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Improving photosynthesis through multidisciplinary efforts: the next frontier of photosynthesis research.

• 1 Center of Excellence for Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai, China
• 2 Department of Agronomy, Faculty of Agriculture, Sher-e-Bangla Agricultural University, Dhaka, Bangladesh
• 3 School of Biotechnology, Devi Ahilya University, Indore, India
• 4 School of Life Science, University of Essex, Colchester, United Kingdom
• 5 Key Laboratory of Photobiology, Institute of Botany, Chinese Academy of Sciences, Beijing, China
• 6 School of Advanced Agricultural Sciences, Peking University, Beijing, China
• 7 Institute of Systems, Molecular and Integrative Biology, University of Liverpool, Liverpool, United Kingdom
• 8 National Laboratory of Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing, China
• 9 School of Life Sciences, Shandong Agricultural University, Taian, China
• 10 Department of Botany, School of Biology, Aristotle University of Thessaloniki, Thessaloniki, Greece
• 11 Department of Botany, University of Innsbruck, Innsbruck, Austria
• 12 Center of Excellence for Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai, China
• 13 Department of Plant Sciences, Centre for Crop Systems Analysis, Wageningen University & Research, Wageningen, Netherlands
• 14 Department of Agronomy, Shihezi University, Shihezi, China

The light-dependent release of oxygen from plants was first discovered in the 1770s by Joseph Priestley and Jan Ingenhousz. More recently, the enzyme-catalyzed pathway of carbon assimilation was characterized by Melvin Calvin, James Bassham, and Andrew Benson in 1950, and since then, photosynthesis has been intensively studied by hundreds and thousands of other pioneers. So far, the major components of photosynthesis in different systems and the regulations over these components have been gradually revealed. Now, photosynthesis research is entering a new era, with the ambitious goal of providing new green solutions for overcoming the challenges facing our society, such as ensuring the sustainable supply of food, fiber, and fuel, as well as improving the ecological stability of our planet. We can also conceive that one day we may also leave our planet to live on others, but certainly not without photoautotrophs! Developing photosynthetic systems, both natural and artificial, with greater efficiency in using resources, such as light, nitrogen, CO 2 , and water, to benefit human society and our planet, is becoming a new frontier of research and a hallmark of this exciting era of photosynthesis research.

Why is there large scope to improve photosynthesis?

There are great variations in the photosynthetic energy conversion efficiency in extant plants, which are nonetheless usually less than 1/3 of the theoretical optimal photosynthetic light use efficiency ( Zhu et al., 2008 ; Slattery and Ort, 2015 ; Yin and Struik, 2015 ). The increased production of biomass and yield in major crops under Free Air CO 2 Enrichment experiments shows that increasing photosynthesis can indeed increase crop yield ( Long et al., 2006 ). Many arguments can be used to explain why evolution has not resulted in optimal photosynthesis. First, evolution selects for survival over productivity. Usually, one particular anatomical, physiological or developmental feature, which confers better tolerance to a particular stress, can offer plants higher fitness in their growth habitat regardless of whether the plant by chance has a high photosynthetic rate or not. As an extreme example, having mechanisms to maintain a high water use efficiency, e.g., the Crassulacean acid metabolism, will be a preferred option for survival in an extremely dry environment while maintaining a superior photosynthetic rate becomes less critical under this condition. Second, since photosynthesis first evolved, there have been dramatic changes in climate, such as CO 2 levels, temperature, precipitation, etc., all historically leading to specialized adaptations that can now be considered “outdated.” Just in the past 200 years, atmospheric CO 2 levels increased from about 200 ppm to 410 ppm, average global temperatures have soared by 1.5°C and precipitation has become increasingly erratic ( IPCC Climate Change, 2021 ). Such rapid changes open up possibilities to optimize photosynthesis toward current and future climate scenarios. Furthermore, the climate is changing at a speed faster than the speed of plant adaptation. This has been demonstrated earlier, for example, by the kinetic properties of Rubisco, for which kinetic properties fit better to the CO 2 level of 400,000 years ago ( Zhu et al., 2004 ). The changes in the global temperature also have a major impact on photosynthetic performance ( Sage and Kubien, 2007 ). Thus, sub-optimality of photosynthesis can be related to the legacy of evolution. Rubisco evolved 2.4 billion years ago, which was a hypoxic and CO 2 -rich environment, under which the inefficiency of Rubisco carboxylation activity was not relevant ( Banda et al., 2020 ).

In contrast to these reasons why evolution has not selected the optimal photosynthesis, there are also other parallel arguments on the current photosynthetic properties that may already represent an “optimal” choice for plants. The balance between plant growth and stress resistance in a highly variable and potentially stressful environment may also prevent the maximization of photosynthesis and hence growth potential ( Zhang et al., 2020 ), i.e., the diverse photosynthetic properties in nature represent different evolutionary choices for plants to survive and thrive in their habitats without human intervention. Along this vein, it is interesting to note that, green plants, purple bacteria, and green sulfur bacteria have drastically different absorption spectra, however, their current light absorption spectrum may be an “optimal” design for the light conditions they commonly experience ( Arp and Kistner-Morris, 2020 ). Similarly, Rubisco, being able to catalyze both ribulose bisphosphate (RuBP) carboxylation and also RuBP oxygenation, may also well represent an evolutionary preferred choice compared to a hypothetically perfect Rubisco, which can only catalyze RuBP carboxylation. This is again because, under stress conditions, this RuBP oxygenation capacity can not only help dissipate excess light energy but also help maintain a metabolite pool which can, when needed, be used to rapidly provide intermediates for the Calvin-Benson cycle ( Stitt and Borghi, 2021 ).

A few factors underlie huge opportunities to improve photosynthesis. First, the rapid global climate change outpaced the speed of plant evolution, as discussed earlier. Second, during crop domestication, crops have drastically different growth habitats compared to those of their ancestors. For example, modern crops usually are grown in monoculture as a dense canopy, as compared to their ancestors which often have access to plenty of sunlight. Thirdly, compared to the situation of plants growing in the wild, which can only rely on their repertoire of weapons and solutions to cope with stresses, crops in agriculture can be protected through human intervention (irrigation, fertilizer application, disease control, etc). As a result, plants can take a competitive growth strategy, rather than a stress tolerant or ruderal strategy ( Grime, 1977 ).

Though it is desirable for plants to have a high demand for improving photosynthetic efficiency, it is worth noting here that, under certain conditions, such as under high light, the photosynthetic efficiency becomes less important, while effective photoprotective mechanisms and ensuring total photosynthetic yield becomes more relevant for plants. Indeed, sophisticated mechanisms have evolved to ensure high photosynthetic yield under high light, especially under concurrent high light and stress combinations, while at the same time confer higher quantum yield when the light becomes a scarce resource ( Ort, 2001 ). This scenario again implies opportunities to utilize the excess energy which is otherwise largely wasted in photoprotection, as shown in the recent success of engineering a faster recovery from photoprotection for greater biomass production ( Kromdijk et al., 2016 ).

Here, we emphasize that the rapid development of synthetic biology tools now offers new opportunities to create completely new designs of improved photosynthetic systems and tailoring photosynthesis to the increasing demands in the context of our changing climate ( Zhu et al., 2020 ). In the following sections, we briefly discuss the available opportunities, the tools used to support studying photosynthesis, and the associated research areas.

An incomplete list of options to improve photosynthesis

First, we provide an incomplete list of opportunities to improve photosynthetic efficiency:

(1) Creating more efficient light harvesting systems, which could utilize the expanded solar spectrum for the generation of proton motive force for generation of ATP and NADPH ( Ort et al., 2015 ) and/or smaller chlorophyll antenna size and lower chlorophyll content reducing the excess absorption of sunlight and improving photosynthetic efficiency ( Ort et al., 2011 ; Moustakas et al., 2022 ).

(2) Creating more efficient photo-protection systems to minimize heat dissipation when unnecessary and to maximize photochemistry;

(3) Creating more efficient state transition and electron transferring between PSII and PSI under changing environment to maximize light-use efficiency;

(4) Generating a Rubisco with a greater catalytic rate and higher specificity for CO 2 ;

(5) Repurposing efficient CO 2 -concentrating mechanisms, either these are Kranz type CO 2 -concentrating mechanisms, or carboxysome- or pyrenoid-based systems to decrease the Rubisco oxygenation flux;

(6) Creating a novel pathway to cope with photorespiratory CO 2 and ammonia loss to minimize the energy associated with refixation of CO 2 and ammonia;

(7) Developing an effective combination of biological CO 2 fixation with solar energy capture to further increase the efficiency of harvesting light energy through capitalizing on the high light conversion efficiency of photovoltaic systems;

(8) Developing nanomaterials to enable better capturing and delivery of CO 2 to Rubisco to decrease the Rubisco oxygenation;

(9) Enhancing antioxidant defense under natural changing conditions to decrease the photodamage;

(10) Development of artificial systems that cope better with high light different conditions through channeling the excess light for production of renewable chemical energy;

(11) Overcoming sink limitations of photosynthesis;

(12) Developing improved stomatal dynamics to increase water and light use efficiency.

(13) Develop photosynthetic systems that can better utilize fluctuating light conditions;

(14) Creation of novel photosynthetic systems which may enable human space exploration.

These are all basic elements required to build a repertoire of highly efficient systems. When these modules for higher efficiency are individually developed, or achieved in combination, we could gain increased plant yield potential either for biomass or grain or storage tissues, as well as greener energy sources.

Technologies and tools to support a new era of photosynthesis research

The rapid progress in many new technologies and tools provides sufficient toolsets for us to overcome these grand challenges and goals ( Table 1 ). These major technological advances that will revolutionize photosynthesis research in the future include:

• Techniques to scan photosynthetic systems . The advances in the fluorescence imaging techniques for in vivo scanning of natural photosynthetic systems will enable in situ characterization of photosynthetic pigment-protein complexes and their distribution/dynamics under different conditions ( Casella et al., 2017 ; Mullineaux and Liu, 2020 ). This information and elucidation of their physiological significance will provide basic information which is needed for the future de novo design of artificial photosynthetic systems.

• Techniques for studying the molecular and supramolecular basis of photosynthesis . The recent development of cryo-electron microscopy (cryo-EM) technology enables rapid progress in solving the structures of major proteins, protein complexes and supercomplexes involved in photosynthesis at near-atomic resolutions through the single-particle analysis method ( Wei et al., 2016 ; Su et al., 2017 ; Zhang et al., 2017 ; Malone et al., 2019 ; Pi et al., 2019 ; Pan et al., 2020 ). Atomic force microscopy (AFM) technology provides the opportunity to delineate the lateral arrangement, protein interactions and dynamics of photosynthetic complexes in the context of photosynthetic membranes ( Liu and Scheuring, 2013 ; Wood et al., 2018 ; Zhao et al., 2020 ). In addition, the cryo-electron tomography (cryo-ET) method allows researchers to visualize the in situ arrangement of photosynthetic complexes in chloroplasts and CO 2 -fixing organelles ( Engel et al., 2015 ; Freeman Rosenzweig et al., 2017 ; Wietrzynski et al., 2020 ; Gupta et al., 2021 ; Ni et al., 2022 ). The structural information combined with the variation of genomic sequences and corresponding changes in biophysical or biochemical properties of the proteins/protein complexes will enable the determination of the molecular and supramolecular basis underlying photosynthetic processes and regulation. The detailed physical mechanisms can then be revealed through a combination of such biological or genetic manipulation, e.g., base editing, experiments with molecular dynamics simulations, especially those that combine quantum mechanics and molecular mechanics (MoD QM/MM) ( Liguori et al., 2020 ) and artificial intelligence-based protein structure prediction ( Jumper et al., 2021 ). It is worth pointing out here that the combination of multiple approaches will not only enable studies on the structure-function relationship of proteins or protein complexes, but also may stimulate ab initio design of new protein/protein complexes with desired properties ( Hsia et al., 2021 ).

• Techniques to mine superiority within the natural variation of photosynthesis . Though in current plants, a photosynthetic system with all components in an optimal state is not yet available, there are great natural variations of photosynthetic machinery across diverse photosynthetic organisms. High-throughput plant phenotyping techniques combined with genome-wide association techniques and genetic tools can allow the identification of novel genes controlling photosynthetic efficiency and characterize those genetic variations conferring superior traits for some components of photosynthesis.

• Multi-scale systems modeling of photosynthesis . The modeling will allow not only the dissection of biological, biophysical, and biochemical mechanisms controlling the efficiency of a particular photosynthetic protein or complex, but also the rational design of optimal photosynthetic systems for greater efficiency under different environments ( Xiao et al., 2017 ). Novel photosynthetic models enable accurate prediction of the photosynthesis process and its regulation at different scales still needs to be developed.

• Availability of versatile synthetic biology tools allowing targeted manipulation of photosynthesis . A highly efficient photosystem requires a strongly coordinated expression of genes that encode the photosystem components. Many promoters that confer precise temporal, spatial, or tissue-specific expression of target genes are available ( Kummari et al., 2020 ); furthermore, with rapid advances in single-cell transcriptomics and stereomics data, new promoters conferring either temporal or spatial or development, or environment specificity will be rapidly identified ( Xia et al., 2022 ). CRISPR-CAS9 tools enable fine-tuning expression levels and translation efficiency have been developed ( Jiang and Doudna, 2017 ). All these will enable an unprecedented opportunity to design and implement new photosynthetic systems.

• Guided evolution techniques . Though during evolution, photosynthetic efficiency might not be a target that selection acts on, we can now implement guided evolution where optimal photosynthetic efficiency or enhanced properties of specific photosynthetic proteins can be a target for the experiment, as shown in the development of new CO 2 fixation pathway in Escherichia coli ( Antonovsky et al., 2016 ). Guided evolution tools combined with artificial intelligence can be used to support the optimization of photosynthetic proteins, such as Rubisco or new photosynthetic pathways, or even the creation of new options for improved photosynthetic efficiency, taking advantage of the power of random mutation and selection.

Table 1 . Methods used to study photosynthesis at different scales.

Research areas on photosynthesis to support development of new strategies for improved photosynthetic efficiency

As the basic process ultimately responsible for the generation of food, fiber, and fuel for our society, and also a crucial component of the global carbon cycle and the water cycle, photosynthesis is arguably one of the most important biological processes on this planet. Understanding how photosynthesis works, and how to further optimize it, will be a never-ending pursuit of humanity. Photosynthesis not only supplies materials and energy supporting our living organisms on Earth, but also holds the promise to provide the basic needs for humans in the forthcoming era of space life. The Photosynthesis and Photobiology section of Frontiers in Plant Sciences provides a unique arena for scientists working in this field to publish their recent advances in these fields; it will also be a window for industrial partners and stakeholders to present their recent development. Advances in photosynthesis research will be a showcase of the triumph of multi-disciplinary research across the diversity of photosynthetic organisms. This Photosynthesis and Photobiology section will welcome high-quality fundamental and applied research across all areas of photosynthesis and photobiology, which include but are not limited to:

• Architecture, assembly, biogenesis, and functional regulation of pigment-protein complexes, supercomplexes, and megacomplexes involved in the light reactions.

• Structure and mechanism of enzymes and transporters associated with photosynthesis and their regulation

• Structure and function of thylakoid membrane systems

• Mechanisms of light energy absorption, transfer, and conversion processes under different light regimes

• Structure, function, genetics, and reconstruction of different CO 2 -concentrating mechanisms (CCM)

• Structure and variation of gene regulatory networks controlling photosynthesis

• Factors controlling stomatal conductance and mesophyll conductance

• Factors controlling leaf and canopy photosynthesis

• Structure, function and genetic regulation of crassulacean acid metabolism

• Photosynthesis under changing climate conditions or stress conditions

• Photosynthesis under different supplies of either macromineral or microelement

• Multiscale models of photosynthesis

• Evolution of photosynthesis

• Photosynthesis on planets other than earth

• Natural variation of photosynthesis and their genetic basis

• Synthetic biology of photosynthesis for better enzymes, systems, or pathways

• Crop improvement for higher photosynthetic efficiency under a changing climate

• Light-induced signal transduction and photomorphogenesis

• Artificial photosynthesis and clean energy generation

• Creation of new hybrid photosynthetic systems for greater light use efficiency.

Photosynthesis research is entering a new era, where more and more work targets at enhancing its efficiency, in addition to the characterization of natural photosynthetic systems. Given that efficiency is inherently a system's property, i.e., it is a result of all the interacting components, rather than any single component. As a result, studying photosynthetic efficiency and identifying new options to improve efficiency will inevitably require the examination of photosynthesis at a range of spatial and temporal scales ( Figure 1 ). Therefore, in this new era of photosynthesis research, we will witness the final success of capitalizing on the power of photosynthesis tailored to gain optimal efficiency for different environments, which will rely on accurate in silico prediction of photosynthesis in action from the first principle based on the spatial arrangement of photosynthetic pigment-protein complexes, and sequence and structure of individual proteins involved. After centuries of research on photosynthesis, the twenty-first century will witness how photosynthesis research will help advance our agricultural and energy development, and sustainably maintain or even improve our environment. The Photosynthesis and Photobiology section of Frontiers in Plant Sciences will serve as an arena for the whole photosynthesis research community to team up and work together to welcome this new era of photosynthesis research.

Figure 1 . Photosynthesis research involves research at different scales. Here we illustrate the multi-scale properties of photosynthesis with the higher plant systems. Systematic studies of the structure, function and regulation of photosyhnthesis at canopy, plant, leaf, cell, chloroplast, pigment protein complexes etc are needed to develop effective methods to identify factors controlling photosynthetic efficiency and hence to design effective approaches to improve photosynthetic efficiency.

Author contributions

X-GZ drafted the article. All authors contributed to the article and approved the submitted version.

Acknowledgments

X-GZ acknowledges support from Ministry of Science and Technology of China (2019YFA0904600, 2019YFA09004600, and 2020YFA0907600), Chinese Academy of Sciences (XDB27020105), National Science Foundati on of China (31870214), Max Planck Society, and University of Illinois at Urbana Champaign for all the support over the years on photosynthesis research. L-NL acknowledges supports from Royal Society (URF\R\180030), the Biotechnology and Biological Sciences Research Council (BBSRC) (BB/V009729/1 and BB/M024202/1), the Leverhulme Trust (RPG-2021-286).

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher's note

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Keywords: photosynthesis, photobiology, multiscale, efficiency, modeling, natural variation, synthetic biology

Citation: Zhu X-G, Hasanuzzaman M, Jajoo A, Lawson T, Lin R, Liu C-M, Liu L-N, Liu Z, Lu C, Moustakas M, Roach T, Song Q, Yin X and Zhang W (2022) Improving photosynthesis through multidisciplinary efforts: The next frontier of photosynthesis research. Front. Plant Sci. 13:967203. doi: 10.3389/fpls.2022.967203

Received: 12 June 2022; Accepted: 18 August 2022; Published: 30 September 2022.

Reviewed by:

Copyright © 2022 Zhu, Hasanuzzaman, Jajoo, Lawson, Lin, Liu, Liu, Liu, Lu, Moustakas, Roach, Song, Yin and Zhang. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY) . The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Xin-Guang Zhu, zhuxg@cemps.ac.cn

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Photosynthetic research in plant science.

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Ayumi Tanaka, Amane Makino, Photosynthetic Research in Plant Science, Plant and Cell Physiology , Volume 50, Issue 4, April 2009, Pages 681–683, https://doi.org/10.1093/pcp/pcp040

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Photosynthesis is a highly regulated, multistep process. It encompasses the harvest of solar energy, transfer of excitation energy, energy conversion, electron transfer from water to NADP + , ATP generation and a series of enzymatic reactions that assimilate carbon dioxide and synthesize carbohydrate.

Photosynthesis has a unique place in the history of plant science, as its central concepts were established by the middle of the last century, and the detailed mechanisms have since been elucidated. For example, measurements of photosynthetic efficiency (quantum yield) at different wavelengths of light (Emerson and Lews 1943 ) led to the insight that two distinct forms of Chl must be excited in oxygenic photosynthesis. These results suggested the concept of two photochemical systems. The reaction center pigments of PSII and PSI (P680 and P700, respectively) were found by studying changes in light absorbance in the red region (Kok 1959 , Döring et al. 1969 ). Chls with absorbance maxima corresponding to these specific wavelengths were proposed as the final light sink. These Chls were shown to drive electron transfer by charge separation. The linkage of electron transfer and CO 2 assimilation was suggested by studies on Hill oxidant (Hill 1937 ). A linear electron transport system with two light-driven reactions (Z scheme) was proposed based upon observations of the redox state of cytochromes (Hill and Bendall 1960 , Duysens et al. 1961 ), and photophosphorylation was found to be associated with thylakoid fragments (Arnon et al. 1954 ). The metabolic pathway that assimilates carbon by fixation of CO 2 was discovered by Calvin's group who used 14 CO 2 radioactive tracers in the 1950s (Bassham and Calvin 1957 ). This was the first significant discovery in biochemistry made using radioactive tracers. The primary reaction of CO 2 fixation is catalyzed by Rubisco (Weissbach et al. 1956 ), initially called Fraction 1 protein (Wildman and Bonner 1947 ). Rubisco is the most abundant protein in the world, largely because it is also the most inefficient with the lowest catalytic turnover rate (1–3 s –1 ). Another CO 2 fixation pathway was then found in sugarcane (Kortschak et al. 1964, Hatch and Slack 1965) and named C 4 photosynthesis.

Although photosynthesis plays the central role in the energy metabolism of plants, historically there have not been strong interactions between photosynthesis research and other fields of plant science. Many techniques and tools developed for photosynthesis research have not been widely used in other fields because they were developed to examine phenomena unique to photosynthesis. For example, excitation energy transfer and charge separation are fundamental but unique processes of photosynthesis. Another reason for the historic isolation of photosynthesis research within plant science is that it was long believed that CO 2 fixation and carbohydrate production are the sole function of photosynthesis, with carbohydrates representing the only link between photosynthesis and other biological phenomena.

However, this situation has begun to change. Recent research has revealed that photosynthesis is closely related to a variety of other physiological processes. It is a major system for controlling the redox state of cells, playing an important role in regulating enzyme activity and many other cellular processes (Buchanan and Balmer 2005 , Hisabori et al. 2007 ). Photosynthesis also generates reactive oxygen species, which are now appreciated as being regulatory factors for many biological processes rather than inevitable by-products of photosynthesis (Wagner et al. 2004 , Beck 2005 ). Precursor molecules of Chl, which are a major component of photosynthesis, act as a chloroplast-derived signal, and are involved in regulating the cell cycle (Kobayashi et al. 2009 ). In light of this new information, it seems important to re-evaluate the function(s), both potential and demonstrated, of photosynthesis from a variety of view points. Photosynthesis research now employs the methods and tools of molecular biology and genetics, which are central methods for plant science in general. Meanwhile, Chl fluorescence and gas exchange measurements, developed especially for photosynthesis research, are now widely used in stress biology and ecology.

Photosynthesis research also contributes to our understanding of ecological phenomena and even the global environments (Farquhar et al. 1980 , de Pury and Farquhar 1997 , Monsi and Saeki 2005 ). Indeed, photosynthesis is now an integral component of simulation models used to predict the future of our planet. Improving the efficiency of photosynthesis by artificial modification of photosynthetic proteins and pathways has long been considered impossible or at best problematic, because, over evolutionary time, photosynthesis has become complex and tightly regulated. However, recent advances have made it possible to manipulate photosynthesis using molecular genetic technology (Andrews and Whiney 2003 , Raines 2006 ). These advances may have positive influences on crop productivity (Parry et al. 2007 ) as photosynthetic rates have frequently been correlated with biomass accretion (Kruger and Volin 2006 ). Thus, we can expect many more novel concepts to be added to this history of photosynthetic research.

As photosynthesis research tackles new challenges, we should also continue to re-evaluate past research. Oxygen evolution, energy dissipation and cyclic electron transport are crucial processes during photosynthesis, yet their mechanisms still remain to be clarified. We have very limited knowledge of the formation and degradation of photosynthetic apparatus. Also, although photosynthesis plays a central role in C and N metabolism in plants, we do not yet understand how potential photosynthesis is related to crop productivity.

Plant and Cell Physiology would like to contribute to the development of novel concepts, pioneering new fields and solving the unanswered questions of photosynthesis. This special issue covers a wide range of topics in photosynthesis research. Terashima et al. (pp. 684–697) readdress the enigmatic question of why leaves are green. They show that the light profile through a leaf is steeper than that of photosynthesis, and that the green wavelengths in white light are more effective in driving photosynthesis than red light. Evans (pp. 698–706) proposes a new model using Chl fluorescence to explore modifications in quantum yield with leaf depth. This new multilayered model can be applied to study variations in light absorption profiles, photosynthetic capacity and calculation of chloroplastic CO 2 concentration at different depths through the leaf.

Singlet oxygen, 1 O 2 , is produced by the photosystem and Chl pigments. 1 O 2 not only causes physiological damage but also activates stress response programs. The flu mutant of Arabidopsis thaliana overaccumulates protochlorophyllide that upon illumination generates singlet oxygen, causing growth cessation and cell death. Coll et al. (pp. 707–718) have isolated suppressor mutants, dubbed ‘singlet oxygen-linked death activator’ (soldat), that specifically abrogate 1 O 2 -mediated stress responses in young flu seedlings, and they discuss the processes of acclimation to stresses. Phephorbide a is a degradation product of Chl and one of the most powerful photosensitzing molecules. Mutants defective in pheophorbide a oxygenase, which converts phephorbide a to open tetrapyrrole, accumulate pheophorbide a and display cell death in a light-dependent manner. Hirashima et al. (pp. 719–729) report that pheophorbide a is involved in this light-independent cell death.

Plants regulate the redox level of the plastoquinone pool in response to the light environment. In acclimation to high-light conditions, the redox level is kept in an oxidized state by the plastoquinone oxidation system (POS). Miyake et al. (pp. 730–743) investigated the mechanism of POS using the Chl fluorescence parameter, qL.

Nagai and Makino (pp. 744–755) examine in detail the differences between rice and wheat, the two most commercially important crops, in the temperature responses of CO 2 assimilation and plant growth. They find that the difference in biomass production between the two species at the level of the whole plant depends on the difference in N-use efficiency in leaf photosynthesis and growth rate. Sage and Sage (pp. 756–772) examine chlorenchyma structure in rice and related Oryza species in relation to photosynthetic function. They find that rice chlorenchyma architecture includes adaptations to maximize the scavenging of photorespired CO 2 and to enhance the diffusive conductance of CO 2 . In addition, they consider that the introduction of Kranz anatomy does not require radical anatomical alterations in engineering C 4 rice.

Bioinformatics has become a powerful tool, especially in photosynthetic research, because photosynthetic organisms have a wide taxonomic distribution among prokaryotes and eukaryotes. Ishikawa et al. (pp. 773–788) present the results of a pilot study of functional orthogenomics, combining bioinformatic and experimental analyses to identify nuclear-encoded chloroplast proteins of endosymbiontic origin (CRENDOs). They conclude that phylogenetic profiling is useful in finding CPRENDOs, although the physiological functions of orthologous genes may be different in chloroplasts and cyanobacteria.

We hope you enjoy this special issue, and would like to invite you to submit more excellent papers to Plant and Cell Physiology in the field of photosynthesis.

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Natural and artificial photosynthesis: fundamentals, progress, and challenges

• Published: 14 November 2022
• Volume 154 , pages 229–231, ( 2022 )

Cite this article

• Mohammad Mahdi Najafpour 1 , 2 , 3 ,
• Jian-Ren Shen 4 &
• Suleyman I. Allakhverdiev 5  

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Energy from the sun directly or indirectly supports all life forms on our planet. In Nature, sunlight is converted into chemical energy by photosynthesis, the green engine of life on Earth. Literally, photosynthesis means “synthesis with light,” which has a broad meaning. Scientifically, photosynthesis is a biological process performed by plants, algae, and many bacteria to capture the sun’s energy and convert them into chemical energy. Indeed, as discussed by Blankenship, photosynthesis could be defined as a process in which an organism captures and stores light (Blankenship, 2021 ). The stored energy is utilized to drive energy-requiring cellular processes. Photosynthesis is the most significant reaction on earth and is estimated to produce more than 100 billion tons of dry biomass annually (Blankenship, 2021 ).

The transition from anoxygenic to oxygenic photosynthesis and the cooperation between photosystems I and II was a vital innovation at least 2.5 billion years ago by cyanobacteria, which confers organisms to the ability to store oxidizing equivalents. Such transition by Nature is difficult because water oxidation reaction toward oxygen production is a four-electron process, whereas photochemistry is a one-electron process (Tommos and Babcock 2000 ). Before this transition, the atmosphere had much more carbon dioxide and virtually no oxygen, and organisms used hydrogen or hydrogen sulfide as the sources of electrons (Ozaki et al. 2019 ).

Fossil fuels, a critical energy source for humans, and oxygen which allows life on an enormous scale in our planet’s atmosphere, are derived from millions of years of photosynthetic activity. Although Mn was known as a necessary ion in the structure of the water-oxidizing complex (WOC) many years ago, Barber and Iwata’s groups in 2004 reported that three Mn, one Ca, and possibly four bridging oxygen atoms form a cubic structure of WOC with a fourth Mn connected outside of the cubane, together with five putative water molecules, two coordinated to Ca, and three coordinated to the dangling Mn, in photosystem II (Ferreira et al. 2004 ). Shen and Kamiya, in 2011, found more details of the WOC and reported four manganese ions, one calcium ion, and five oxygen atoms in the structure, with four water molecules, two coordinated to the Ca, and two to the dangling Mn (Mn(4). The structure could thus be described as Mn 4 CaO 5 (H 2 O) 4 (Umena et al. 2011 ; Suga et al. 2015 ). They subsequently investigated the intermediate S-state structures following flash illuminations by X-ray free electron lasers (XFEL) and found the insertion of an oxygen atom (O6) at a position close to the O5 atom in the S 3 -state for the first time (Suga et al. 2017 ). This was confirmed by Kern et al. ( 2018 ) and Suga et al. ( 2019 ). The pump-probe time-resolved XFEL structural analysis further revealed the possible proton exit and water inlet pathways (Kern et al. 2018 ; Suga et al. 2019 ; Ibrahim et al. 2020 ; Hussein et al. 2021 ).

Indeed, many biological patterns, such as body size, are affected by the amount of oxygen in the earth’s atmosphere (Payne et al. 2011 ). Oxygen also produces the ozone layer 20–40 miles above the surface of the earth, which protects the earth from ultraviolet radiation. In addition, photosynthesis captures carbon dioxide from the air and then uses it to produce organic products, which serve as the energy source for almost all other life forms on the earth.

On the other hand, the development of the economy, the increase in the population, and the negative health effect of using fossil fuels cause significant problems in the earth’s environment, which force us to switch energy source to renewable ones such as solar and wind. The storage problem needs to be solved to fully use these renewable energy sources, because of the intermittent nature of renewable energy resources. Herein, photosynthesis could be a blueprint for the design of efficient systems to capture sunlight and store it in chemicals (Nagy and Garab 2021 ). On the other hand, developing technology in plant research could improve light use efficiency and ultimately the performance of cultivated species, leading to increased food production. Indeed, using new species to cultivate them in low-quality land for crop production under the global atmospheric change is an issue of particular interest (Srinivasan et al. 2017 ).

Recently, advanced techniques have improved our understanding of photosynthesis. Artificial photosynthesis tries to replicate natural photosynthesis by using sunlight to store energy and is an umbrella term for converting water, CO 2 , or N 2 into energy-rich compounds using sunlight artificially or by engineered bacteria (Bard and Fox 1995 ; Hammarström et al. 2001 ; Pace 2005 ; Kanan and Nocera 2008 ; Najafpour 2012 ; Najafpour and Allakhverdiev 2012 ). Many materials currently proposed in artificial photosynthetic systems are inefficient, non-durable, expensive, and/or toxic. A challenge in artificial photosynthesis is to use cheap and environmentally friendly compounds as Nature uses in photosynthesis. Although many intelligent strategies must be encouraged and tested, learning from the natural systems makes sense since Nature has been using this system successfully for millions of years.

In this special issue, we collected papers on the new progress in natural and artificial photosynthesis from different scientists in different countries. We hope you enjoy this particular issue and would like to invite you to submit your papers to the Photosynthesis Research journal in future.

Data availability

Data available on request from the authors.

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Acknowledgements

The authors wish to thank Institute for Advanced Studies in Basic Sciences (IASBS) and the National Elite Foundation for a grant which helped support this work. SIA was supported by a grant from the Russian Science Foundation (No. 19-14-00118) and the Ministry of Science and Higher Education of the Russian Federation (project No.122050400128-1). The authors would like to thank all the authors in this special issue and also thank professor Terry Bricker (Editor-in-Chief) and Matthew Cheng for their invaluable support.

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Mohammad Mahdi Najafpour

Center of Climate Change and Global Warming, Institute for Advanced Studies in Basic Sciences (IASBS), Zanjan, 45137-66731, Iran

Research Center for Basic Sciences & Modern Technologies (RBST), Institute for Advanced Studies in Basic Sciences (IASBS), Zanjan, 45137-66731, Iran

Research Institute for Interdisciplinary Science and Graduate School of Natural Science and Technology, Okayama University, Okayama, 700-8530, Japan

Jian-Ren Shen

K. A. Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Street 35, Moscow, 127276, Russia

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Najafpour, M.M., Shen, JR. & Allakhverdiev, S.I. Natural and artificial photosynthesis: fundamentals, progress, and challenges. Photosynth Res 154 , 229–231 (2022). https://doi.org/10.1007/s11120-022-00982-z

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Chemists create an 'artificial photosynthesis' system that is 10 times more efficient than existing systems

Uchicago breakthrough creates methane fuel from sun, carbon dioxide and water.

For the past two centuries, humans have relied on fossil fuels for concentrated energy; hundreds of millions of years of photosynthesis packed into a convenient, energy-dense substance. But that supply is finite, and fossil fuel consumption has tremendous negative impact on Earth’s climate.

“The biggest challenge many people don’t realize is that even nature has no solution for the amount of energy we use,” said University of Chicago chemist Wenbin Lin. Not even photosynthesis is that good, he said: “We will have to do better than nature, and that’s scary.”

One possible option scientists are exploring is “artificial photosynthesis”—reworking a plant’s system to make our own kinds of fuels. However, the chemical equipment in a single leaf is incredibly complex, and not so easy to turn to our own purposes.

A Nature Catalysis study from six chemists at the University of Chicago shows an innovative new system for artificial photosynthesis that is more productive than previous artificial systems by an order of magnitude. Unlike regular photosynthesis, which produces carbohydrates from carbon dioxide and water, artificial photosynthesis could produce ethanol, methane, or other fuels.

Though it has a long way to go before it can become a way for you to fuel your car every day, the method gives scientists a new direction to explore—and may be useful in the shorter term for production of other chemicals.

“This is a huge improvement on existing systems, but just as importantly, we were able to lay out a very clear understanding of how this artificial system works at the molecular level, which has not been accomplished before,” said Lin, who is the James Franck Professor of Chemistry at the University of Chicago and senior author of the study.

‘We will need something else’

“Without natural photosynthesis, we would not be here. It made the oxygen we breathe on Earth and it makes the food we eat,” said Lin. “But it will never be efficient enough to supply fuel for us to drive cars; so we will need something else.”

The trouble is that photosynthesis is built to create carbohydrates, which are great for fueling us, but not our cars, which need much more concentrated energy. So researchers looking to create alternates to fossil fuels have to re-engineer the process to create more energy-dense fuels, such as ethanol or methane.

In nature, photosynthesis is performed by several very complex assemblies of proteins and pigments. They take in water and carbon dioxide, break the molecules apart, and rearrange the atoms to make carbohydrates—a long string of hydrogen-oxygen-carbon compounds. Scientists, however, need to rework the reactions to instead produce a different arrangement with just hydrogen surrounding a juicy carbon core—CH4, also known as methane.

This re-engineering is much trickier than it sounds; people have been tinkering with it for decades, trying to get closer to the efficiency of nature.

Lin and his lab team thought that they might try adding something that artificial photosynthesis systems to date haven’t included: amino acids.

The team started with a type of material called a metal-organic framework or MOF, a class of compounds made up of metal ions held together by an organic linking molecules. Then they designed the MOFs as a single layer, in order to provide the maximum surface area for chemical reactions, and submerged everything in a solution that included a cobalt compound to ferry electrons around. Finally, they added amino acids to the MOFs, and experimented to find out which worked best.

They were able to make improvements to both halves of the reaction: the process that breaks apart water and the one that adds electrons and protons to carbon dioxide. In both cases, the amino acids helped the reaction go more efficiently.

Even with the significantly improved performance, however, artificial photosynthesis has a long way to go before it can produce enough fuel to be relevant for widespread use. “Where we are now, it would need to scale up by many orders of magnitude to make an sufficient amount of methane for our consumption,” Lin said.

The breakthrough could also be applied widely to other chemical reactions; you need to make a lot of fuel for it to have an impact, but much smaller quantities of some molecules, such as the starting materials to make pharmaceutical drugs and nylons, among others, could be very useful.

“So many of these fundamental processes are the same,” said Lin. “If you develop good chemistries, they can be plugged into many systems.”

The scientists used resources at the Advanced Photon Source, a synchrotron located at the U.S. Department of Energy’s Argonne National Laboratory, to characterize the materials.

The co-first authors of the paper were Guangxu Lan (PhD’20, now with Peking University), graduate student Yingjie Fan, and Wenjie Shi (Visiting student, now with Tianjin University of Technology. The other authors of the paper were Eric You (BS’20, now a graduate student at MIT) and Samuel Veroneau (BS’20, now a PhD student at Harvard University).

Citation: “ Biomimetic active sites on monolayered metal–organic frameworks for artificial photosynthesis .” Lan et al, Nature Catalysis, Nov. 10, 2022.

Funding: University of Chicago, National Science Foundation, China Scholarship Council

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Recent advances in understanding and improving photosynthesis

Affiliation.

• 1 Department of Biology, Universitat de les Illes Balears, INAGEA, Palma de Mallorca, Spain.
• PMID: 33659937
• PMCID: PMC7886073
• DOI: 10.12703/b/9-5

Since 1893, when the word "photosynthesis" was first coined by Charles Reid Barnes and Conway MacMillan, our understanding of the elements and regulation of this complex process is far from being entirely understood. We aim to review the most relevant advances in photosynthesis research from the last few years and to provide a perspective on the forthcoming research in this field. Recent discoveries related to light sensing, harvesting, and dissipation; kinetics of CO 2 fixation; components and regulators of CO 2 diffusion through stomata and mesophyll; and genetic engineering for improving photosynthetic and production capacities of crops are addressed.

Keywords: engineering photosynthesis; light harvesting; mesophyll conductance; photosystem; rubisco; stomatal conductance.

Copyright: © 2020 Flexas J et al.

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The authors declare that they have no competing interests.No competing interests were disclosed.No competing interests were disclosed.

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