From leaf to multiscale models of photosynthesis: applications and challenges for crop improvement.

To keep up with the growth of human population and to circumvent deleterious effects of global climate change, it is essential to enhance crop yield to achieve higher production. Here we review mathematical models of oxygenic photosynthesis that are extensively used, and discuss in depth a subset that accounts for diverse approaches providing solutions to our objective. These include models (1) to study different ways to enhance photosynthesis, such as fine-tuning antenna size, photoprotection and electron transport; (2) to bioengineer carbon metabolism; and (3) to evaluate the interactions between the process of photosynthesis and the seasonal crop dynamics, or those that have included statistical whole-genome prediction methods to quantify the impact of photosynthesis traits on the improvement of crop yield. We conclude by emphasizing that the results obtained in these studies clearly demonstrate that mathematical modelling is a key tool to examine different approaches to improve photosynthesis for better productivity, while effective multiscale crop models, especially those that also include remote sensing data, are indispensable to verify different strategies to obtain maximized crop yields.

Remembering Jan Amesz (1934-2001): a great gentleman, a major discoverer, and an internationally renowned biophysicist of both oxygenic and anoxygenic photosynthesisa.

We present here the research contributions of Jan Amesz (1934-2001) on deciphering the details of the early physico-chemical steps in oxygenic photosynthesis in plants, algae and cyanobacteria, as well as in anoxygenic photosynthesis in purple, green, and heliobacteria. His research included light absorption and the mechanism of excitation energy transfer, primary photochemistry, and electron transfer steps until the reduction of pyridine nucleotides. Among his many discoveries, we emphasize his 1961 proof, with L. N. M. Duysens, of the "series scheme" of oxygenic photosynthesis, through antagonistic effects of Light I and II on the redox state of cytochrome f. Further, we highlight the following research on oxygenic photosynthesis: the experimental direct proof that plastoquinone and plastocyanin function at their respective places in the Z-scheme. In addition, Amesz's major contributions were in unraveling the mechanism of excitation energy transfer and electron transport steps in anoxygenic photosynthetic bacteria (purple, green and heliobacteria). Before we present his research, focusing on his key discoveries, we provide a glimpse of his personal life. We end this Tribute with reminiscences from three of his former doctoral students (Sigi Neerken; Hjalmar Pernentier, and Frank Kleinherenbrink) and from several scientists (Suleyman Allakhverdiev; Robert Blankenship; Richard Cogdell) including two of the authors (G. Garab and A. Stirbet) of this Tribute.

Reduced expression of chlorophyllide a oxygenase (CAO) decreases the metabolic flux for chlorophyll synthesis and downregulates photosynthesis in tobacco plants.

Chlorophyll b is synthesized from chlorophyllide a, catalyzed by chlorophyllide a oxygenase (CAO). To examine whether reduced chlorophyll b content regulates chlorophyll (Chl) synthesis and photosynthesis, we raised CAO transgenic tobacco plants with antisense CAO expression, which had lower chlorophyll b content and, thus, higher Chl a/b ratio. Further, these plants had (i) lower chlorophyll b and total Chl content, whether they were grown under low or high light; (ii) decreased steady-state levels of chlorophyll biosynthetic intermediates, due, perhaps, to a feedback-controlled reduction in enzyme expressions/activities; (iii) reduced electron transport rates in their intact leaves, and reduced Photosystem (PS) I, PS II and whole chain electron transport activities in their isolated thylakoids; (iv) decreased carbon assimilation in plants grown under low or high light. We suggest that reduced synthesis of chlorophyll b by antisense expression of CAO, acting at the end of Chl biosynthesis pathway, downregulates the chlorophyll b biosynthesis, resulting in decreased Chl b, total chlorophylls and increased Chl a/b. We have previously shown that the controlled up-regulation of chlorophyll b biosynthesis and decreased Chl a/b ratio by over expression of CAO enhance the rates of electron transport and CO2 assimilation in tobacco. Conversely, our data, presented here, demonstrate that-antisense expression of CAO in tobacco, which decreases Chl b biosynthesis and increases Chl a/b ratio, leads to reduced photosynthetic electron transport and carbon assimilation rates, both under low and high light. We conclude that Chl b modulates photosynthesis; its controlled down regulation/ up regulation decreases/ increases light-harvesting, rates of electron transport, and carbon assimilation. Supplementary Information: The online version contains supplementary material available at 10.1007/s12298-023-01395-5.

On the Pelletier and Caventou (1817, 1818) papers on chlorophyll and beyond.

The first use of the word 'chlorophyll' (chlorophile or chlorophyle in the French original) appeared in two papers by Pierre-Joseph Pelletier and Joseph Bienaimé Caventou, pharmacists in Paris who isolated and studied the green pigment from plants. Here, we provide English translations of their 1818 note and the slightly longer 1817 paper. Historical context is provided including a timeline of key discoveries in chlorophyll chemistry pertaining to photosynthesis.

Addressing the long-standing limitations of double exponential and non-rectangular hyperbolic models in quantifying light-response of electron transport rates in different photosynthetic organisms under various conditions.

The models used to describe the light response of electron transport rate in photosynthesis play a crucial role in determining two key parameters i.e., the maximum electron transport rate (J max) and the saturation light intensity (I sat). However, not all models accurately fit J-I curves, and determine the values of J max and I sat. Here, three models, namely the double exponential (DE) model, the non-rectangular hyperbolic (NRH) model, and a mechanistic model developed by one of the coauthors (Z-P Ye) and his coworkers (referred to as the mechanistic model), were compared in terms of their ability to fit J-I curves and estimate J max and I sat. Here, we apply these three models to a series of previously collected Chl a fluorescence data from seven photosynthetic organisms, grown under different conditions. Our results show that the mechanistic model performed well in describing the J-I curves, regardless of whether photoinhibition/dynamic down-regulation of photosystem II (PSII) occurs. Moreover, both J max and I sat estimated by this model are in very good agreement with the measured data. On the contrary, although the DE model simulates quite well the J-I curve for the species studied, it significantly overestimates both the J max of Amaranthus hypochondriacus and the I sat of Microcystis aeruginosa grown under NH4 +-N supply. More importantly, the light intensity required to achieve the potential maximum of J (J s) estimated by this model exceeds the unexpected high value of 105 µmol photons m-2 s-1 for Triticum aestivum and A. hypochondriacus. The NRH model fails to characterize the J-I curves with dynamic down-regulation/photoinhibition for Abies alba, Oryza sativa and M. aeruginosa. In addition, this model also significantly overestimates the values of J max for T. aestivum at 21% O2 and A. hypochondriacus grown under normal condition, and significantly underestimates the values of J max for M. aeruginosa grown under NO3 -N supply. Our study provides evidence that the 'mechanistic model' is much more suitable than both the DE and NRH models in fitting the J-I curves and in estimating the photosynthetic parameters. This is a powerful tool for studying light harvesting properties and the dynamic down-regulation of PSII/photoinhibition.

Impact of individual, combined and sequential stress on photosynthesis machinery in rice (Oryza sativa L).

Abiotic stresses such as heat, drought and submergence are major threats to global food security. Despite simultaneous or sequential occurrence of these stresses being recurrent under field conditions, crop response to such stress combinations is poorly understood. Rice is a staple food crop for the majority of human beings. Exploitation of existing genetic diversity in rice for combined and/or sequential stress is a useful approach for developing climate-resilient cultivars. We phenotyped ~400 rice accessions under high temperature, drought, or submergence and their combinations. A cumulative performance index revealed Lomello as the best performer across stress and stress combinations at the seedling stage. Lomello showed a remarkable ability to maintain a higher quantum yield of photosystem (PS) II photochemistry. Moreover, the structural integrity of the photosystems, electron flow through both PSI and PSII and the ability to protect photosystems against photoinhibition were identified as the key traits of Lomello across the stress environments. A higher membrane stability and an increased amount of leaf chlorophyll under stress may be due to an efficient management of reactive oxygen species (ROS) at the cellular level. Further, an efficient electron flow through the photosystems and, thus, a higher photosynthetic rate in Lomello is expected to act as a sink for ROS by reducing the rate of electron transport to the high amount of molecular oxygen present in the chloroplast. However, further studies are needed to identify the molecular mechanism(s) involved in the stability of photosynthetic machinery and stress management in Lomello during stress conditions.

Evaluation of secondary sexual dimorphism of the dioecious Amaranthus palmeri under abiotic stress.

The evolution of secondary sex-specific traits of dioecious species under abiotic stress conditions has received limited research, especially in the case of Amaranthus palmeri, a fast adapting and highly competing plant. Here, we have examined the interactive effects of abiotic stress on mineral accumulation, chlorophyll a and b content, and the operating capacity of Photosystem II (PSII) in both male and female A. palmeri plants grown under three different intensities of white light, and under N, K or P deficiency. Mineral profiling of the leaves and stems (with inflorescence) highlighted intra- and intersexual differences in their accumulation pattern and mineral associations. Chlorophyll a and chlorophyll b were different between the male and the female plants, being slightly lower in the latter, at high light intensity towards maturity, or under K or P deficiency. Further, slight, although statistically significant differences were recorded in the chlorophyll a/b ratio, which was lower at the higher light intensity in the female, over that in the male, plants towards maturity. Chlorophyll fluorescence parameters, i.e., steady state and maximum fluorescence increased under high light intensity, whereas the PSII operating efficiency decreased in the female plants, indicating reduced PSII capacity. Sex-specific differences in A. palmeri showed a differential response to stressful conditions because of differences in their ontogeny and physiology, and possibly due to the cost of reproduction. We suggest that the breeding system of dioecious species has weaknesses that can be used for the ecological management of dioecious weeds without relying on the use of herbicides.

Paul A. Castelfranco (1921-2021): a scientist par excellence, a man of lasting faith, and ever a humanist.

We present here the life and the work of Paul A. Castelfranco (1921-2021), a very special person who was not only a top chemist of chlorophyll biosynthesis, but also made major contributions on fatty acid oxidation, acetate metabolism and cellular organization. He led an extraordinary and exemplary life as a human being. We present here both his personal life as well as his scientific life, which is followed by reminiscences by William Breidenbach, Kevin Smith, Alan Stemler, Ann Castelfranco, and John Castelfranco. As the subtitle of this Tribute implies, till the end Paul was a scientist par excellence, an intellectual with unlimited curiosity, a humanist, and a man of enduring religious faith. We all miss him dearly.

Determination of Fv /Fm from Chlorophyll a Fluorescence without Dark Adaptation by an LSSVM Model.

Evaluation of photosynthetic quantum yield is important for analyzing the phenotype of plants. Chlorophyll a fluorescence (ChlF) has been widely used to estimate plant photosynthesis and its regulatory mechanisms. The ratio of variable to maximum fluorescence, Fv /Fm , obtained from a ChlF induction curve, is commonly used to reflect the maximum photochemical quantum yield of photosystem II (PSII), but it is measured after a sample is dark-adapted for a long time, which limits its practical use. In this research, a least-squares support vector machine (LSSVM) model was developed to explore whether Fv /Fm can be determined from ChlF induction curves measured without dark adaptation. A total of 7,231 samples of 8 different experiments, under diverse conditions, were used to train the LSSVM model. Model evaluation with different samples showed excellent performance in determining Fv /Fm from ChlF signals without dark adaptation. Computation time for each test sample was less than 4 ms. Further, the prediction performance of test dataset was found to be very desirable: a high correlation coefficient (0.762 to 0.974); a low root mean squared error (0.005 to 0.021); and a residual prediction deviation of 1.254 to 4.933. These results clearly demonstrate that Fv /Fm , the widely used ChlF induction feature, can be determined from measurements without dark adaptation of samples. This will not only save experiment time but also make Fv /Fm useful in real-time and field applications. This work provides a high-throughput method to determine the important photosynthetic feature through ChlF for phenotyping plants.

Solar energy conversion by photosystem II: principles and structures.

Photosynthetic water oxidation by Photosystem II (PSII) is a fascinating process because it sustains life on Earth and serves as a blue print for scalable synthetic catalysts required for renewable energy applications. The biophysical, computational, and structural description of this process, which started more than 50 years ago, has made tremendous progress over the past two decades, with its high-resolution crystal structures being available not only of the dark-stable state of PSII, but of all the semi-stable reaction intermediates and even some transient states. Here, we summarize the current knowledge on PSII with emphasis on the basic principles that govern the conversion of light energy to chemical energy in PSII, as well as on the illustration of the molecular structures that enable these reactions. The important remaining questions regarding the mechanism of biological water oxidation are highlighted, and one possible pathway for this fundamental reaction is described at a molecular level.

David (Dave) Charles Fork (1929-2020): a gentle human being, a great experimenter, and a passionate researcher.

We provide here an overview of the remarkable life and outstanding research of David (Dave) Charles Fork (March 4, 1929-December 13, 2021) in oxygenic photosynthesis. In the words of the late Jack Edgar Myers, he was a top 'photosynthetiker'. His research dealt with novel findings on light absorption, excitation energy distribution, and redistribution among the two photosystems, electron transfer, and their relation to dynamic membrane change as affected by environmental changes, especially temperature. David was an attentive listener and a creative designer of experiments and instruments, and he was also great fun to work with. He is remembered here by his family, coworkers, and friends from around the world including Australia, France, Germany, Japan, Sweden, Israel, and USA.

In memory of Vladimir Anatolievich Shuvalov (1943-2022): an outstanding biophysicist.

We present here a tribute to one of the foremost biophysicists of our time, Vladimir Anatolievich Shuvalov, who made important contributions in bioenergetics, especially on the primary steps of conversion of light energy into charge-separated states in both anoxygenic and oxygenic photosynthesis. For this, he and his research team exploited pico- and femtosecond transient absorption spectroscopy, photodichroism & circular dichroism spectroscopy, light-induced FTIR (Fourier-transform infrared) spectroscopy, and hole-burning spectroscopy. We remember him for his outstanding leadership and for being a wonderful mentor to many scientists in this area. Reminiscences by many [Suleyman Allakhverdiev (Russia); Robert Blankenship (USA); Richard Cogdell (UK); Arvi Freiberg (Estonia); Govindjee Govindjee (USA); Alexander Krasnovsky, jr, (Russia); William Parson (USA); Andrei Razjivin (Russia); Jian- Ren Shen (Japan); Sergei Shuvalov (Russia); Lyudmilla Vasilieva (Russia); and Andrei Yakovlev (Russia)] have included not only his wonderful personal character, but his outstanding scientific research.

Overexpression of cytoplasmic C4 Flaveria bidentis carbonic anhydrase in C3 Arabidopsis thaliana increases amino acids, photosynthetic potential, and biomass.

An important method to improve photosynthesis in C3 crops, such as rice and wheat, is to transfer efficient C4 characters to them. Here, cytosolic carbonic anhydrase (CA: ßCA3) of the C4 Flaveria bidentis (Fb) was overexpressed under the control of 35 S promoter in Arabidopsis thaliana, a C3 plant, to enhance its photosynthetic efficiency. Overexpression of CA resulted in a better supply of the substrate HCO3- for the endogenous phosphoenolpyruvate carboxylase in the cytosol of the overexpressers, and increased its activity for generating malate that feeds into the tricarboxylic acid cycle. This provided additional carbon skeleton for increased synthesis of amino acids aspartate, asparagine, glutamate, and glutamine. Increased amino acids contributed to higher protein content in the transgenics. Furthermore, expression of FbßCA3 in Arabidopsis led to a better growth due to expression of several genes leading to higher chlorophyll content, electron transport, and photosynthetic carbon assimilation in the transformants. Enhanced CO2 assimilation resulted in increased sugar and starch content, and plant dry weight. In addition, transgenic plants had lower stomatal conductance, reduced transpiration rate, and higher water-use efficiency. These results, taken together, show that expression of C4 CA in the cytosol of a C3 plant can indeed improve its photosynthetic capacity with enhanced water-use efficiency.

Remembering Robert (Bob) Togasaki (1932-2019): A leader in Chlamydomonas genetics and in plant biology, as well as a teacher par excellence.

Robert (Bob) K. Togasaki was devoted to science and the people in the scientific community. He elucidated some of the most fundamental aspects of photosynthesis and carbon metabolism through classic genetic approaches and later using the tools of modern biotechnology. Along the way, he freely shared his ideas and enthusiasm with established scientists, junior researchers, graduate students, and even elementary students. His career trajectory led him to work with some of the leaders in the field, including the late Martin Gibbs and R. Paul Levine. His dedicated research has led to a more complete understanding of some of the core biochemical functions relating to photosynthesis of the green alga Chlamydomonas; this has included carbon-concentrating mechanisms, hydrogenases, and superoxide dismutase to name just a few. The focus of this Tribute is personal reminiscences by his postdoctoral advisor R. Paul Levine; his collaborators Teruo Ogawa, Jean-David Rochaix, Hidehiro Sakurai, Michael Seibert; and by his students William Belknap, Susan Carlson, Charlene Forest, Arthur Grossman, Gregory Katzman, Masahiko Kitayama, and Jon Suzuki. All remember Bob Togasaki for his intellect, dedication to science education, and his unwavering goodwill and optimism towards his fellow human beings.

Evaluating the Impact of Summer Drought on Vegetation Growth Using Space-Based Solar-Induced Chlorophyll Fluorescence Across Extensive Spatial Measures.

Drought is the primary and dominant natural cause of stress on vegetation, and thus, it needs our full attention. Current understanding of drought across extensive spatial measures, around the world, is considerably limited. As case studies to evaluate the feasibility of utilizing space-based solar-induced chlorophyll fluorescence (SIF) across extensive spatial measures, here, we have used data from 2007 to 2017 in Heilongjiang and Jiangsu provinces of China. The onset of the 2015 drought was accompanied by a substantial response of SIF from vegetation in both the provinces; these data were associated with changes in soil moisture, standardized precipitation evapotranspiration index, and emissivity. Our findings suggest that SIF can effectively provide the spatial and temporal progress of drought, as inferred through substantial associations with SIF normalized by absorbed photosynthetically active radiation (related to ΦF) and by photosynthetically active radiation (SIFpar). For the depiction of onset to drought, SIF, ΦF, and SIFpar provide a significant association and a quicker response than the leaf area index and the normalized difference vegetation index. Furthermore, we found that the correlation between gross primary productivity and SIF is highly substantial in both Heilongjiang (R2 = 0.85, p < 0.001) and Jiangsu (R2 = 0.75, p < 0.001) during the drought period. Our results indicate that continuing evaluation from space-based SIF can indeed provide an understanding of the seasonal differences in vegetation for evaluating the impact of drought across extensive spatial measures.

Plant lectins and their many roles: Carbohydrate-binding and beyond.

Lectins are ubiquitous proteins that reversibly bind to specific carbohydrates and, thus, serve as readers of the sugar code. In photosynthetic organisms, lectin family proteins play important roles in capturing and releasing photosynthates via an endogenous lectin cycle. Often, lectin proteins consist of one or more lectin domains in combination with other types of domains. This structural diversity of lectins is the basis for their current classification, which is consistent with their diverse functions in cell signaling associated with growth and development, as well as in the plant's response to biotic, symbiotic, and abiotic stimuli. Furthermore, the lectin family shows evolutionary expansion that has distinct clade-specific signatures. Although the function(s) of many plant lectin family genes are unknown, studies in the model plant Arabidopsis thaliana have provided insights into their diverse roles. Here, we have used a biocuration approach rooted in the critical review of scientific literature and information available in the public genomic databases to summarize the expression, localization, and known functions of lectins in Arabidopsis. A better understanding of the structure and function of lectins is expected to aid in improving agricultural productivity through the manipulation of candidate genes for breeding climate-resilient crops, or by regulating metabolic pathways by applications of plant growth regulators.

Regulation of Photosynthesis in Bloom-Forming Cyanobacteria with the Simplest ß-Diketone.

Selective inhibition of photosynthesis is a fundamental strategy to solve the global challenge caused by harmful cyanobacterial blooms. However, there is a lack of specificity of the currently used cyanocides, because most of them act on cyanobacteria by generating nontargeted oxidative stress. Here, for the first time, we find that the simplest ß-diketone, acetylacetone, is a promising specific cyanocide, which acts on Microcystis aeruginosa through targeted binding on bound iron species in the photosynthetic electron transport chain, rather than by oxidizing the components of the photosynthetic apparatus. The targeted binding approach outperforms the general oxidation mechanism in terms of specificity and eco-safety. Given the essential role of photosynthesis in both natural and artificial systems, this finding not only provides a unique solution for the selective control of cyanobacteria but also sheds new light on the ways to modulate photosynthesis.

Martin David Kamen (1913-2002): discoverer of carbon 14, and of new cytochromes in photosynthetic bacteria.

Martin Kamen was a giant of twentieth century science. Trained as a physical chemist, he was the co-discoverer of radioactive Carbon 14, which has transformed many areas of science as a tracer and as a way to date artifacts. He later switched to the study of metabolism and biochemistry and made important contributions to the understanding of nitrogen fixation and photosynthesis. Finally, he studied cytochromes, primarily from anoxygenic photosynthetic bacteria.