatile functions and to the
288
irreversibility of their catalysed reactions, besides their key roles in the synthesis
289
of secondary metabolites, P450s are highly attractive potential targets for
290
biotechnology applications (Rasool and Mohamed, 2016; Leister, 2019b; Russo 9
291
et al., 2019). In eukaryotes, P450s are located in the endoplasmic reticulum
292
(ER), where they are reduced by a membrane bound NADPH-dependent
293
reductase (Jensen and Scharff, 2019). Given that the expression levels of
294
P450s in plants are generally low and their activity is limited by the availability of
295
both NADPH and substrates inside the ER (Wlodarczyk et al., 2016; Russo et
296
al., 2019), synthetic biology approaches have attempted to introduce P450
297
pathways into the plant chloroplast and redirect the electrons from PSI to the
298
P450s (Russo et al., 2019; Urlacher and Girhard, 2019). For example, direct
299
coupling of P450 from S. bicolor (CYP79A1) to barley (Hordeum vulgare) PSI
300
enabled the conversion of tyrosine to hydroxyphenyl-acetaldoxime during the
301
biosynthesis of the cyanogenic glucoside dhurrin (Jensen et al., 2011). In
302
addition, expression of a fusion between CYP79A1 and Fd in the thylakoid
303
membrane in N. benthamiana allowed coupling of photosynthetic reducing
304
power to the heme iron reduction (Mellor et al., 2016; Urlacher and Girhard,
305
2019). Afterwards, this strategy was extended by successfully inserting two
306
P450s (CYP79A1 and CYP71A1) and a UDP glucosyl transferase from the S.
307
bicolor biosynthetic pathway of dhurrin
308
transiently transformed N. benthamiana leaves (Nielsen et al., 2013) or into the
309
cyanobacterium Synechocystis sp. PCC 6803 (Wlodarczyk et al., 2016)(Figure
310
1). Collectively, these findings demonstrate the feasibility of transferring P450
311
dependent pathways to redirect the photosynthetic electron flow for the
312
biosynthesis of primary and secondary metabolites in chloroplasts of either
313
plants or heterologous hosts such as cyanobacteria.
into the thylakoid membranes of
314
Apart from the production of high-value compounds by means of P450
315
catalysis, recent synthetic biology efforts have exploited overall light reactions to
316
directly power enzymes for a large number of diverse biotechnological
317
applications (Sorigué et al., 2017; Ito et al., 2018; Yunus et al., 2018).
318
Moreover, other pioneering studies have offered a demonstration of how light-
319
driven enzymes can play a major role, for example, in the degradation of
320
polysaccharides (Cannella et al., 2016), in the conversion of long-chain fatty
321
acids into alka(e)nes in microalgae and in the conversion of CO2 into
322
hydrocarbons in photosynthetic microorganisms (Sorigué et al., 2017).
323
Interestingly, light-driven catalysis can even be created in non-photosynthetic
324
membranes (Russo et al., 2019), as recently shown in a study seeking to 10
325
optimize the application of particulate methane monooxygenases (pMMOs) by
326
using
327
Methylosinus trichosporium OB3b for methane hydroxylation (Ito et al., 2018).
328
Considering the capacity of PSII to extract electrons from water and its
329
contribution for the electrochemical potential across membranes (Semin et al.,
330
2019), electrons from water oxidation can be extracted on the acceptor side of
331
PSII for many additional energy applications .
332
the
reconstituted
PSII
containing
membrane-bound
pMMO
of
From the studies described up to now, it becomes evident that the ample
333
availability
of
solar energy provides
opportunities
to
drive
not
only
334
photosynthesis but also unrelated metabolic reactions requiring electrons for
335
their catalytic cycle (Leister, 2019a; Russo et al., 2019). However, some
336
fundamental challenges remain. One of them is that, apart from modifying light
337
capture and increasing the conversion efficiency of light energy into biomass or
338
into valuable compounds, a true synthetic biology program should also aim to
339
design photosystems insensitive to photodamage and which produce fewer
340
harmful reactive oxygen species (ROS) (Leister, 2012; Schmermund et al.,
341
2019). For that purpose, photosystems might have to be redesigned to include
342
additional “devices” that use or quench excess excitation energy and, at the
343
same time, dramatically reduce the number of proteins and thus preventing the
344
requirement for a plethora of assembly factors (Leister, 2012). Moreover, this
345
problem might be solved by using (i) cells which allow repair of a damaged D1
346
subunit of PSII (e.g., cyanobacteria, algae) or by (ii) transferring entire PSII core
347
module from organisms (e.g. non-model green alga Chlorella ohadii) which
348
probably generate fewer ROS or which are better protected against to or even
349
less accessible to ROS (Treves et al., 2016; Leister, 2019a). Finally, it must be
350
kept in mind that, regardless of the approach taken, well-validated mechanistic
351
models will be decisive to understand and further manipulate light reactions with
352
the final aim to predictably modify the organisms and obtain desired functions
353
through synthetic biology tools.
354 355
Synthetic biology offers great promise to introduce CCMs into C3 plants
356 357
The introduction of CCMs into C3 plants has been a key driver of many
358
synthetic biology strategies aimed at improving photosynthesis (see Figure 2 for 11
359
details). C4 photosynthesis, which has evolved in angiosperm families at least
360
66 independent times, is a remarkable convergent evolutionary phenomena
361
(Sage et al., 2011; Aliscioni et al., 2012; Orr et al., 2017). According to the
362
carbon starvation hypothesis, C4 plants arose in open and arid regions where
363
the low atmospheric CO2 concentration, in concert with warmer weather,
364
triggered the evolution of C4 metabolism, as a strategy to minimize the
365
oxygenase activity of RuBisCO. In addition to the reduction of photorespiration,
366
the C4 traits have enabled C4 plants to increase their efficiencies in the use of
367
radiation, nitrogen, and water in comparison to C3 plants (Sage, 2004; Zhu et
368
al., 2008a; Maurino and Peterhänsel, 2010; Peterhänsel and Maurino, 2011;
369
Sage et al., 2012; Schuler et al., 2016). Thereupon, the understanding of the
370
genetic mechanisms underlying this complex trait could provide further insights
371
into the conversion of the C3 pathway into C4, with the ultimate goal of
372
enhancing C3 photosynthetic efficiency (Schuler et al., 2016).
373
Engineering C4 photosynthesis into C3 plants has been recently outlined
374
as a stepwise process reviewed by Kubis and Bar-Even (2019). The
375
modification of the tissue anatomy, as well as the establishment of the bundle
376
sheath (BS) morphology and the maintenance of a cell type-specific enzyme
377
expression are key aspects which must be taken into account in this process
378
(Sage et al., 2012; Schuler et al., 2016). Accordingly, the introduction of all
379
these traits into C3 plants that may lack the ability to naturally evolve C4
380
photosynthesis is considered a challenging task (Figure 2A; Denton et al., 2013;
381
Schuler et al., 2016; Wang et al., 2016). As previously shown in rice and in
382
many others C3 crops, yield is drastically limited by the photosynthetic capacity
383
of leaves and the carbohydrates factories are unable to fill the larger number of
384
florets or fruits of modern plants (Pearcy and Ehleringer, 1984; Hibberd et al.,
385
2008; von Caemmerer and Evans, 2010; von Caemmerer et al., 2012;
386
Sowjanya et al., 2019). Therefore, the introduction of higher-capacity
387
photosynthetic mechanism has challenged the scientific community to engineer
388
C4 pathway into rice (Hibberd et al., 2008).
389
Genomic and transcriptomic approaches have produced thrilling results
390
about potential metabolite transporters and transcriptional factors which might
391
be useful for engineering C4 rice (von Caemmerer et al., 2012; Wang et al.,
392
2016; Von Caemmerer et al., 2017). However, several efforts to engineer C4 12
393
photosynthesis into C3 species have been hampered by an incomplete list of
394
genes and gene functions required to support the trait (Weber and Bar-Even,
395
2019). Therefore, the identification and functional characterization of the
396
associated genes seem to be a fundamental challenge faced by the
397
researchers and a crucial step towards the introduction of the C4 pathway into
398
important C3 crop plants (Schuler et al., 2016; Kurz et al., 2016; Orr et al.,
399
2017). In addition, both the metabolic intermediates between mesophyll cell
400
(MC) and bundle sheath cells (BSC) and the factors involved in the
401
development of Kranz anatomy are still not fully identified and thus remain to be
402
elucidated (Schuler et al., 2016). Notably, these studies and other recently
403
summarized (Ermakova et al., 2019b) represent fundamental breakthroughs in
404
understanding and engineering C4 into C3 photosynthesis plants and, although
405
there is still room for improvement, it seems reasonable to assume that we are
406
facing now a move from the proof-of-concept stage to expanded strategic field
407
testing. These examples illustrate the critical integration of different research
408
fields to improve crops that can be provided by synthetic biology.
409
Another group of plants which represents one strategic and alternative
410
target to understand and engineer C3 photosynthesis are those with CAM
411
photosynthesis (Figure 2B; Orr et al., 2017; Kubis and Bar-Even, 2019). Unlike
412
the C4 pathway, CAM plants separate the activities of PEPC and RuBisCO
413
temporally, rather than spatially (Edwards, 2019). Given that CAM species fix
414
CO2 during the night, while stomata are closed (Rae et al., 2017), CAM reduces
415
the water evaporation and increases WUE by 20–80%, an adaptive trait for hot
416
and dry climates (Borland et al., 2009; Borland et al., 2014; Yang et al., 2015;
417
Kubis and Bar-Even, 2019). The existence of C3-CAM intermediate plants
418
represents a clear potential target for synthetic biology to introduce improved
419
WUE into C3 crops for a warmer and drier condition (Borland et al., 2009;
420
Borland et al., 2011).
421
Another strategy to increase C3 photosynthesis is the introduction of
422
biophysical CCMs from cyanobacteria and green algae into plant chloroplasts
423
(Figure 2C; Long et al., 2006b; Dean Price et al., 2011; Dean Prince et al.,
424
2013; Long et al., 2016; Long et al., 2018). As well reviewed in the current
425
literature, cyanobacteria and green algae such as C. reinhardii use a
426
biophysical CCM (Raven et al., 2012; Kupriyanova et al., 2013; Mackinder, 13
427
2018). The CCMs of microalgae and cyanobacteria rely on a range of active
428
and facilitated uptake mechanisms for inorganic carbon (Ci) such as carbonic
429
acids (HCO3-). After the participation of these transporters, bicarbonate is
430
further transported into specialized compartments packed with RuBisCO, the
431
carboxysome in cyanobacteria and pyrenoids in green algae, where CO2 is
432
released from bicarbonate by carbonic anhydrases (Dean Prince et al., 2013;
433
Mangan et al., 2016; Orr et al., 2017; Long et al., 2018; Poschenrieder et al.,
434
2018). Compelling evidence has demonstrated that the overexpression of the Ci
435
transporter ictB from cyanobacteria in Arabidopsis and tobacco enhances
436
photosynthesis and growth (Lieman-Hurwitz et al., 2003; Simkin et al., 2015)
437
(Figure 2C and Table 1). In addition, transgenic rice expressing the ccaA, ictB
438
and FBP/SBPase derived from cyanobacteria exhibited significant increases in
439
their photosynthetic capacities, mesophilic conductance and grain yield (Yang
440
et al., 2008; Gong et al., 2015; Gong et al., 2017). Similar results found that ictB
441
also contributes to enhancement of the soybean photosynthetic CO2
442
assimilation (Hay et al., 2017).
443
Another engineering strategy aiming to generate CCM in crop plants is
444
the introduction of genes encoding both the carboxysome and its encapsulated
445
RuBisCO (Dean Prince et al., 2013; Long et al., 2016). Significant progress
446
toward synthesizing a carboxysome in chloroplasts of C3 plants has been made
447
by using tobacco as a model system (Figure 2C; Lin et al., 2014a; Hanson et
448
al., 2016b; Occhialini et al., 2016). However, the big challenge and the first step
449
to be achieved as a key requirement for the introduction of a functional
450
biophysical CCM into C3 plants is to provide the expression and the correct
451
localization of Ci transporters from cyanobacteria or green alga into transgenic
452
C3 plants. Once this step is completed, we can go further with the next step, the
453
establishment of functional RuBisCO-containing compartments (Kubis and Bar-
454
Even, 2019). Recently, Long et al., (2018) have successfully produced
455
simplified carboxysome within tobacco chloroplast and replaced endogenous
456
RuBisCO large subunit genes with cyanobacterial form-1A RuBisCO large and
457
small subunit genes, producing carboxysome which encapsulates RuBisCO and
458
enable autotrophic growth at elevated CO2. Therefore, these new findings are
459
offering alternative avenues to tailor microcompartment design based on
460
simplified sets of genes. 14
461 462
Engineering RuBisCO
463 464
RuBisCO, a key regulator of the CBC, is responsible for the assimilation
465
of CO2 and is recognized as the most abundant protein in nature (Ellis, 1979;
466
Reven, 2013; Erb and Zarzycki, 2018). Given that RuBisCO exhibits slower
467
catalytic rate than most enzymes involved in the central metabolism of plants, it
468
has long been considered a limiting step for photosynthesis and hence for
469
primary productivity (Pottier et al., 2018). Therefore, a number of metabolic
470
engineering and synthetic biology strategies have been proposed to improve
471
RuBisCO’s ability to fix CO2 (Figure 3; Weigmann, 2019). However, some
472
strategies to achieve this goal have generally faced significant technical
473
challenges, suggesting that RuBisCO is already operating at or near
474
physiological optimum in plants (Long et al., 2015).
475
A key challenge in engineering RuBisCO is that the enzyme is a robust
476
hexadecameric complex (550 kDa) comprising eight copies of a large subunit
477
(RbcL), encoded by the chloroplast genome, and additional eight copies of a
478
small subunit (RbcS), encoded by the nuclear genome (Pottier et al., 2018).
479
Moreover, RuBisCO exhibits extensive natural diversity regarding subunit
480
stoichiometry and carboxylation kinetics (Whitney and Sharwood, 2008;
481
Sharwood, 2017). Further development has been obtained by manipulating the
482
small subunit of RuBisCO, an approach which has provided higher RuBisCO
483
catalytic turnover rates in rice (Ishikawa et al., 2011; Ogawa et al., 2012) and
484
Arabidopsis (Makino et al., 2012; Atkinson et al., 2017). In addition, the
485
introduction of a foreign RuBisCO from Synechococcus elongatus PCC7942
486
into tobacco allowed complete assembly of RubisCO with functional activity and
487
photosynthetical competence, supporting autotrophic growth (Lin et al., 2014b;
488
Occhialini et al., 2016).
489
It is also already known that the folding and assembly of RuBisCO large
490
and small subunits in L8S8 holoenzymes within the chloroplast stroma involves
491
many auxiliary factors, including chaperones such as bundle sheath defective 2
492
protein (BSD2) (Figure 3; Aigner et al., 2017; Bracher et al., 2017; Conlan and
493
Whitney, 2018; Conlan et al., 2019). According with Aigner et al., (2017), these
494
factors might assist RuBisCO folding by stabilizing an end-state assembly. In 15
495
addition, they can further facilitate efforts to enhance the kinetics of RuBisCO
496
though mutagenesis. Moreover, the catalytic parameter can be improved by
497
changes in the carbamylating activity which is a prerequisite for RuBisCO
498
activity (Lorimer and Miziorko, 1980; Kubis and Bar-Even, 2019). In fact, the
499
catalytic chaperone RuBisCO activase (Rca) presents itself as an attractive
500
target for engineering enhanced photosynthesis (Salvucci and Crafts-Brandner,
501
2004; Kurek et al., 2007; Fukayama et al., 2012; Yamori et al., 2012). These
502
findings, combined with those of previous studies, indicate that RuBisCo activity
503
and by consequence photosynthesis can be engineered and improved by
504
means of synthetic biology.
505 506
Optimizing
the
CBC
and
507
photorespiration bypass routes
advances
in
engineering
synthetic
508
Several attempts have focused on enhancing photosynthetic carbon
509
fixation and it has also been recognized that CBC enzymes represent promising
510
targets to accelerate plant carbon fixation (Figure 3; Raines, 2003; Feng et al.,
511
2007a; Raines, 2011; Singh et al., 2014; Orr et al., 2017; Kubis and Bar-Even,
512
2019). These assumptions are in consonance with computational models which
513
have suggested that the natural distribution of enzymes within the CBC is not
514
optimal and thus could directly limit photosynthesis performance (Kebeish et al.,
515
2007; Zhu et al., 2007; Bar-Even, 2018). Furthermore, it was predicted that
516
higher levels of sedoheptulose-1,7-biphosphatase (SBPase) and fructose-1,6-
517
biphosphate aldolase (FBPA) could support higher productivity, generating
518
extra thermodynamic push and enabling better flux control (Zhu et al., 2007;
519
Bar-Even, 2018; Kubis and Bar-Even, 2019).
520
Different glasshouse experiments have identified higher photosynthetic
521
rates and total biomass in transgenic tobacco and tomato plants overexpressing
522
SBPase (Lefebvre et al., 2005; Ding et al., 2016). Moreover, overexpression of
523
SBPase in rice plants enhanced photosynthesis rate under both high
524
temperature (Feng et al., 2007a) and salt stress (Feng et al., 2007b), by
525
providing higher regeneration of RuBP in the stroma. Similar results were
526
obtained by increasing SBPase activity in transgenic wheat, which exhibit
527
enhanced leaf photosynthesis, total biomass and dry seed yield (Driever et al.,
528
2017). In addition, increases in SBPase activity in tomato plants resulted in 16
529
higher photosynthetic efficiency by higher RuBP regeneration capacity and
530
increased LUE, in addition to higher tolerance to chilling stress (Ding et al.,
531
2016).
532
In order to avoid bottlenecks in different parts of the CBC, additional
533
efforts have been pursued to implement engineering principles to other CBC
534
targets (Simkin et al., 2015; Simkin et al., 2017b). These include the enzymes
535
FBPase, FBPA and photorespiratory glycine decarboxylase-H (GDH-H), and
536
the last was shown to increase photosynthesis and biomass when
537
overexpressed in transgenic tobacco plants (López-Calcagno et al., 2018). In
538
this respect, intensive effort has been placed into multigene manipulation of
539
photosynthetic carbon assimilation to improve crop yield (Simkin et al., 2015).
540
For
541
photosynthesis and yield in transgenic tobacco (Table 1; Simkin et al., 2015;
542
Simkin et al., 2017b). In addition, co-expression of GDC-H with SBPase and
543
FBPA resulted in a positive impact on leaf area and biomass in Arabidopsis
544
(Simkin et al., 2017b). However, despite promising results obtained so far,
545
multigene manipulations are still in development and still need to be tested
546
under field conditions.
instance,
co-overexpression
of
SBPase
and
FBPA
enhanced
547
An alternative approach to optimize CBC and reducing the negative
548
effects of photorespiration has been proposed to ameliorate carbon and energy
549
losses during carbon fixation. This strategy is based on the introduction of
550
synthetic metabolic pathways that incorporate enzyme-catalysed reactions
551
found in microorganism such as bacteria, algae and even Archaea, into higher
552
plants for the creation of the so called “photorespiratory bypasses” (Peterhänsel
553
and Maurino, 2011; Peterhänsel et al., 2013; Nölke et al., 2014; John Andralojc
554
et al., 2018). The metabolic engineering of photorespiratory bypasses enhances
555
the total photosynthetic yield, while the ammonia release in the mitochondrion is
556
omitted, thereby saving ammonia re-assimilation costs (Maier et al., 2012;
557
Peterhänsel et al., 2013). However, according to Peterhänsel et al., (2013),
558
advantages of this bypass have been only detectable under short-day
559
conditions, where energy efficiency of carbon fixation is more limiting for growth,
560
than under long-day conditions. This is a highly promising approach, yet further
561
studies under field conditions and stress conditions are still required.
562 17
563 564
Redesigning photorespiration and CO2 fixation pathways Given
that
carbon
loss
is
the
greatest
problem
caused
by
565
photorespiration and a challenge for boosting carbon fixation, recent systematic
566
analysis have aimed to identify photorespiratory bypass routes that do not lead
567
to the release of CO2 (Trudeau et al., 2018; Kubis and Bar-Even, 2019). By
568
combining natural and artificially designed enzymes, the activity of a synthetic
569
carbon-conserving photorespiration bypass have been established in vitro
570
(Trudeau et al., 2018). Briefly, the authors successfully jointly engineered the
571
two enzymes responsible to catalyse the glycolate reduction to glycolaldehyde,
572
an acetyl-CoA synthetase and an NADH-dependent propionyl-CoA, and further
573
combined, in a test tube, the glycolate reduction module with three natural
574
enzymes required to convert glycolate to RuBP. Since NADPH and ATP were
575
consumed and RuBP accumulated upon addition of glycolate and 3PGA
576
(Trudeau et al., 2018), the study provides a proof of principle of an alternative
577
synthetic photorespiration bypass that does not release CO2. However, once
578
this metabolic sequence has been only demonstrated in vitro, it awaits in planta
579
investigations.
580
Beyond carbon conservation, other studies have recently suggested
581
carbon-positive photorespiration shunts as a strategy to improve
582
efficiency (Yu et al., 2018; Kubis and Bar-Even, 2019). For instance, a synthetic
583
malyl-CoA-glycerate (MCG) carbon fixation pathway designed for the
584
conversion of glycolate to acetyl-CoA was introduced to complement the
585
deficiency of the CBC for acetyl-CoA synthesis (Yu et al., 2018). To this end,
586
the authors first tested the feasibility of the MCG pathway in vitro and in E. coli,
587
and then evaluated the coupling of the MCG pathway with the CBB cycle for the
588
acetyl-CoA synthesis in the cyanobacteria S. elongatus. Although the MCG
589
pathway cannot be considered a true photorespiration bypass, since acetyl-CoA
590
cannot be easily re-assimilated into the CBC (Weber and Bar-Even, 2019), the
591
pathway
592
cyanobacteria (Yu et al., 2018; Kubis and Bar-Even, 2019).
facilitated
a
2-fold
increase
in
bicarbonate
CBC
assimilation
in
593
Instead of generating photorespiration bypasses, alternative studies have
594
attempted to construct and optimize completely artificial routes for the fixation of
595
CO2 in vitro to further replacing the CBC with a synthetic carbon fixation
596
pathway (Figure 3; Schwander et al., 2016; Weber and Bar-Even, 2019; Kubis 18
597
and Bar-Even, 2019). Towards in vitro reconstitution of an enzymatic network,
598
the original CBC pathway was replaced by synthetic reaction sequences where
599
different enzymes were engineered to either limit side reactions of promiscuous
600
enzymes or proofread other enzymes required to correct for the generation of
601
dead-end metabolites (Schwander et al., 2016). Notably, the CETCH pathway,
602
which relies on the reductive carboxylation of enoyl-CoA esters, was able to
603
convert CO2 into the C2 intermediate glyoxylate (Schwander et al., 2016). In
604
total, 17 enzymes originating from nine organisms of all three domains of life
605
were used for the assembly of the CETCH cycle (Schwander et al., 2016), thus
606
opening the way for future applications in the field of carbon fixation reactions.
607
By using a synthetic biology approach, South et al., 2019 investigated
608
three alternative photorespiratory bypass strategies by generating a total of 17
609
construct designs with and without one RNAi construct in field-grown tobacco.
610
The RNAi approach was used to down regulate a native chloroplast glycolate
611
transporter in the photorespiratory pathway, thereby limiting metabolite flux
612
through the native pathway. Remarkably, the synthetic glycolate metabolism
613
pathway have stimulated crop growth and biomass productivity under both
614
greenhouse and field conditions. Similarly, a new photorespiratory bypass was
615
recently designed in rice by (Shen et al., 2019). By using a multi-gene
616
chloroplastidic bypass, it was possible to create a reduce participation of the
617
glycolate oxidase, oxalate oxidase, and catalase, allowing the generation of the
618
so called GOC pathway. The transgenic plants showed significant increases in
619
photosynthetic efficiency, biomass yield as well as increases nitrogen content
620
under both greenhouse and field conditions (Shen et al., 2019). Altogether,
621
these results coupled with others (Xin et al., 2015; Eisenhut et al., 2019) provide
622
compelling evidence for the potential of creating new photorespiratory bypass
623
by means of synthetic biology. Nevertheless, the effectiveness of such
624
approaches is clearly dependent on the complex metabolic regulation that exist
625
between photorespiration and related metabolic pathways. That being said, not
626
only the current strategies of synthetic biology but also novel approaches to
627
develop synthetic biochemical pathways that bypass photorespiration, hold a
628
highly promising potential for significant yield increases in C3 crops.
629
In addition to the in vitro synthesis of artificial designed carbon fixation
630
pathways (Bar-Even et al., 2010; Schwander et al., 2016), strategies to improve 19
631
carbon fixation have attempt to introduce natural or non-natural CO2 fixation
632
pathways into heterotroph organisms such as E. coli (Antonovsky et al., 2016;
633
Kerfeld, 2016). The functional introduction of a fully non-native CBC was
634
obtained, for the first time, by combining heterologous expression and rational
635
laboratory evolution approaches (Antonovsky et al., 2016; Claassens et al.,
636
2016). Interestingly, isotopic analysis of the biomass content in the transformed
637
strain revealed that the CBC implementation allowed a generation of 35% of the
638
biomass from CO2. Taking into account the most advanced state of the
639
engineering tools available for heterotrophic model microorganisms than to
640
autotrophic hosts, the transplanting of partial, and recently even complete, CO2
641
fixation pathways and other energy-harvesting systems related to autotrophy
642
into heterotrophs can be seen as an alternative promising concept (Claassens
643
et al., 2016). Further advances of synthetic biology in that direction
644
involve complementary approaches (Bailey-Serres et al., 2019) including
645
integrated analysis, higher comprehension of the gene regulatory networks and
646
plastid transformation (for details see Bock, 2014), which may altogether deliver
647
substantial gains in crop performance.
might
648 649 650
Going back to the beginning: De novo domestication
651 652
The process of crop improvement, using either traditional or modern
653
agricultural technologies, has been accompanied by large reductions in the
654
genetic variability available for breeding and also in the nutritional quality of
655
crops (Zsögön et al., 2017). To reverse this situation, adaptive traits taken from
656
wild species can be readily introgressed onto the background of cultivated crops
657
(Dani, 2001), which demonstrate the prospect of de novo domestication (Fernie
658
and Yan, 2019). Once native populations contain the genetic diversity that has
659
been lost through thousands of years of crop domestication, wild plants can be
660
re-domesticated or domesticated de novo by the targeted manipulation of
661
specific genes, in order to generate novel varieties containing the lost traits of
662
interest (Palmgren et al., 2015; Shelef et al., 2017; Wolter et al., 2019). It is
663
important to have in mind that in C3 plants, which represent most of land plants,
664
three major physiological and biochemical limitations, namely the stomatal 20
665
conductance (gs), the mesophyll conductance (gm) and the biochemistry lead by
666
the Rubisco, drives that overall photosynthetic performance. In this context,
667
maximal potential photosynthesis can be limited by individual or combinations of
668
all of specifically if they are co-limiting in a balanced manner. Remarkably,
669
knowing that those photosynthetic limitations are governed by several genes,
670
naturally occurring genetic variation in plants provides itself a powerful tool to
671
not only understand but also to modulate complex physiological traits such as
672
photosynthesis and photorespiration (Nunes-Nesi et al., 2016; de Oliveira Silva
673
et al., 2018; Adachi et al., 2019). The recent perspectives for improving gm in
674
different plant species have been expertly reviewed elsewhere (Lundgren and
675
Fleming, 2019; Cousins et al., 2020; Fernández‐Marín et al., 2020). It is
676
important to mention that molecular mechanisms governing gm still remain
677
mostly unknown. This fact aside, further studies are clearly required to fully
678
understand the biochemical aspects connecting an improved photosynthesis
679
with gm responses. This is particularly true give that improvement of
680
photosynthetic machinery must be combined with fast enough diffusion of CO2,
681
via gm, or the capacity to improve photosynthesis will be severely compromised.
682
Following the genetic transfer of desired traits from wild progenitors to
683
domesticated varieties, it is necessary to elucidate the genetic basis responsible
684
for the phenotypic outcome (Fernie and Yan, 2019). The genetic and molecular
685
dissection of QUANTITATIVE TRAIT LOCI (QTL) and the comparative mapping
686
of segregating populations obtained by crossing of a cultivated accession with
687
its wild relative has been the most common approach used to identify the
688
genetic basis for the phenotypic differences. A detailed study using a set of 76
689
introgression lines (ILs) from a cross between Lycopersicon pennellii and the
690
cultivated cv M82 (Eshed and Zamir, 1995) identified genomic regions involved
691
in the regulation of fundamental physiological processes in tomato (de Oliveira
692
Silva et al., 2018). Interestingly, 14 candidate genes were directly related to
693
photosynthetic rates, as follows: 3 photosynthesis-related genes per se; 6
694
genes related to photosynthesis and starch accumulation; 5 genes related to
695
photosynthesis and root dry mass accumulation.
696
Alongside re-domestication, de novo domestication, i.e., the creation of
697
new crop plants from wild species (Zsögön et al., 2017), has been proposed as
698
an avenue for making agriculture more sustainable in addition to ensuring food 21
699
security (Fernie and Yan, 2019). In combination with synthetic biology
700
approaches, the de novo domestication is a promising tool to boost efforts to
701
rapidly engineer better crops (Zsögön et al., 2018), as can be seen on the list of
702
genes related to domestication (Table 1). Genomic editing technologies have
703
allowed highly precise modifications in the DNA sequence and can represent a
704
breakthrough in plant breeding (Chen et al., 2019; Schindele et al., 2020). Due
705
to its simplicity, efficiency and versatility, CRISPR/Cas9 has overcome the
706
ZFNs and TALENS techniques and has been successfully used to promote
707
precise multiplex modifications on DNA of different organisms, including plants
708
(Armario Najera et al., 2019). By means of the simultaneous editing of multiple
709
targets, CRISPR systems hold a promise to build regulatory circuits, which
710
could create novel traits for precise plant breeding in agriculture (Chen et al.,
711
2019). All this success in DNA editing through the CRISPR/Cas technique has
712
shed new light on plant breeding and will probably allow us to get around the
713
big current challenge of producing food that can supply the demands of a
714
growing world population. Given the current scenario, genome editing through
715
the CRISPR technique has the potential to allow thousands of years of
716
domestication and crop improvement to be revived and restructured, making
717
food production more socially and environmentally sustainable.
718
Although the de novo domestication or re-domestication presents itself
719
as valuable approaches to engineering improved photosynthesis, a cautionary
720
note is the fact that most cultivated plants were selected mainly according to
721
survival or production during evolution (Denison et al., 2014; Leister, 2019b;
722
Weiner, 2019) and not necessarily for higher photosynthetic rates. In this
723
context it should not be overlooked that, the advantageous traits conferring
724
better photosynthesis that we are only starting to reveal, most likely have not
725
been selected under natural conditions or by domestication processes. It seems
726
reasonable to assume therefore that traits that confer higher photosynthesis can
727
be more easily transferred to those crops. It should be noticed that, although
728
higher photosynthesis is clearly an important trait, not only stress-resistant
729
crops are also required to ensure yield stability, but also nutrient efficiency
730
crops should be of special attentions in the near future. It is equally important to
731
mention that the compelling evidence has revealed that improvements of model
732
and non-cultivated species can be achieved by single domestication genes 22
733
(reviewed in Fernie and Yan, 2019; Bailey-Serres et al., 2019; Zsögön et al.,
734
2017).
735
By
regulating
diverse
pathways
involved
in
plant
growth
and
736
development, transcription factors (TFs) also represent an important class of
737
potential targets for modifying domestication-related phenotypes and conferring
738
tolerance to environmental stress (Ambavaram et al., 2014; Wu et al., 2019). In
739
agreement, several examples of TFs modification strategies have been used in
740
different species. For instance, by using transgenic rice plants expressing the
741
TF HYR (HIGHER YIELD RICE) it was demonstrated that HYR is a master
742
regulator, directly activating cascades of TFs and other downstream genes
743
involved in photosynthetic carbon metabolism and yield stability under either
744
normal or drought conditions (Ambavaram et al., 2014). In addition, the control
745
of grain size and rice yield performed by OsGRF4 (Growth Regulating Factor 4)
746
appears to occur by modulating specific brassinosteroid-induced responses
747
(Che et al., 2015; Liebsch and Palatnik, 2020). Moreover, the overexpression of
748
a maize MADS-box transcription factor gene, zmm28 culminated with increases
749
in growth, photosynthesis capacity, and nitrogen utilization in maize (Wu et al.,
750
2019). Altogether, these and other examples justify the overrepresentation of
751
TFs in the list of known genes underlying domestication (Olsen and Wendel,
752
2013; Zhu et al., 2019) and make TFs potentially suitable for targeted
753
modification by synthetic biology tools.
754 755
A long road ahead: the best of synthetic biology is yet to come
756 757
Much attention has been given to the improvement of photosynthesis as
758
an approach to optimize crop yields to fulfil human needs for food and energy
759
(Nowicka et al., 2018). Plant biotechnology is currently facing a dramatic
760
challenge to develop crops with higher yield, increased resilience and higher
761
nutritional content. Recent developments in genome editing and genetic
762
manipulation have been used to boost an impressive number of targeted
763
approaches to simultaneously produce more and more sustainably. Even
764
though more targeted and precise genetic manipulation strategies have been
765
recently generated in plant photosynthesis, a range of challenges remains. In
766
conjunction with extensive system biology data, these manipulations have 23
767
clearly advanced our understanding of the contribution of individual genes,
768
transcripts,
769
Considering the tremendous amount of time and resources invested to
770
‘improve’ plants (Weiner, 2019), the observations above raise the question of
771
how, when and to what extent these improvements will solve world food crises
772
(Sinclair et al., 2019). The fact that evolution has not already provided such
773
‘improved’ plants in nature by positively selecting mutations demonstrate that
774
more progress is likely to happen if breeders think in terms of ‘trade-offs’
775
instead of ‘improvements’ (Weiner, 2019). Moreover, revolutionary synthetic
776
biology technologies must be effectively engaged to access new opportunities
777
aimed at transform agriculture (Wurtzel et al., 2019) and provide not only
778
improved yield but also stress resilient crops, while facing major climatic
779
changes (Bailey-Serres et al., 2019). Alternatively, it is quite probable that
780
photosynthesis will be made more efficient if designed outside of plants (Liu et
781
al., 2016; Weiner, 2019), by means of future developments of enzymology and
782
computational approaches to overcome the limitations associated with the
783
execution of synthetic pathways that are now tractable to be designed in silico
784
(Erb, 2019). Once synthetic biology has opened the door toward comprehensive
785
networks for the utilization of solar energy and carbon sources (Luan et al.,
786
2020), the future will tell us whether synthetic biology will fully develop its
787
tremendous potential for building completely novel pathways and crops in
788
predictable desired directions and, thus, provide the solutions for the social,
789
economic and environmental challenges we already have at hand.
proteins
and
metabolites
for
photosynthetic
performance.
790 791
Author Contributions
792
W.B-S., and P. F-P. jointly wrote the original manuscript draft, prepared the
793
figures and table. A.O.M. contributed to writing and preparation of figures and
794
tables. A.Z., A.N-N., and W.L.A. planned the review outline. All authors
795
contributed to the reviewing and editing of the manuscript.
796 797
Acknowledgements
798
This work was made possible through financial support from the Serrapilheira
799
Institute (grant Serra-1812-27067), the Max Planck Society, the CNPq (National
800
Council for Scientific and Technological Development, Brazil) [grant No. 24
801
402511/2016-6]; the FAPEMIG (Foundation for Research Assistance of the
802
Minas Gerais State, Brazil) [grant Nos. APQ-01357-14, APQ-01078-15, and
803
RED-00053-16]. We also thank the scholarships granted by the Brazilian
804
Federal Agency for Support and Evaluation of Graduate Education (CAPES-
805
Brazil) to PF-P and WB-S. Research fellowships granted by CNPq-Brazil to
806
ANN and WLA are also gratefully acknowledged. No conflict of interest
807
declared.
808 809 810 811 812
25
813
Figure legends
814 815
Figure 1 - Light reactions and potential targets for improvement
816
strategies. Overview of linear electron flow from water oxidation by OEC (gray
817
rectangle) in the PSII LHCII super complex (light green), though cytochrome b6f
818
(orange), to PTOX (light red circle) and/or PC (circle red) or algal cytochrome c6
819
(opened rectangle), then to PSI-LHCI (light green), followed by reduction of
820
NADP+ by ferredoxin (brown) and ferredoxin:NADP+ reductase (oval purple
821
circle), releasing protons into the lumen, which is then used to drive the ATP
822
biosynthesis by ATP synthase (blue). In addition to linear electron flow, there
823
are also cyclic electron transfer pathways that mediated by PGR5/PGRL1 or
824
NDH complex (purple). These pathways confer dynamic protection preventing
825
the production of ROS Noteworthy, ion channels, such as TPK3 and KEA3
826
(yellow), can be modulated by light fluctuations, regulating the proton motive
827
force in the chloroplast and thus be important regulators of ATP biosynthesis by
828
exchanging K+ and H+ between stroma and lumen. Moreover, recently in
829
Nicotina benthamiana a new strategy rerouting electron transferred by PSI to
830
P450s monooxygenase was performed (Mellor et al., 2016; Urlacher and
831
Girhard, 2019).CYP fused into Fd was expressed in the thylakoid membrane of
832
chloroplasts, enabling direct coupling of photosynthetic electron transfer to the
833
heme iron reduction. The reducing power (e−) needed for dhurrin formation in
834
the chloroplast is thus ultimately derived by the water splitting activity of PSII
835
(pink, gray and yellow intermembrane canes). Abbreviation:
836
Photosystem I light-harvesting complex I; PSII-LHCII, Photosystem II light-
837
harvesting complex II; PQ, Plastoquinone; PQH, semi-plastoquinone; PTOX,
838
plastoquinol terminal oxidase;
839
Cytb6f, cytochrome b6f; OEC, oxygen-evolving complex; Fd; ferredoxin; NDH,
840
NAD(P)H dehydrogenase; PGR5, proton gradient regulation 5; PGRL1, PGR5-
841
like protein 1; TPK3, two-pore K+ channel3 ; KEA3, potassium cation efflux
842
antiporter3.
PSI-LHCI,
PC, plastocyanin; Cyt C6, cytochrome C6;
843 844 845
26
846
Figure 2 - Photosynthetic mechanisms and strategies used to introduce
847
carbon concentration mechanisms (CCMs) into C3 plants. A) Converting
848
C3 into C4 mechanism. The transition from C3 to C4 metabolism requires the
849
differentiation of photosynthetically active vascular BS cells, modification in the
850
biochemistry reactions of several enzymes and modulation of metabolites
851
transport in both inter and intracellular compartments, as well as transferring
852
GDC into BS cell (Schuler et al., 2018). B) Converting C3 into Crassulacean
853
Acid Metabolism (CAM). The pathway of CAM in a mesophyll cell is temporally
854
separated. The different background color indicates light at the top and dark at
855
the bottom. The green-boxes on both sides indicate the epidermis under these
856
two different conditions (opened – night and closed – day). As an alternative
857
engineering target and less complicate process not involving changes in
858
morphological structure, is the introduction of CAM metabolism into C3 plants.
859
Such engineering requires precise control of several key enzymes, such as
860
PEP carboxylase, malic enzyme, and RuBisCO (Kubis and Bar-Even, 2019). C)
861
Transferring cyanobacteria and algal CCM components to C3 chloroplasts.
862
Transfer of HCO3- transporter (red and yellow circle) on inner chloroplast
863
membrane and expression of functional carboxysome (yellow icosahedron) and
864
introducing an algal pyrenoid CCM (brown circle) in the chloroplast stroma.
865
Long et al., (2018) using sophisticated approaches took us to a closer step to
866
achieving high stromal HCO3- pool in the presence of functional carboxysome
867
increasing CO2 fixation and yield up to 60% in transformed tobacco, as
868
previously predicted by McGrath and Long (2014). Abbreviations: Asp,
869
Aspartate; CA, carbonic anidrase; GDC, glycine decarboxylase; PEP,
870
phosphoenolpyruvate; PEPcase, phosphoenolpyruvate carboxylase; PPDK,
871
pyruvate phosphate dikinase; ME, malic enzyme.
872
27
873
Figure 3 - Calvin-Benson Cycle (CBC) advances, RuBP supply and
874
photorespiratory bypasses. RuBisCO catalyze CO2 and O2 fixation. The
875
product of CO2 fixation is the 3PGA that enters in the CBC and can be directed
876
to starch biosynthesis and/or sugars in the cytosol (black arrow). In addition, the
877
oxygenation drives the production of 2PGA, which is metabolized in the C2
878
photorespiratory pathway (blue arrows). Recently, three new synthetic
879
photorespiratory bypasses have been proposed to improve the carbon
880
assimilation and reduce photorespiration losses in C3 plants. See details in pink
881
circles (1), glycolate is diverted into glycerate within the chloroplast, shifting the
882
release of CO2 from mitochondria to chloroplasts, and reducing ammonia
883
release (dashed light green arrows) (For details see Kebeish et al., 2007); (2)
884
Peroxisomal pathway, catalyzed by two Escherichia coli enzymes, convert
885
glyoxylate into hydroxypyruvate and CO2 in a two-step process (brown) (For
886
details see Peterhänsel et al., 2012); (3) Lastly, bypass 3 is considered a non-
887
real bypass since the glycolate is completely oxidized into CO2 inside
888
chloroplasts by both newly introduced and native enzymes (dashed red arrows)
889
(For details see Peterhänsel et al., 2012; Fonseca-Pereira et al., 2020). In
890
parallel, overexpression of GDC (oval circle gray) in Arabidopsis increased net
891
carbon assimilation. Besides of that, RuBisCO activity is also limited by RuBP
892
regeneration, which involved two main enzymes, SBPase and FBPA (oval circle
893
yellow). The combination of SBPase and FBPA overexpression resulted in
894
cumulative positive effects on leaf area and biomass accumulation (Parry et al.,
895
2017). Recent studies have showed that BSD2 (red star) chaperone is crucial
896
for cyanobacterial RuBisCO assembly into functional enzyme in tobacco
897
(Conlan et al., 2018). Therefore, all these changes are considered important
898
check point targets to optimize and improve the photosynthetic efficiency.
899
Abbreviations: 3PGA, 3-phosphoglycerate; CBC, Calvin-Benson cycle; FBPA,
900
fructose-1,6-bisphosphate
901
bisphosphatase; BSD2, bundle sheath defective 2 protein.
aldolase;
SBPase,
sedoheptulose-1,7-
902
28
903
Table 1 - Some domesticated genes that are providing improvements on photosynthetic rates and/or crops yield. Crop
Domesticated genes
Function
Traits
Reference
Fructose-1,6-bisphosphate FBPA/SBPase:
aldolase/Sedoheptulose-1,7bisphosphatase
ictB
Increases on photosynthetic
leaf (Simkin Cyanobacterial putative2015) area, and biomass yield inorganic carbon transporter carbon
assimilation,
et
al.,
B, Tobacco
Tomato
(López-Calcagno
GCS H-protein
Glycine cleavage system
Biomass yield
PsbS
Photosystem II Subunit S
(Głowacka et al., Reduction in water loss per CO2 assimilated 2018)
ZEP VDE PsbS
Zeaxanthin epoxidase Volaxanthinde-epoxidase Photosystem II Subunit S
SP (Self pruning)
Flowering repressor
SBPase
Sedoheptulose-1,7bisphosphatase
ictB
Inorganic carbon transporter B
Rice
Increased leaf CO2 uptake and plant dry matter productivity A quick burst of flower production that translates to an early yield Enhancement of photosynthesis to high temperature Higher photosynthesis and carboxylation efficiencies, lower CO2 compensation
et al., 2018)
(Kromdijk et al., 2016b) (Soyk et al., 2017) (Feng et al., 2007a) (Yang et al., 2008)
29
points Fructose-1,6-bisphosphate Net photosynthetic rate, aldolase/Sedoheptulose-1,7(Gong et al., 2017) carboxylation efficiency bisphosphatase Formerly icfA: inorganic ccaA carbon fixation A Sugars Will Eventually be (Sosso et al., ZmSWEET4c/OsSWEET4 Seed filling Exported Transporters 2015) FBPA/SBPase
Wheat
SBPase
Maize
ZmSWEET4c/OsSWEET4
PRK
Sedoheptulose-1,7-
Improves
bisphosphatase
and grain yield
Sugars
will
eventually
be
exported transporters Phosphoribulokinase
GDC L-protein
Glycine cleavage system
et
al.,
et
al.,
2017) (Sosso
Seed filling
2015)
Photosynthetic
capacity, (López-Calcagno
growth and seed yield increased
Arabidopsis
photosynthesis (Driever
rates
of
et al., 2017) CO2
assimilation, photorespiration, and plant
(Timm et al., 2015)
growth
soybean
PetC
Rieske FeS subunit of the Cytochrome b6f complex
ictB
Inorganic carbon transporter B
increases electron transport (Simkin et al., rates and biomass yield 2017a) Increases in photosynthetic (Hay et al., 2017) CO2 and dry mass
30
Setaria viridis
PetC
Rieske FeS subunit of the Cytochrome b6f complex
Better light conversion (Ermakova et al., efficiency, higher CO2 2019a) assimilation
31
904
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54
Figure 1
OEC
e-
2H2O
e-
NDH
Fd
Fd PSI LHCI
PTOX PC Cyt c 6 e-
e-
CYP71E1 CYP79A1
Oxime
e-
Hydroxylation
K+ K+ H+
K+ K+ H+
H+ ATP synthase
PQH
PGR5/PGRL1
-
PSII PQ e LHCII
Cytb6f
Fd
UGT85B1
KEA3
e-
Cyanohydrin
Tyrosine
Hydroxylation e-
ADP+Pi
TPK3
FdR
e-
ATP
Dhurrin Glycosylation
NADP+H NADPH +
H+
Stroma
Lumen
O2 + 4H+
Figure 1 - Light reactions and potential targets for improvement strategies.
Figure 2
A
B
Sucrose Starch Fructan
PEP
Malate
Vacuole
Malate
Malate PPDK PEPcase
PEP
Pyruvate
Chloroplast
HCO 3CA
Night-time
Mesophyll cell
OAA
Light-time
Pyruvate
CO2
CO2
H2O
H2O
Chloroplast
C 3PGA 2PG
Sugar
Algal Pyrenoid
CBC
CBC
3-PGA
RuBP O2 CO2
CO2 HCO3Cyanobacteria Carboxysome
HCO3-
Figure 2 - Photosynthetic mechanisms and strategies used to introduce carbon concentration mechanisms (CCMs) into C3 plants.
Figure 3 NADH CO2
3 Pyruvate
Acetyl-CoA
NADPH CO2
Malate CO2
GDC
Tartronic Semialdehyde
Glycolate 3PGA
2PG
1
NAD+
Glycerate CO2 Tartronic semialdehyde
FBPA
2
CBC SBPase Glycerate
BSD2
RuBP CO2
Hydroxypyruvate
RubisCO O2
Figure 3 - Calvin-Benson Cycle (CBC) advances, RuBP supply and photorespiratory bypasses. RuBisCO catalyze CO2 and O2 fixation.
S2590-3462(20)30013-4
DOI:
https://doi.org/10.1016/j.xplc.2020.100032
Reference:
XPLC 100032
To appear in:
PLANT COMMUNICATIONS
Please cite this article as: Batista-Silva, W., da Fonseca-Pereira, P., Martins, A.O., Zsögön, A., NunesNesi, A., Araújo, W.L., Engineering Improved Photosynthesis in the Era of Synthetic Biology, PLANT COMMUNICATIONS (2020), doi: https://doi.org/10.1016/j.xplc.2020.100032. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. 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. © 2020
1 2
Engineering Improved Photosynthesis in the Era of Synthetic Biology
3 4
Willian Batista-Silva1#, Paula da Fonseca-Pereira1#, Auxiliadora Oliveira
5
Martins1, Agustín Zsögön1, Adriano Nunes-Nesi1, and Wagner L. Araújo1*
6 7 8
Authors Affiliations
9
1
10
Departamento de Biologia Vegetal, Universidade Federal de Viçosa, 36570-
900, Viçosa, Minas Gerais, Brazil
11 12
#
These authors contributed equally to this work
13 14 15
Running title: Improving Photosynthesis through Synthetic Biology
16 17 18
Short summary:
19
We summarize here the progress on the emerging field of synthetic biology
20
applied to photosynthesis. We further discuss recent strategies used for
21
manipulating photosynthetic efficiency and their potential biotechnological
22
applications.
23 24 25
* Corresponding author
26
Wagner L. Araújo
27
Departamento de Biologia Vegetal
28
Universidade Federal de Viçosa
29
36570-900, Viçosa, Minas Gerais, Brazil
30
E-mail: [email protected]
31
Tel.:+55 31 3612 5358
32 33
1
34
ABSTRACT
35
Much attention has been given to the enhancement of photosynthesis as a
36
strategy for the optimization of crop productivity. As traditional plant breeding is
37
most likely reaching a plateau, there is a timely need to accelerate
38
improvements in photosynthetic efficiency by means of novel tools and
39
biotechnological solutions. The emerging field of synthetic biology offers the
40
potential for building completely novel pathways in predictable directions and,
41
thus, addresses the global requirements for higher yields expected to occur in
42
the 21st century. Here we discuss the recent advances and current challenges
43
of engineering improved photosynthesis in the era of synthetic biology toward
44
optimized utilization of solar energy and carbon sources to optimize the
45
production of food, fibre and fuel.
46
Keywords: photosynthesis; synthetic biology; genetic engineering; yield
47
improvement; targeted manipulation
48 49 50 51 52
2
53
The need for increased photosynthesis in crops
54
Photosynthesis is the main driving force for plant growth and biomass
55
production and, as such, considered as a cornerstone of human civilization (Ort
56
et al., 2015; Orr et al., 2017; Simkin et al., 2019). Notably, most attention in
57
research that could result in an improvement of the productivity of crops has
58
been directed to photosynthesis (Nowicka et al., 2018). Moreover, the
59
accelerated growth of global population and the uncertainties derived from
60
global climate change make the enhancement of photosynthetic efficiency of
61
paramount importance to ensure food security over the coming decades
62
(National Academies of Sciences, Engineering and Medicine, 2019) and an
63
exciting opportunity to address the challenge of sustainable yield increases
64
required to meet future food demand (Foyer et al., 2017; Éva et al., 2019;
65
Fernie and Yan, 2019).
66
Until recently, it was generally believed that plant photosynthesis had
67
already been optimized during evolution to perform at its optimum, and thus it
68
could not be further improved (Leister, 2012). However, research efforts toward
69
better understanding of the photosynthetic process have actually demonstrated
70
that photosynthesis in terrestrial plants can be considered remarkably inefficient
71
(Ort et al., 2015; Éva et al., 2019). As a consequence, a range of opportunities
72
aimed at enhancing the photosynthetic capacity have been proposed (Orr et al.,
73
2017; Nowicka et al., 2018; Nowicka, 2019; Kubis and Bar-Even, 2019) and
74
promising results have been obtained. If successfully transferred to crops, these
75
results would enable agriculture to keep pace with the exponential demand for
76
increased yield from growing human population (Shih, 2018; Éva et al., 2019).
77
The strategies aimed at enhancing crop yield have changed over time.
78
From the onset of crop domestication and the very beginning of agriculture until
79
the current state of global agriculture, humankind has learned to improve crops
80
in order to fulfil its evolving needs (Pouvreau et al., 2018; Fernie and Yan,
81
2019). In the past, particularly in the second half of the 20th century, during the
82
so-called ‘Green Revolution’, traditional plant breeding strategies, in conjunction
83
with greater inputs of fertilizers, pesticides and water, provided a rapid and
84
significant increase in crop yield, especially for cereals (Betti et al., 2016;
85
Nowicka et al., 2018; Éva et al., 2019). As a result, large increases in the yield
86
of the staple crops were achieved (Long et al., 2006; Nowicka et al., 2018). 3
87
However, yield improvements for several major crops are either slowing or
88
stagnating (Long et al., 2015). Furthermore, it is predicted that the productivity
89
of the major crop species is approaching the highest yield that can be obtained
90
using traditional breeding methods (Betti et al., 2016; Hanson et al., 2016;
91
Nowicka et al., 2018). Therefore, there is a timely need to accelerate our
92
understanding of the mechanisms controlling photosynthetic and associated
93
processes in response to the environment to allow higher photosynthesis for
94
increased biomass production and yield (Long et al., 2015; Vavitsas et al.,
95
2019). However, according with Leister (2019), few, if any, increases in crop
96
yield have been attained through increases in photosynthetic rate.
97
As traditional methods of crop improvement are probably reaching a
98
plateau, further increases in the productivity of crops must be obtained by
99
means of novel tools and technological solutions (Ort et al., 2015; Nowicka et
100
al., 2018; Simkin et al., 2019). Much of the ongoing research has aimed at
101
identifying natural genetic variation responsible for increased photosynthetic
102
capacity (Hüner et al., 2016; Nunes-Nesi et al., 2016). However, the limited
103
genetic variation that is naturally found in the enzymes and photosynthesis
104
related processes, especially for major crops, hampers the task of optimizing
105
photosynthesis (Ort et al., 2015; Dann and Leister, 2017). Such challenges can
106
potentially be overcome using genetic engineering in conjunction with
107
systems/synthetic biology and computational modelling strategies as part of a
108
new Green Revolution (Long et al., 2015; Wallace et al., 2018; Fernie and Yan,
109
2019). Instead of exchanging single components, synthetic biology tools can
110
engineer and redesign entire processes to overcome the challenges that cannot
111
be easily solved using existing systems (Weber and Bar-Even, 2019).
112
Our aim here is to provide an overview of the current state and the
113
prospects for engineering improved photosynthesis and plant productivity in the
114
era of synthetic biology. To this end, we summarize recently identified strategies
115
for manipulating photosynthetic efficiency and further discuss their potential
116
application for plant biomass production and crop yield, as well as for producing
117
valuable and highly-demanded compounds in vivo to address the global
118
requirements for higher yields expected to occur in the 21st century.
119 120
Photosynthesis as a target for synthetic biology strategies 4
121
Oxygenic photosynthesis is the process in which plants and other
122
phototrophs use solar energy to fix carbon dioxide (CO2) into carbohydrates,
123
releasing oxygen (O2) as a by-product through a series of reactions occurring in
124
the thylakoid membranes (photochemical reactions) and in the chloroplast
125
stroma (carbon-fixing and reducing reactions). In the photochemical reactions,
126
the absorbed light energy oxidizes water to O2 and drives a series of reduction-
127
oxidation (redox) reactions in which electrons flow through several specialized
128
compounds, ultimately reducing NADP+ to NADPH, with the concomitant
129
generation of ATP during the electron transfer from water to NADP+ (Nielsen et
130
al., 2013). The resulting high energy compounds, NAPDH and ATP, are used to
131
power the Calvin-Benson cycle (CBC) allowing the assimilation and reduction of
132
CO2 into trioses phosphate, which are then stored in the chloroplast as starch or
133
exported by the phloem in the form of sucrose to support growth and
134
metabolism of sink tissues and organs.
135
At least three kinds of photosynthesis namely C3, C4, and crassulacean
136
acid metabolism (CAM) are found in plants based on a set of characteristics,
137
such as the identity of the first molecule produced upon CO2 fixation,
138
photorespiratory rate and natural habitat (Moses, 2019). The central enzyme of
139
the
140
(RuBisCO), catalyses the carboxylation reaction of RuBP (CO2 fixation) to form
141
two molecules of 3-phosphoglycerate (3PGA) in the first step of the C3
142
photosynthetic carbon reduction cycle (Moses, 2019). Because carboxylation
143
and oxygenation occur within the same active site of the RuBisCO, in all
144
photosynthetic organisms, and the enzyme does not discriminate well between
145
CO2 and O2, the concentration ratio of CO2 to O2 in the vicinity of RuBisCO
146
determines the efficiency of CO2 fixation (Betti et al., 2016; Hagemann and
147
Bauwe, 2016; Nölke et al., 2019).
CBC,
ribulose-1,5-bisphosphate
(RuBP)
carboxylase/oxygenase
148
The majority of the plants (~85%), including major crops like wheat
149
(Triticum aestivum), rice (Oryza sativa), and soybean (Glycine max) have a C3-
150
type metabolism (Stitt; Moses, 2019). In contrast to C3, in which oxygenase
151
activity of RuBisCO causes a significant waste of resources, some plant
152
species, as well as cyanobacteria and algae, have evolved carbon
153
concentration mechanisms (CCMs) to favour the carboxylase activity of
154
RuBisCO and thus limit their photorespiratory rates known as C4 and CAM 5
155
photosynthesis (Peterhänsel et al., 2013; Long et al., 2016; Nowicka et al.,
156
2018; Nölke et al., 2019). By contrast, C3 plants maximize CO2 capture by
157
maintaining high stromal RubisCO concentrations (up to 50% of leaf total
158
protein), at the cost of relatively higher rates of photorespiration and lower
159
water-use efficiency (WUE) (Raines, 2011; Orr et al., 2017; Rae et al., 2017). In
160
consequence, most of the efforts to optimize photosynthesis have been directed
161
toward the introduction of desired metabolic pathways of either CAM or C4
162
photosynthesis into C3 plants (Orr et al., 2017; Weber and Bar-Even, 2019).
163
Considering that the number of genes and metabolic routes bearing a
164
potential for improved photosynthesis and biomass production is high (Orr et al.,
165
2017; Nowicka et al., 2018), targeted manipulation based on engineering
166
principles have been extensively used to modify and optimize photosynthesis
167
and, thus, facilitate the management of such complexity. Synthetic biology
168
offers a promising interdisciplinary approach to integrate the principles of
169
molecular
170
computational tools to modify an existent organism or to artificially create novel
171
life forms for different purposes (South et al., 2018; Stewart et al., 2018),
172
including the improvement of photosynthesis. Thus, within the next sections, we
173
will shed light on the challenges, advances and prospects for the applicability of
174
synthetic biology concepts, from an integrated and holistic perspective, to
175
multitargeted manipulations of the photosynthetic machinery.
biology
with
biochemical
engineering
in
conjunction
with
176 177
Approaches to optimize light reactions of photosynthesis
178 179
Photosynthesis is the only known biological process capable of using the
180
energy derived from light to produce chemical energy for the synthesis of
181
complex carbon compounds. As shown in Figure 1, light-dependent reactions of
182
land plant photosynthesis consist of two photochemical complexes, called
183
photosystems I and II (PSI and PSII), which operate in series and are spatially
184
separated in the thylakoid and lamella membranes (Éva et al., 2019). PSI and
185
PSII work in conjunction with their respective light-absorbing antenna systems,
186
LHCI and LHCII, and are connected to each other by an electron-transport
187
chain (ETC)(Amthor, 2010). While the light-absorbing pigments of the antenna
188
complex are responsible for collecting the light and physically transferring the 6
189
energy, specialized chlorophyll molecules associated with the reaction center
190
complex transduce the energy from the light and use it for the photochemical
191
reactions leading to the long-term chemical energy storage.
192
In view of the complexity and the importance of light reactions of
193
photosynthesis, it is not surprising that not only an efficient and robust
194
apparatus but also flexibility in the responses to changing environmental
195
conditions is required (Kramer et al., 2004). This fact aside, many scholars have
196
argued that overall plant photosynthesis is remarkably inefficient, since many
197
drawbacks have been identified within this system (Kornienko et al., 2018; Éva
198
et al., 2019; Moses, 2019). To begin with, less than half of the average solar
199
spectrum
200
photosynthetically active fraction of 400-740 nm) can be used to drive oxygenic
201
photosynthesis in plants (Moses, 2019). Secondly, the theoretical efficiency of
202
solar energy conversion into biomass by natural photosynthesis is considered
203
low (maximum of 4.6 and 6% for C3 and C4 plants, respectively; 1–2% typical
204
for crops and 0.1% for most other plants) (Zhu et al., 2008b; Zhu et al., 2010)
205
Thirdly, PSII is highly susceptible to photoinhibition at high light intensity
206
(Nishiyama et al., 2011; Liu et al., 2019), possibly due to the evolutionary origin
207
of photosynthesis in prokaryotes, initially in marine conditions (i.e., low- light)
208
and in the absence of oxygen (Leister, 2012; Éva et al., 2019). Therefore, the
209
many losses known to occur from light absorption to photochemical events and
210
beyond provide the necessary room for improvement of the plant photosynthetic
211
light reactions.
incident
on
the
earth’s
surface
(corresponding
to
the
212
Several approaches aiming at increasing the efficiency to process the
213
influx of energy by the photosynthetic apparatus, thus mitigating energy losses
214
during photosynthesis, have been proposed (Blankenship et al., 2011; Orr et al.,
215
2017). Significant increases in growth rates were recently obtained in tobacco
216
by accelerating recovery from photoprotection by means of an improved non-
217
photochemical quenching (NPQ) (Kromdijk et al., 2016a). Furthermore, different
218
recent approaches have emerged as alternatives to improve photosynthesis
219
based on changes in NPQ (Murchie and Niyogi, 2011; Harada et al., 2019) as
220
well as on the regulation of the cytochrome b6f complex and its related proteins
221
PsbS and Rieske FeS subunit (Shikanai, 2014; Ermakova et al., 2019a). Apart
222
from the alterations in NPQ or cytochrome b6f complex, two main ideas 7
223
suggested to optimize light-use efficiency (LUE) by plants are (i) the expansion
224
of the light absorption spectrum to capture more of the available light and (ii) the
225
reduction of antenna size of the photosystems (Terao and Katoh, 1996; Ort et
226
al., 2011; Bielczynski et al., 2019). In this respect, a promising strategy would
227
be the use of bacteriochlorophylls found in anoxygenic photosynthetic
228
organisms, which have absorption maxima that extend out to the far-red region
229
(~1100 nm), to engineer one of the photosystems, thus expanding the visible
230
light spectrum of plant photosynthetic apparatus (Blankenship et al., 2011; Ort
231
et al., 2015; Orr et al., 2017). Alternatively, chlorophylls and bacteriochlorophylls
232
could also be combined in the same organism (Leister, 2019a). On the other
233
hand, reducing the size of the antenna could be a feasible approach to extend
234
the absorption spectrum without favouring saturation effects (Blankenship et al.,
235
2011).
236
The temptation to modify core photosynthetic proteins has generally led
237
to undesired effects, as expertly reviewed elsewhere (Leister, 2019b). For
238
instance, exchanges of conserved individual photosynthetic proteins from either
239
cyanobacterial PSI (PsaA) or PSII (D1, CP43, CP47, and PsbH) by their plant
240
counterparts caused side effects such as slower growth (Nixon et al., 1991),
241
loss of photoautotrophy (Carpenter et al., 1993; Vermaas et al., 1996), higher
242
light sensitivity (Chiaramonte et al., 1999), lower chlorophyll content
243
(Chiaramonte et al., 1999), impaired photoautotrophic growth and drastically
244
reduced chlorophyll-phycocyanin ratio (Viola et al., 2014; Leister, 2019b).
245
Hence, single mutations or replacements of core photosynthetic proteins will not
246
be probably enough to increase the photosynthetic performance owing to the
247
multiple interactions of the photosynthetic machinery, which evolved over
248
billions of years and is locked in a “frozen metabolic state” (Gimpel et al., 2016;
249
Leister, 2019a; Leister, 2019b).
250
In view of the highly integrated nature of the photosynthetic machinery,
251
the transfer of entire photosynthetic multiprotein complexes from different
252
species seems to be a more promising approach than the exchange of
253
individual photosynthetic proteins (Leister, 2019b). The first successful
254
demonstration of a whole photosynthetic complex being exchanged was made
255
by Gimpel et al., 2016. Six subunits of the entire PSII core of C. reinhardtii were
256
replaced by a single synthetic construct that contained the orthologous genes 8
257
from two other green algae (Volvox carteri or Scenedesmus obliquus) (Gimpel
258
et al., 2016). Despite their photoautotrophic growth, the resulting strains
259
exhibited lower photosynthetic efficiency and lower levels of the heterologous
260
proteins in comparison with those proteins they were replacing (Gimpel et al.,
261
2016; Leister, 2019b). These results suggest that the aforementioned synthetic
262
exchange might have disturbed interactions with other PSII proteins in the
263
transgenic strains (Gimpel et al., 2016). Therefore, it might be mandatory to not
264
only exchange the core subunits, but also the supplementary proteins that
265
physically and/or physiologically interact with the core photosynthetic proteins.
266
However, whether this approach is feasible in practice is still a matter of debate
267
and a target of future engineering and optimization efforts (Nowicka et al., 2018;
268
Leister, 2019a).
269
Several recent synthetic biology studies have endeavoured to insert
270
photosynthetic proteins into host species which lack the related homologs
271
(Tognetti et al., 2006; Chida et al., 2007; Tognetti et al., 2007; Blanco et al.,
272
2011; Yamamoto et al., 2016). Promising results were obtained by the
273
introduction of the algal cytochrome c6 protein in the photosynthetic ETC of
274
Arabidopsis (Chida et al., 2007) and of tobacco (Yadav et al., 2018) (Figure 1).
275
In both cases, photosynthetic rates and growth were higher in the transgenic
276
lines (Chida et al., 2007; Yadav et al., 2018). In addition, improved pigment
277
contents and WUE were observed when the Cyt c6 from the green macroalgae
278
Ulva fasciata was overexpressed in tobacco (Yadav et al., 2018). Therefore, the
279
overexpression of the heterologous Cyt c6 protein is a promising approach
280
toward delivering step change advancement in crop productivity by means of
281
synthetic biology.
282
In addition to the improvement of photosynthesis for higher biomass,
283
synthetic biology efforts have also been proposed to modify the photosynthetic
284
apparatus to redirect metabolic energy towards the production of desired
285
compounds (Mellor et al., 2019; Russo et al., 2019). P450s are a large and
286
diverse family of redox enzymes wide-spread across the kingdoms (Mellor et
287
al., 2019). Owing to their involvement in extreme versatile functions and to the
288
irreversibility of their catalysed reactions, besides their key roles in the synthesis
289
of secondary metabolites, P450s are highly attractive potential targets for
290
biotechnology applications (Rasool and Mohamed, 2016; Leister, 2019b; Russo 9
291
et al., 2019). In eukaryotes, P450s are located in the endoplasmic reticulum
292
(ER), where they are reduced by a membrane bound NADPH-dependent
293
reductase (Jensen and Scharff, 2019). Given that the expression levels of
294
P450s in plants are generally low and their activity is limited by the availability of
295
both NADPH and substrates inside the ER (Wlodarczyk et al., 2016; Russo et
296
al., 2019), synthetic biology approaches have attempted to introduce P450
297
pathways into the plant chloroplast and redirect the electrons from PSI to the
298
P450s (Russo et al., 2019; Urlacher and Girhard, 2019). For example, direct
299
coupling of P450 from S. bicolor (CYP79A1) to barley (Hordeum vulgare) PSI
300
enabled the conversion of tyrosine to hydroxyphenyl-acetaldoxime during the
301
biosynthesis of the cyanogenic glucoside dhurrin (Jensen et al., 2011). In
302
addition, expression of a fusion between CYP79A1 and Fd in the thylakoid
303
membrane in N. benthamiana allowed coupling of photosynthetic reducing
304
power to the heme iron reduction (Mellor et al., 2016; Urlacher and Girhard,
305
2019). Afterwards, this strategy was extended by successfully inserting two
306
P450s (CYP79A1 and CYP71A1) and a UDP glucosyl transferase from the S.
307
bicolor biosynthetic pathway of dhurrin
308
transiently transformed N. benthamiana leaves (Nielsen et al., 2013) or into the
309
cyanobacterium Synechocystis sp. PCC 6803 (Wlodarczyk et al., 2016)(Figure
310
1). Collectively, these findings demonstrate the feasibility of transferring P450
311
dependent pathways to redirect the photosynthetic electron flow for the
312
biosynthesis of primary and secondary metabolites in chloroplasts of either
313
plants or heterologous hosts such as cyanobacteria.
into the thylakoid membranes of
314
Apart from the production of high-value compounds by means of P450
315
catalysis, recent synthetic biology efforts have exploited overall light reactions to
316
directly power enzymes for a large number of diverse biotechnological
317
applications (Sorigué et al., 2017; Ito et al., 2018; Yunus et al., 2018).
318
Moreover, other pioneering studies have offered a demonstration of how light-
319
driven enzymes can play a major role, for example, in the degradation of
320
polysaccharides (Cannella et al., 2016), in the conversion of long-chain fatty
321
acids into alka(e)nes in microalgae and in the conversion of CO2 into
322
hydrocarbons in photosynthetic microorganisms (Sorigué et al., 2017).
323
Interestingly, light-driven catalysis can even be created in non-photosynthetic
324
membranes (Russo et al., 2019), as recently shown in a study seeking to 10
325
optimize the application of particulate methane monooxygenases (pMMOs) by
326
using
327
Methylosinus trichosporium OB3b for methane hydroxylation (Ito et al., 2018).
328
Considering the capacity of PSII to extract electrons from water and its
329
contribution for the electrochemical potential across membranes (Semin et al.,
330
2019), electrons from water oxidation can be extracted on the acceptor side of
331
PSII for many additional energy applications .
332
the
reconstituted
PSII
containing
membrane-bound
pMMO
of
From the studies described up to now, it becomes evident that the ample
333
availability
of
solar energy provides
opportunities
to
drive
not
only
334
photosynthesis but also unrelated metabolic reactions requiring electrons for
335
their catalytic cycle (Leister, 2019a; Russo et al., 2019). However, some
336
fundamental challenges remain. One of them is that, apart from modifying light
337
capture and increasing the conversion efficiency of light energy into biomass or
338
into valuable compounds, a true synthetic biology program should also aim to
339
design photosystems insensitive to photodamage and which produce fewer
340
harmful reactive oxygen species (ROS) (Leister, 2012; Schmermund et al.,
341
2019). For that purpose, photosystems might have to be redesigned to include
342
additional “devices” that use or quench excess excitation energy and, at the
343
same time, dramatically reduce the number of proteins and thus preventing the
344
requirement for a plethora of assembly factors (Leister, 2012). Moreover, this
345
problem might be solved by using (i) cells which allow repair of a damaged D1
346
subunit of PSII (e.g., cyanobacteria, algae) or by (ii) transferring entire PSII core
347
module from organisms (e.g. non-model green alga Chlorella ohadii) which
348
probably generate fewer ROS or which are better protected against to or even
349
less accessible to ROS (Treves et al., 2016; Leister, 2019a). Finally, it must be
350
kept in mind that, regardless of the approach taken, well-validated mechanistic
351
models will be decisive to understand and further manipulate light reactions with
352
the final aim to predictably modify the organisms and obtain desired functions
353
through synthetic biology tools.
354 355
Synthetic biology offers great promise to introduce CCMs into C3 plants
356 357
The introduction of CCMs into C3 plants has been a key driver of many
358
synthetic biology strategies aimed at improving photosynthesis (see Figure 2 for 11
359
details). C4 photosynthesis, which has evolved in angiosperm families at least
360
66 independent times, is a remarkable convergent evolutionary phenomena
361
(Sage et al., 2011; Aliscioni et al., 2012; Orr et al., 2017). According to the
362
carbon starvation hypothesis, C4 plants arose in open and arid regions where
363
the low atmospheric CO2 concentration, in concert with warmer weather,
364
triggered the evolution of C4 metabolism, as a strategy to minimize the
365
oxygenase activity of RuBisCO. In addition to the reduction of photorespiration,
366
the C4 traits have enabled C4 plants to increase their efficiencies in the use of
367
radiation, nitrogen, and water in comparison to C3 plants (Sage, 2004; Zhu et
368
al., 2008a; Maurino and Peterhänsel, 2010; Peterhänsel and Maurino, 2011;
369
Sage et al., 2012; Schuler et al., 2016). Thereupon, the understanding of the
370
genetic mechanisms underlying this complex trait could provide further insights
371
into the conversion of the C3 pathway into C4, with the ultimate goal of
372
enhancing C3 photosynthetic efficiency (Schuler et al., 2016).
373
Engineering C4 photosynthesis into C3 plants has been recently outlined
374
as a stepwise process reviewed by Kubis and Bar-Even (2019). The
375
modification of the tissue anatomy, as well as the establishment of the bundle
376
sheath (BS) morphology and the maintenance of a cell type-specific enzyme
377
expression are key aspects which must be taken into account in this process
378
(Sage et al., 2012; Schuler et al., 2016). Accordingly, the introduction of all
379
these traits into C3 plants that may lack the ability to naturally evolve C4
380
photosynthesis is considered a challenging task (Figure 2A; Denton et al., 2013;
381
Schuler et al., 2016; Wang et al., 2016). As previously shown in rice and in
382
many others C3 crops, yield is drastically limited by the photosynthetic capacity
383
of leaves and the carbohydrates factories are unable to fill the larger number of
384
florets or fruits of modern plants (Pearcy and Ehleringer, 1984; Hibberd et al.,
385
2008; von Caemmerer and Evans, 2010; von Caemmerer et al., 2012;
386
Sowjanya et al., 2019). Therefore, the introduction of higher-capacity
387
photosynthetic mechanism has challenged the scientific community to engineer
388
C4 pathway into rice (Hibberd et al., 2008).
389
Genomic and transcriptomic approaches have produced thrilling results
390
about potential metabolite transporters and transcriptional factors which might
391
be useful for engineering C4 rice (von Caemmerer et al., 2012; Wang et al.,
392
2016; Von Caemmerer et al., 2017). However, several efforts to engineer C4 12
393
photosynthesis into C3 species have been hampered by an incomplete list of
394
genes and gene functions required to support the trait (Weber and Bar-Even,
395
2019). Therefore, the identification and functional characterization of the
396
associated genes seem to be a fundamental challenge faced by the
397
researchers and a crucial step towards the introduction of the C4 pathway into
398
important C3 crop plants (Schuler et al., 2016; Kurz et al., 2016; Orr et al.,
399
2017). In addition, both the metabolic intermediates between mesophyll cell
400
(MC) and bundle sheath cells (BSC) and the factors involved in the
401
development of Kranz anatomy are still not fully identified and thus remain to be
402
elucidated (Schuler et al., 2016). Notably, these studies and other recently
403
summarized (Ermakova et al., 2019b) represent fundamental breakthroughs in
404
understanding and engineering C4 into C3 photosynthesis plants and, although
405
there is still room for improvement, it seems reasonable to assume that we are
406
facing now a move from the proof-of-concept stage to expanded strategic field
407
testing. These examples illustrate the critical integration of different research
408
fields to improve crops that can be provided by synthetic biology.
409
Another group of plants which represents one strategic and alternative
410
target to understand and engineer C3 photosynthesis are those with CAM
411
photosynthesis (Figure 2B; Orr et al., 2017; Kubis and Bar-Even, 2019). Unlike
412
the C4 pathway, CAM plants separate the activities of PEPC and RuBisCO
413
temporally, rather than spatially (Edwards, 2019). Given that CAM species fix
414
CO2 during the night, while stomata are closed (Rae et al., 2017), CAM reduces
415
the water evaporation and increases WUE by 20–80%, an adaptive trait for hot
416
and dry climates (Borland et al., 2009; Borland et al., 2014; Yang et al., 2015;
417
Kubis and Bar-Even, 2019). The existence of C3-CAM intermediate plants
418
represents a clear potential target for synthetic biology to introduce improved
419
WUE into C3 crops for a warmer and drier condition (Borland et al., 2009;
420
Borland et al., 2011).
421
Another strategy to increase C3 photosynthesis is the introduction of
422
biophysical CCMs from cyanobacteria and green algae into plant chloroplasts
423
(Figure 2C; Long et al., 2006b; Dean Price et al., 2011; Dean Prince et al.,
424
2013; Long et al., 2016; Long et al., 2018). As well reviewed in the current
425
literature, cyanobacteria and green algae such as C. reinhardii use a
426
biophysical CCM (Raven et al., 2012; Kupriyanova et al., 2013; Mackinder, 13
427
2018). The CCMs of microalgae and cyanobacteria rely on a range of active
428
and facilitated uptake mechanisms for inorganic carbon (Ci) such as carbonic
429
acids (HCO3-). After the participation of these transporters, bicarbonate is
430
further transported into specialized compartments packed with RuBisCO, the
431
carboxysome in cyanobacteria and pyrenoids in green algae, where CO2 is
432
released from bicarbonate by carbonic anhydrases (Dean Prince et al., 2013;
433
Mangan et al., 2016; Orr et al., 2017; Long et al., 2018; Poschenrieder et al.,
434
2018). Compelling evidence has demonstrated that the overexpression of the Ci
435
transporter ictB from cyanobacteria in Arabidopsis and tobacco enhances
436
photosynthesis and growth (Lieman-Hurwitz et al., 2003; Simkin et al., 2015)
437
(Figure 2C and Table 1). In addition, transgenic rice expressing the ccaA, ictB
438
and FBP/SBPase derived from cyanobacteria exhibited significant increases in
439
their photosynthetic capacities, mesophilic conductance and grain yield (Yang
440
et al., 2008; Gong et al., 2015; Gong et al., 2017). Similar results found that ictB
441
also contributes to enhancement of the soybean photosynthetic CO2
442
assimilation (Hay et al., 2017).
443
Another engineering strategy aiming to generate CCM in crop plants is
444
the introduction of genes encoding both the carboxysome and its encapsulated
445
RuBisCO (Dean Prince et al., 2013; Long et al., 2016). Significant progress
446
toward synthesizing a carboxysome in chloroplasts of C3 plants has been made
447
by using tobacco as a model system (Figure 2C; Lin et al., 2014a; Hanson et
448
al., 2016b; Occhialini et al., 2016). However, the big challenge and the first step
449
to be achieved as a key requirement for the introduction of a functional
450
biophysical CCM into C3 plants is to provide the expression and the correct
451
localization of Ci transporters from cyanobacteria or green alga into transgenic
452
C3 plants. Once this step is completed, we can go further with the next step, the
453
establishment of functional RuBisCO-containing compartments (Kubis and Bar-
454
Even, 2019). Recently, Long et al., (2018) have successfully produced
455
simplified carboxysome within tobacco chloroplast and replaced endogenous
456
RuBisCO large subunit genes with cyanobacterial form-1A RuBisCO large and
457
small subunit genes, producing carboxysome which encapsulates RuBisCO and
458
enable autotrophic growth at elevated CO2. Therefore, these new findings are
459
offering alternative avenues to tailor microcompartment design based on
460
simplified sets of genes. 14
461 462
Engineering RuBisCO
463 464
RuBisCO, a key regulator of the CBC, is responsible for the assimilation
465
of CO2 and is recognized as the most abundant protein in nature (Ellis, 1979;
466
Reven, 2013; Erb and Zarzycki, 2018). Given that RuBisCO exhibits slower
467
catalytic rate than most enzymes involved in the central metabolism of plants, it
468
has long been considered a limiting step for photosynthesis and hence for
469
primary productivity (Pottier et al., 2018). Therefore, a number of metabolic
470
engineering and synthetic biology strategies have been proposed to improve
471
RuBisCO’s ability to fix CO2 (Figure 3; Weigmann, 2019). However, some
472
strategies to achieve this goal have generally faced significant technical
473
challenges, suggesting that RuBisCO is already operating at or near
474
physiological optimum in plants (Long et al., 2015).
475
A key challenge in engineering RuBisCO is that the enzyme is a robust
476
hexadecameric complex (550 kDa) comprising eight copies of a large subunit
477
(RbcL), encoded by the chloroplast genome, and additional eight copies of a
478
small subunit (RbcS), encoded by the nuclear genome (Pottier et al., 2018).
479
Moreover, RuBisCO exhibits extensive natural diversity regarding subunit
480
stoichiometry and carboxylation kinetics (Whitney and Sharwood, 2008;
481
Sharwood, 2017). Further development has been obtained by manipulating the
482
small subunit of RuBisCO, an approach which has provided higher RuBisCO
483
catalytic turnover rates in rice (Ishikawa et al., 2011; Ogawa et al., 2012) and
484
Arabidopsis (Makino et al., 2012; Atkinson et al., 2017). In addition, the
485
introduction of a foreign RuBisCO from Synechococcus elongatus PCC7942
486
into tobacco allowed complete assembly of RubisCO with functional activity and
487
photosynthetical competence, supporting autotrophic growth (Lin et al., 2014b;
488
Occhialini et al., 2016).
489
It is also already known that the folding and assembly of RuBisCO large
490
and small subunits in L8S8 holoenzymes within the chloroplast stroma involves
491
many auxiliary factors, including chaperones such as bundle sheath defective 2
492
protein (BSD2) (Figure 3; Aigner et al., 2017; Bracher et al., 2017; Conlan and
493
Whitney, 2018; Conlan et al., 2019). According with Aigner et al., (2017), these
494
factors might assist RuBisCO folding by stabilizing an end-state assembly. In 15
495
addition, they can further facilitate efforts to enhance the kinetics of RuBisCO
496
though mutagenesis. Moreover, the catalytic parameter can be improved by
497
changes in the carbamylating activity which is a prerequisite for RuBisCO
498
activity (Lorimer and Miziorko, 1980; Kubis and Bar-Even, 2019). In fact, the
499
catalytic chaperone RuBisCO activase (Rca) presents itself as an attractive
500
target for engineering enhanced photosynthesis (Salvucci and Crafts-Brandner,
501
2004; Kurek et al., 2007; Fukayama et al., 2012; Yamori et al., 2012). These
502
findings, combined with those of previous studies, indicate that RuBisCo activity
503
and by consequence photosynthesis can be engineered and improved by
504
means of synthetic biology.
505 506
Optimizing
the
CBC
and
507
photorespiration bypass routes
advances
in
engineering
synthetic
508
Several attempts have focused on enhancing photosynthetic carbon
509
fixation and it has also been recognized that CBC enzymes represent promising
510
targets to accelerate plant carbon fixation (Figure 3; Raines, 2003; Feng et al.,
511
2007a; Raines, 2011; Singh et al., 2014; Orr et al., 2017; Kubis and Bar-Even,
512
2019). These assumptions are in consonance with computational models which
513
have suggested that the natural distribution of enzymes within the CBC is not
514
optimal and thus could directly limit photosynthesis performance (Kebeish et al.,
515
2007; Zhu et al., 2007; Bar-Even, 2018). Furthermore, it was predicted that
516
higher levels of sedoheptulose-1,7-biphosphatase (SBPase) and fructose-1,6-
517
biphosphate aldolase (FBPA) could support higher productivity, generating
518
extra thermodynamic push and enabling better flux control (Zhu et al., 2007;
519
Bar-Even, 2018; Kubis and Bar-Even, 2019).
520
Different glasshouse experiments have identified higher photosynthetic
521
rates and total biomass in transgenic tobacco and tomato plants overexpressing
522
SBPase (Lefebvre et al., 2005; Ding et al., 2016). Moreover, overexpression of
523
SBPase in rice plants enhanced photosynthesis rate under both high
524
temperature (Feng et al., 2007a) and salt stress (Feng et al., 2007b), by
525
providing higher regeneration of RuBP in the stroma. Similar results were
526
obtained by increasing SBPase activity in transgenic wheat, which exhibit
527
enhanced leaf photosynthesis, total biomass and dry seed yield (Driever et al.,
528
2017). In addition, increases in SBPase activity in tomato plants resulted in 16
529
higher photosynthetic efficiency by higher RuBP regeneration capacity and
530
increased LUE, in addition to higher tolerance to chilling stress (Ding et al.,
531
2016).
532
In order to avoid bottlenecks in different parts of the CBC, additional
533
efforts have been pursued to implement engineering principles to other CBC
534
targets (Simkin et al., 2015; Simkin et al., 2017b). These include the enzymes
535
FBPase, FBPA and photorespiratory glycine decarboxylase-H (GDH-H), and
536
the last was shown to increase photosynthesis and biomass when
537
overexpressed in transgenic tobacco plants (López-Calcagno et al., 2018). In
538
this respect, intensive effort has been placed into multigene manipulation of
539
photosynthetic carbon assimilation to improve crop yield (Simkin et al., 2015).
540
For
541
photosynthesis and yield in transgenic tobacco (Table 1; Simkin et al., 2015;
542
Simkin et al., 2017b). In addition, co-expression of GDC-H with SBPase and
543
FBPA resulted in a positive impact on leaf area and biomass in Arabidopsis
544
(Simkin et al., 2017b). However, despite promising results obtained so far,
545
multigene manipulations are still in development and still need to be tested
546
under field conditions.
instance,
co-overexpression
of
SBPase
and
FBPA
enhanced
547
An alternative approach to optimize CBC and reducing the negative
548
effects of photorespiration has been proposed to ameliorate carbon and energy
549
losses during carbon fixation. This strategy is based on the introduction of
550
synthetic metabolic pathways that incorporate enzyme-catalysed reactions
551
found in microorganism such as bacteria, algae and even Archaea, into higher
552
plants for the creation of the so called “photorespiratory bypasses” (Peterhänsel
553
and Maurino, 2011; Peterhänsel et al., 2013; Nölke et al., 2014; John Andralojc
554
et al., 2018). The metabolic engineering of photorespiratory bypasses enhances
555
the total photosynthetic yield, while the ammonia release in the mitochondrion is
556
omitted, thereby saving ammonia re-assimilation costs (Maier et al., 2012;
557
Peterhänsel et al., 2013). However, according to Peterhänsel et al., (2013),
558
advantages of this bypass have been only detectable under short-day
559
conditions, where energy efficiency of carbon fixation is more limiting for growth,
560
than under long-day conditions. This is a highly promising approach, yet further
561
studies under field conditions and stress conditions are still required.
562 17
563 564
Redesigning photorespiration and CO2 fixation pathways Given
that
carbon
loss
is
the
greatest
problem
caused
by
565
photorespiration and a challenge for boosting carbon fixation, recent systematic
566
analysis have aimed to identify photorespiratory bypass routes that do not lead
567
to the release of CO2 (Trudeau et al., 2018; Kubis and Bar-Even, 2019). By
568
combining natural and artificially designed enzymes, the activity of a synthetic
569
carbon-conserving photorespiration bypass have been established in vitro
570
(Trudeau et al., 2018). Briefly, the authors successfully jointly engineered the
571
two enzymes responsible to catalyse the glycolate reduction to glycolaldehyde,
572
an acetyl-CoA synthetase and an NADH-dependent propionyl-CoA, and further
573
combined, in a test tube, the glycolate reduction module with three natural
574
enzymes required to convert glycolate to RuBP. Since NADPH and ATP were
575
consumed and RuBP accumulated upon addition of glycolate and 3PGA
576
(Trudeau et al., 2018), the study provides a proof of principle of an alternative
577
synthetic photorespiration bypass that does not release CO2. However, once
578
this metabolic sequence has been only demonstrated in vitro, it awaits in planta
579
investigations.
580
Beyond carbon conservation, other studies have recently suggested
581
carbon-positive photorespiration shunts as a strategy to improve
582
efficiency (Yu et al., 2018; Kubis and Bar-Even, 2019). For instance, a synthetic
583
malyl-CoA-glycerate (MCG) carbon fixation pathway designed for the
584
conversion of glycolate to acetyl-CoA was introduced to complement the
585
deficiency of the CBC for acetyl-CoA synthesis (Yu et al., 2018). To this end,
586
the authors first tested the feasibility of the MCG pathway in vitro and in E. coli,
587
and then evaluated the coupling of the MCG pathway with the CBB cycle for the
588
acetyl-CoA synthesis in the cyanobacteria S. elongatus. Although the MCG
589
pathway cannot be considered a true photorespiration bypass, since acetyl-CoA
590
cannot be easily re-assimilated into the CBC (Weber and Bar-Even, 2019), the
591
pathway
592
cyanobacteria (Yu et al., 2018; Kubis and Bar-Even, 2019).
facilitated
a
2-fold
increase
in
bicarbonate
CBC
assimilation
in
593
Instead of generating photorespiration bypasses, alternative studies have
594
attempted to construct and optimize completely artificial routes for the fixation of
595
CO2 in vitro to further replacing the CBC with a synthetic carbon fixation
596
pathway (Figure 3; Schwander et al., 2016; Weber and Bar-Even, 2019; Kubis 18
597
and Bar-Even, 2019). Towards in vitro reconstitution of an enzymatic network,
598
the original CBC pathway was replaced by synthetic reaction sequences where
599
different enzymes were engineered to either limit side reactions of promiscuous
600
enzymes or proofread other enzymes required to correct for the generation of
601
dead-end metabolites (Schwander et al., 2016). Notably, the CETCH pathway,
602
which relies on the reductive carboxylation of enoyl-CoA esters, was able to
603
convert CO2 into the C2 intermediate glyoxylate (Schwander et al., 2016). In
604
total, 17 enzymes originating from nine organisms of all three domains of life
605
were used for the assembly of the CETCH cycle (Schwander et al., 2016), thus
606
opening the way for future applications in the field of carbon fixation reactions.
607
By using a synthetic biology approach, South et al., 2019 investigated
608
three alternative photorespiratory bypass strategies by generating a total of 17
609
construct designs with and without one RNAi construct in field-grown tobacco.
610
The RNAi approach was used to down regulate a native chloroplast glycolate
611
transporter in the photorespiratory pathway, thereby limiting metabolite flux
612
through the native pathway. Remarkably, the synthetic glycolate metabolism
613
pathway have stimulated crop growth and biomass productivity under both
614
greenhouse and field conditions. Similarly, a new photorespiratory bypass was
615
recently designed in rice by (Shen et al., 2019). By using a multi-gene
616
chloroplastidic bypass, it was possible to create a reduce participation of the
617
glycolate oxidase, oxalate oxidase, and catalase, allowing the generation of the
618
so called GOC pathway. The transgenic plants showed significant increases in
619
photosynthetic efficiency, biomass yield as well as increases nitrogen content
620
under both greenhouse and field conditions (Shen et al., 2019). Altogether,
621
these results coupled with others (Xin et al., 2015; Eisenhut et al., 2019) provide
622
compelling evidence for the potential of creating new photorespiratory bypass
623
by means of synthetic biology. Nevertheless, the effectiveness of such
624
approaches is clearly dependent on the complex metabolic regulation that exist
625
between photorespiration and related metabolic pathways. That being said, not
626
only the current strategies of synthetic biology but also novel approaches to
627
develop synthetic biochemical pathways that bypass photorespiration, hold a
628
highly promising potential for significant yield increases in C3 crops.
629
In addition to the in vitro synthesis of artificial designed carbon fixation
630
pathways (Bar-Even et al., 2010; Schwander et al., 2016), strategies to improve 19
631
carbon fixation have attempt to introduce natural or non-natural CO2 fixation
632
pathways into heterotroph organisms such as E. coli (Antonovsky et al., 2016;
633
Kerfeld, 2016). The functional introduction of a fully non-native CBC was
634
obtained, for the first time, by combining heterologous expression and rational
635
laboratory evolution approaches (Antonovsky et al., 2016; Claassens et al.,
636
2016). Interestingly, isotopic analysis of the biomass content in the transformed
637
strain revealed that the CBC implementation allowed a generation of 35% of the
638
biomass from CO2. Taking into account the most advanced state of the
639
engineering tools available for heterotrophic model microorganisms than to
640
autotrophic hosts, the transplanting of partial, and recently even complete, CO2
641
fixation pathways and other energy-harvesting systems related to autotrophy
642
into heterotrophs can be seen as an alternative promising concept (Claassens
643
et al., 2016). Further advances of synthetic biology in that direction
644
involve complementary approaches (Bailey-Serres et al., 2019) including
645
integrated analysis, higher comprehension of the gene regulatory networks and
646
plastid transformation (for details see Bock, 2014), which may altogether deliver
647
substantial gains in crop performance.
might
648 649 650
Going back to the beginning: De novo domestication
651 652
The process of crop improvement, using either traditional or modern
653
agricultural technologies, has been accompanied by large reductions in the
654
genetic variability available for breeding and also in the nutritional quality of
655
crops (Zsögön et al., 2017). To reverse this situation, adaptive traits taken from
656
wild species can be readily introgressed onto the background of cultivated crops
657
(Dani, 2001), which demonstrate the prospect of de novo domestication (Fernie
658
and Yan, 2019). Once native populations contain the genetic diversity that has
659
been lost through thousands of years of crop domestication, wild plants can be
660
re-domesticated or domesticated de novo by the targeted manipulation of
661
specific genes, in order to generate novel varieties containing the lost traits of
662
interest (Palmgren et al., 2015; Shelef et al., 2017; Wolter et al., 2019). It is
663
important to have in mind that in C3 plants, which represent most of land plants,
664
three major physiological and biochemical limitations, namely the stomatal 20
665
conductance (gs), the mesophyll conductance (gm) and the biochemistry lead by
666
the Rubisco, drives that overall photosynthetic performance. In this context,
667
maximal potential photosynthesis can be limited by individual or combinations of
668
all of specifically if they are co-limiting in a balanced manner. Remarkably,
669
knowing that those photosynthetic limitations are governed by several genes,
670
naturally occurring genetic variation in plants provides itself a powerful tool to
671
not only understand but also to modulate complex physiological traits such as
672
photosynthesis and photorespiration (Nunes-Nesi et al., 2016; de Oliveira Silva
673
et al., 2018; Adachi et al., 2019). The recent perspectives for improving gm in
674
different plant species have been expertly reviewed elsewhere (Lundgren and
675
Fleming, 2019; Cousins et al., 2020; Fernández‐Marín et al., 2020). It is
676
important to mention that molecular mechanisms governing gm still remain
677
mostly unknown. This fact aside, further studies are clearly required to fully
678
understand the biochemical aspects connecting an improved photosynthesis
679
with gm responses. This is particularly true give that improvement of
680
photosynthetic machinery must be combined with fast enough diffusion of CO2,
681
via gm, or the capacity to improve photosynthesis will be severely compromised.
682
Following the genetic transfer of desired traits from wild progenitors to
683
domesticated varieties, it is necessary to elucidate the genetic basis responsible
684
for the phenotypic outcome (Fernie and Yan, 2019). The genetic and molecular
685
dissection of QUANTITATIVE TRAIT LOCI (QTL) and the comparative mapping
686
of segregating populations obtained by crossing of a cultivated accession with
687
its wild relative has been the most common approach used to identify the
688
genetic basis for the phenotypic differences. A detailed study using a set of 76
689
introgression lines (ILs) from a cross between Lycopersicon pennellii and the
690
cultivated cv M82 (Eshed and Zamir, 1995) identified genomic regions involved
691
in the regulation of fundamental physiological processes in tomato (de Oliveira
692
Silva et al., 2018). Interestingly, 14 candidate genes were directly related to
693
photosynthetic rates, as follows: 3 photosynthesis-related genes per se; 6
694
genes related to photosynthesis and starch accumulation; 5 genes related to
695
photosynthesis and root dry mass accumulation.
696
Alongside re-domestication, de novo domestication, i.e., the creation of
697
new crop plants from wild species (Zsögön et al., 2017), has been proposed as
698
an avenue for making agriculture more sustainable in addition to ensuring food 21
699
security (Fernie and Yan, 2019). In combination with synthetic biology
700
approaches, the de novo domestication is a promising tool to boost efforts to
701
rapidly engineer better crops (Zsögön et al., 2018), as can be seen on the list of
702
genes related to domestication (Table 1). Genomic editing technologies have
703
allowed highly precise modifications in the DNA sequence and can represent a
704
breakthrough in plant breeding (Chen et al., 2019; Schindele et al., 2020). Due
705
to its simplicity, efficiency and versatility, CRISPR/Cas9 has overcome the
706
ZFNs and TALENS techniques and has been successfully used to promote
707
precise multiplex modifications on DNA of different organisms, including plants
708
(Armario Najera et al., 2019). By means of the simultaneous editing of multiple
709
targets, CRISPR systems hold a promise to build regulatory circuits, which
710
could create novel traits for precise plant breeding in agriculture (Chen et al.,
711
2019). All this success in DNA editing through the CRISPR/Cas technique has
712
shed new light on plant breeding and will probably allow us to get around the
713
big current challenge of producing food that can supply the demands of a
714
growing world population. Given the current scenario, genome editing through
715
the CRISPR technique has the potential to allow thousands of years of
716
domestication and crop improvement to be revived and restructured, making
717
food production more socially and environmentally sustainable.
718
Although the de novo domestication or re-domestication presents itself
719
as valuable approaches to engineering improved photosynthesis, a cautionary
720
note is the fact that most cultivated plants were selected mainly according to
721
survival or production during evolution (Denison et al., 2014; Leister, 2019b;
722
Weiner, 2019) and not necessarily for higher photosynthetic rates. In this
723
context it should not be overlooked that, the advantageous traits conferring
724
better photosynthesis that we are only starting to reveal, most likely have not
725
been selected under natural conditions or by domestication processes. It seems
726
reasonable to assume therefore that traits that confer higher photosynthesis can
727
be more easily transferred to those crops. It should be noticed that, although
728
higher photosynthesis is clearly an important trait, not only stress-resistant
729
crops are also required to ensure yield stability, but also nutrient efficiency
730
crops should be of special attentions in the near future. It is equally important to
731
mention that the compelling evidence has revealed that improvements of model
732
and non-cultivated species can be achieved by single domestication genes 22
733
(reviewed in Fernie and Yan, 2019; Bailey-Serres et al., 2019; Zsögön et al.,
734
2017).
735
By
regulating
diverse
pathways
involved
in
plant
growth
and
736
development, transcription factors (TFs) also represent an important class of
737
potential targets for modifying domestication-related phenotypes and conferring
738
tolerance to environmental stress (Ambavaram et al., 2014; Wu et al., 2019). In
739
agreement, several examples of TFs modification strategies have been used in
740
different species. For instance, by using transgenic rice plants expressing the
741
TF HYR (HIGHER YIELD RICE) it was demonstrated that HYR is a master
742
regulator, directly activating cascades of TFs and other downstream genes
743
involved in photosynthetic carbon metabolism and yield stability under either
744
normal or drought conditions (Ambavaram et al., 2014). In addition, the control
745
of grain size and rice yield performed by OsGRF4 (Growth Regulating Factor 4)
746
appears to occur by modulating specific brassinosteroid-induced responses
747
(Che et al., 2015; Liebsch and Palatnik, 2020). Moreover, the overexpression of
748
a maize MADS-box transcription factor gene, zmm28 culminated with increases
749
in growth, photosynthesis capacity, and nitrogen utilization in maize (Wu et al.,
750
2019). Altogether, these and other examples justify the overrepresentation of
751
TFs in the list of known genes underlying domestication (Olsen and Wendel,
752
2013; Zhu et al., 2019) and make TFs potentially suitable for targeted
753
modification by synthetic biology tools.
754 755
A long road ahead: the best of synthetic biology is yet to come
756 757
Much attention has been given to the improvement of photosynthesis as
758
an approach to optimize crop yields to fulfil human needs for food and energy
759
(Nowicka et al., 2018). Plant biotechnology is currently facing a dramatic
760
challenge to develop crops with higher yield, increased resilience and higher
761
nutritional content. Recent developments in genome editing and genetic
762
manipulation have been used to boost an impressive number of targeted
763
approaches to simultaneously produce more and more sustainably. Even
764
though more targeted and precise genetic manipulation strategies have been
765
recently generated in plant photosynthesis, a range of challenges remains. In
766
conjunction with extensive system biology data, these manipulations have 23
767
clearly advanced our understanding of the contribution of individual genes,
768
transcripts,
769
Considering the tremendous amount of time and resources invested to
770
‘improve’ plants (Weiner, 2019), the observations above raise the question of
771
how, when and to what extent these improvements will solve world food crises
772
(Sinclair et al., 2019). The fact that evolution has not already provided such
773
‘improved’ plants in nature by positively selecting mutations demonstrate that
774
more progress is likely to happen if breeders think in terms of ‘trade-offs’
775
instead of ‘improvements’ (Weiner, 2019). Moreover, revolutionary synthetic
776
biology technologies must be effectively engaged to access new opportunities
777
aimed at transform agriculture (Wurtzel et al., 2019) and provide not only
778
improved yield but also stress resilient crops, while facing major climatic
779
changes (Bailey-Serres et al., 2019). Alternatively, it is quite probable that
780
photosynthesis will be made more efficient if designed outside of plants (Liu et
781
al., 2016; Weiner, 2019), by means of future developments of enzymology and
782
computational approaches to overcome the limitations associated with the
783
execution of synthetic pathways that are now tractable to be designed in silico
784
(Erb, 2019). Once synthetic biology has opened the door toward comprehensive
785
networks for the utilization of solar energy and carbon sources (Luan et al.,
786
2020), the future will tell us whether synthetic biology will fully develop its
787
tremendous potential for building completely novel pathways and crops in
788
predictable desired directions and, thus, provide the solutions for the social,
789
economic and environmental challenges we already have at hand.
proteins
and
metabolites
for
photosynthetic
performance.
790 791
Author Contributions
792
W.B-S., and P. F-P. jointly wrote the original manuscript draft, prepared the
793
figures and table. A.O.M. contributed to writing and preparation of figures and
794
tables. A.Z., A.N-N., and W.L.A. planned the review outline. All authors
795
contributed to the reviewing and editing of the manuscript.
796 797
Acknowledgements
798
This work was made possible through financial support from the Serrapilheira
799
Institute (grant Serra-1812-27067), the Max Planck Society, the CNPq (National
800
Council for Scientific and Technological Development, Brazil) [grant No. 24
801
402511/2016-6]; the FAPEMIG (Foundation for Research Assistance of the
802
Minas Gerais State, Brazil) [grant Nos. APQ-01357-14, APQ-01078-15, and
803
RED-00053-16]. We also thank the scholarships granted by the Brazilian
804
Federal Agency for Support and Evaluation of Graduate Education (CAPES-
805
Brazil) to PF-P and WB-S. Research fellowships granted by CNPq-Brazil to
806
ANN and WLA are also gratefully acknowledged. No conflict of interest
807
declared.
808 809 810 811 812
25
813
Figure legends
814 815
Figure 1 - Light reactions and potential targets for improvement
816
strategies. Overview of linear electron flow from water oxidation by OEC (gray
817
rectangle) in the PSII LHCII super complex (light green), though cytochrome b6f
818
(orange), to PTOX (light red circle) and/or PC (circle red) or algal cytochrome c6
819
(opened rectangle), then to PSI-LHCI (light green), followed by reduction of
820
NADP+ by ferredoxin (brown) and ferredoxin:NADP+ reductase (oval purple
821
circle), releasing protons into the lumen, which is then used to drive the ATP
822
biosynthesis by ATP synthase (blue). In addition to linear electron flow, there
823
are also cyclic electron transfer pathways that mediated by PGR5/PGRL1 or
824
NDH complex (purple). These pathways confer dynamic protection preventing
825
the production of ROS Noteworthy, ion channels, such as TPK3 and KEA3
826
(yellow), can be modulated by light fluctuations, regulating the proton motive
827
force in the chloroplast and thus be important regulators of ATP biosynthesis by
828
exchanging K+ and H+ between stroma and lumen. Moreover, recently in
829
Nicotina benthamiana a new strategy rerouting electron transferred by PSI to
830
P450s monooxygenase was performed (Mellor et al., 2016; Urlacher and
831
Girhard, 2019).CYP fused into Fd was expressed in the thylakoid membrane of
832
chloroplasts, enabling direct coupling of photosynthetic electron transfer to the
833
heme iron reduction. The reducing power (e−) needed for dhurrin formation in
834
the chloroplast is thus ultimately derived by the water splitting activity of PSII
835
(pink, gray and yellow intermembrane canes). Abbreviation:
836
Photosystem I light-harvesting complex I; PSII-LHCII, Photosystem II light-
837
harvesting complex II; PQ, Plastoquinone; PQH, semi-plastoquinone; PTOX,
838
plastoquinol terminal oxidase;
839
Cytb6f, cytochrome b6f; OEC, oxygen-evolving complex; Fd; ferredoxin; NDH,
840
NAD(P)H dehydrogenase; PGR5, proton gradient regulation 5; PGRL1, PGR5-
841
like protein 1; TPK3, two-pore K+ channel3 ; KEA3, potassium cation efflux
842
antiporter3.
PSI-LHCI,
PC, plastocyanin; Cyt C6, cytochrome C6;
843 844 845
26
846
Figure 2 - Photosynthetic mechanisms and strategies used to introduce
847
carbon concentration mechanisms (CCMs) into C3 plants. A) Converting
848
C3 into C4 mechanism. The transition from C3 to C4 metabolism requires the
849
differentiation of photosynthetically active vascular BS cells, modification in the
850
biochemistry reactions of several enzymes and modulation of metabolites
851
transport in both inter and intracellular compartments, as well as transferring
852
GDC into BS cell (Schuler et al., 2018). B) Converting C3 into Crassulacean
853
Acid Metabolism (CAM). The pathway of CAM in a mesophyll cell is temporally
854
separated. The different background color indicates light at the top and dark at
855
the bottom. The green-boxes on both sides indicate the epidermis under these
856
two different conditions (opened – night and closed – day). As an alternative
857
engineering target and less complicate process not involving changes in
858
morphological structure, is the introduction of CAM metabolism into C3 plants.
859
Such engineering requires precise control of several key enzymes, such as
860
PEP carboxylase, malic enzyme, and RuBisCO (Kubis and Bar-Even, 2019). C)
861
Transferring cyanobacteria and algal CCM components to C3 chloroplasts.
862
Transfer of HCO3- transporter (red and yellow circle) on inner chloroplast
863
membrane and expression of functional carboxysome (yellow icosahedron) and
864
introducing an algal pyrenoid CCM (brown circle) in the chloroplast stroma.
865
Long et al., (2018) using sophisticated approaches took us to a closer step to
866
achieving high stromal HCO3- pool in the presence of functional carboxysome
867
increasing CO2 fixation and yield up to 60% in transformed tobacco, as
868
previously predicted by McGrath and Long (2014). Abbreviations: Asp,
869
Aspartate; CA, carbonic anidrase; GDC, glycine decarboxylase; PEP,
870
phosphoenolpyruvate; PEPcase, phosphoenolpyruvate carboxylase; PPDK,
871
pyruvate phosphate dikinase; ME, malic enzyme.
872
27
873
Figure 3 - Calvin-Benson Cycle (CBC) advances, RuBP supply and
874
photorespiratory bypasses. RuBisCO catalyze CO2 and O2 fixation. The
875
product of CO2 fixation is the 3PGA that enters in the CBC and can be directed
876
to starch biosynthesis and/or sugars in the cytosol (black arrow). In addition, the
877
oxygenation drives the production of 2PGA, which is metabolized in the C2
878
photorespiratory pathway (blue arrows). Recently, three new synthetic
879
photorespiratory bypasses have been proposed to improve the carbon
880
assimilation and reduce photorespiration losses in C3 plants. See details in pink
881
circles (1), glycolate is diverted into glycerate within the chloroplast, shifting the
882
release of CO2 from mitochondria to chloroplasts, and reducing ammonia
883
release (dashed light green arrows) (For details see Kebeish et al., 2007); (2)
884
Peroxisomal pathway, catalyzed by two Escherichia coli enzymes, convert
885
glyoxylate into hydroxypyruvate and CO2 in a two-step process (brown) (For
886
details see Peterhänsel et al., 2012); (3) Lastly, bypass 3 is considered a non-
887
real bypass since the glycolate is completely oxidized into CO2 inside
888
chloroplasts by both newly introduced and native enzymes (dashed red arrows)
889
(For details see Peterhänsel et al., 2012; Fonseca-Pereira et al., 2020). In
890
parallel, overexpression of GDC (oval circle gray) in Arabidopsis increased net
891
carbon assimilation. Besides of that, RuBisCO activity is also limited by RuBP
892
regeneration, which involved two main enzymes, SBPase and FBPA (oval circle
893
yellow). The combination of SBPase and FBPA overexpression resulted in
894
cumulative positive effects on leaf area and biomass accumulation (Parry et al.,
895
2017). Recent studies have showed that BSD2 (red star) chaperone is crucial
896
for cyanobacterial RuBisCO assembly into functional enzyme in tobacco
897
(Conlan et al., 2018). Therefore, all these changes are considered important
898
check point targets to optimize and improve the photosynthetic efficiency.
899
Abbreviations: 3PGA, 3-phosphoglycerate; CBC, Calvin-Benson cycle; FBPA,
900
fructose-1,6-bisphosphate
901
bisphosphatase; BSD2, bundle sheath defective 2 protein.
aldolase;
SBPase,
sedoheptulose-1,7-
902
28
903
Table 1 - Some domesticated genes that are providing improvements on photosynthetic rates and/or crops yield. Crop
Domesticated genes
Function
Traits
Reference
Fructose-1,6-bisphosphate FBPA/SBPase:
aldolase/Sedoheptulose-1,7bisphosphatase
ictB
Increases on photosynthetic
leaf (Simkin Cyanobacterial putative2015) area, and biomass yield inorganic carbon transporter carbon
assimilation,
et
al.,
B, Tobacco
Tomato
(López-Calcagno
GCS H-protein
Glycine cleavage system
Biomass yield
PsbS
Photosystem II Subunit S
(Głowacka et al., Reduction in water loss per CO2 assimilated 2018)
ZEP VDE PsbS
Zeaxanthin epoxidase Volaxanthinde-epoxidase Photosystem II Subunit S
SP (Self pruning)
Flowering repressor
SBPase
Sedoheptulose-1,7bisphosphatase
ictB
Inorganic carbon transporter B
Rice
Increased leaf CO2 uptake and plant dry matter productivity A quick burst of flower production that translates to an early yield Enhancement of photosynthesis to high temperature Higher photosynthesis and carboxylation efficiencies, lower CO2 compensation
et al., 2018)
(Kromdijk et al., 2016b) (Soyk et al., 2017) (Feng et al., 2007a) (Yang et al., 2008)
29
points Fructose-1,6-bisphosphate Net photosynthetic rate, aldolase/Sedoheptulose-1,7(Gong et al., 2017) carboxylation efficiency bisphosphatase Formerly icfA: inorganic ccaA carbon fixation A Sugars Will Eventually be (Sosso et al., ZmSWEET4c/OsSWEET4 Seed filling Exported Transporters 2015) FBPA/SBPase
Wheat
SBPase
Maize
ZmSWEET4c/OsSWEET4
PRK
Sedoheptulose-1,7-
Improves
bisphosphatase
and grain yield
Sugars
will
eventually
be
exported transporters Phosphoribulokinase
GDC L-protein
Glycine cleavage system
et
al.,
et
al.,
2017) (Sosso
Seed filling
2015)
Photosynthetic
capacity, (López-Calcagno
growth and seed yield increased
Arabidopsis
photosynthesis (Driever
rates
of
et al., 2017) CO2
assimilation, photorespiration, and plant
(Timm et al., 2015)
growth
soybean
PetC
Rieske FeS subunit of the Cytochrome b6f complex
ictB
Inorganic carbon transporter B
increases electron transport (Simkin et al., rates and biomass yield 2017a) Increases in photosynthetic (Hay et al., 2017) CO2 and dry mass
30
Setaria viridis
PetC
Rieske FeS subunit of the Cytochrome b6f complex
Better light conversion (Ermakova et al., efficiency, higher CO2 2019a) assimilation
31
904
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905
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Figure 1
OEC
e-
2H2O
e-
NDH
Fd
Fd PSI LHCI
PTOX PC Cyt c 6 e-
e-
CYP71E1 CYP79A1
Oxime
e-
Hydroxylation
K+ K+ H+
K+ K+ H+
H+ ATP synthase
PQH
PGR5/PGRL1
-
PSII PQ e LHCII
Cytb6f
Fd
UGT85B1
KEA3
e-
Cyanohydrin
Tyrosine
Hydroxylation e-
ADP+Pi
TPK3
FdR
e-
ATP
Dhurrin Glycosylation
NADP+H NADPH +
H+
Stroma
Lumen
O2 + 4H+
Figure 1 - Light reactions and potential targets for improvement strategies.
Figure 2
A
B
Sucrose Starch Fructan
PEP
Malate
Vacuole
Malate
Malate PPDK PEPcase
PEP
Pyruvate
Chloroplast
HCO 3CA
Night-time
Mesophyll cell
OAA
Light-time
Pyruvate
CO2
CO2
H2O
H2O
Chloroplast
C 3PGA 2PG
Sugar
Algal Pyrenoid
CBC
CBC
3-PGA
RuBP O2 CO2
CO2 HCO3Cyanobacteria Carboxysome
HCO3-
Figure 2 - Photosynthetic mechanisms and strategies used to introduce carbon concentration mechanisms (CCMs) into C3 plants.
Figure 3 NADH CO2
3 Pyruvate
Acetyl-CoA
NADPH CO2
Malate CO2
GDC
Tartronic Semialdehyde
Glycolate 3PGA
2PG
1
NAD+
Glycerate CO2 Tartronic semialdehyde
FBPA
2
CBC SBPase Glycerate
BSD2
RuBP CO2
Hydroxypyruvate
RubisCO O2
Figure 3 - Calvin-Benson Cycle (CBC) advances, RuBP supply and photorespiratory bypasses. RuBisCO catalyze CO2 and O2 fixation.