Understanding and Improving Crop Photosynthesis. Volume 130 in Burleigh Dodds Series in Agricultural Science

A leading challenge for humanity in the new millennium will be to boost crop productivity to feed a global population approaching 9 billion people, and to do so with finite amounts of land, fertilizing nutrients and water. Moreover, the resource inputs supporting agricultural productivity are declining because of impacts of climate change, soil erosion and urbanization, whereas the demand for crop products is growing with the advent of novel bio-economies and next-generation biofuels. A major means to improve agricultural output is to increase the energy and carbon foundation upon which all plant productivity is based by improving photosynthesis. As Monteith and colleagues showed five decades ago (Monteith and Moss, 1977), improved photosynthesis enhances two key determinants of crop yield: light interception efficiency and the efficiency of converting light energy into biomass. The use of the C₄ photosynthetic pathway, for example, improves light interception efficiency relative to C₃ species while also increasing conversion efficiency by reducing photorespiratory losses (Zhu et al., 2010). With the realization that enhancement of photosynthesis is an effective strategy to address the challenges of population growth, global change and limited land and resources, research funding for photosynthetic improvement has been healthy in the new millennium. This funding has expanded to include non-governmental support for international consortia, such as the RIPE program (Realizing Increased Photosynthetic Efficiency; https://ripe.illinois.edu/), which aims to improve C₃ photosynthetic performance through actions such as improving Rubisco and light-harvesting efficiency, and the C₄ Rice Project (https://C4rice.com), which aspires to engineer the C₄ photosynthetic pathway into rice.

Over the decades, photosynthesis research has been one of the more active areas in plant biology and has produced a rich body of research that is challenging in its depth and complexity for newcomers and seasoned experts alike. To appreciate strategies for improving photosynthesis, understanding this body of basic research is essential yet can be tough for newcomers and the broader audience because it tends to be published in highly specialized articles written for the advanced expert. In this light, the new volume edited by Robert Sharwood, entitled Understanding and Improving Crop Photosynthesis, is a particularly timely addition to the photosynthesis literature. The volume stands out for its principal focus on photosynthetic improvement, yet supports this focus by providing essential basic background that allows readers to understand and appreciate the most promising strategies for enhancing photosynthetic productivity in C₃ crops.

Understanding and Improving Crop Photosynthesis consists of ten chapters by established leaders and rising stars in the field of photosynthesis. Dr Sharwood is one of Australia’s leading young photosynthetic biologists, known for his research on Rubisco function and improvement. His preface opens the book with an informative overview that highlights the contributions of each chapter. The book is divided into three parts: (1) general issues; (2) light harvesting; and (3) optimizing chloroplast function and light conversion. Chapter 1, by Christine Raines and colleagues, presents an overview of photosynthesis in C₃ plants, emphasizing the limitations on carbon gain owing to chloroplast biochemistry and potential mechanisms to overcome these limitations. The chapter sets the pattern present in most chapters, whereby a thorough introduction to the topic is presented initially, after which the focus turns to mechanisms for improvement. Raines et al. initially discuss the steps limiting carbon metabolism, followed by considerations of metabolic modelling that are key to identifying targets for molecular engineering. One strong insight provided by the chapter is a synopsis of future challenges, specifically noting that improvements are needed in understanding: (1) the natural diversity of most components making up the photosynthetic apparatus; (2) the regulatory controls over individual gene expression; and (3) metabolic profiling of flux pathways.

Given the need for a better understanding of gene regulation, it is fitting that P. Carvalho, Elias da Silva and N. J. M. Saibo follow in Chapter 2 with a review of the genetics of C₃ photosynthesis. In their chapter, they present select examples describing how some of the ~3000 proteins used in photosynthesis could be manipulated through genetic engineering. As the authors note, improving photosynthesis is not simply a matter of improving metabolic pathways or light-harvesting efficiency, but requires manipulation of proteins that contribute to the structure of chloroplasts, peroxisomes and mitochondria, and the trafficking of proteins and metabolites between each compartment within the cell. A particular strength of the chapter is its discussion of gene regulators, whose manipulation will be key to eventual outcomes; however, the authors emphasize that the basic understanding of transcriptional regulation is sparse for most photosynthetic genes, and thus a substantial amount of basic research is needed to establish a platform that enables longer-term engineering goals.

Chapter 3, by Marina Quirroz, Martin Battle and Matthew Jones, begins the second section of the book with a review of interactions between photosynthesis and the circadian regulatory system. Although often overlooked, circadian control of photosynthetic gene expression is essential for effective coordination of plant metabolism with the environment, and thus the circadian regulators sit at the beginning of many signal-transduction pathways in plants. Understanding these pathways will help to identify targets for manipulating regulatory control over gene expression. Min Chen and Robert Blankenship follow with chapter 4, in which they discuss strategies to improve light-harvesting antennae in plants. The chapter provides a strong introduction to key issues in light harvesting, noting factors that contribute to inefficiency, damaging photoinhibition and, finally, mechanisms for improving efficiency. The authors note that optimizing pigment composition and photoprotection are two promising options for enhancing light interception efficiency. Research into understanding of photosynthetic light harvesting has been one of the pillars of the photosynthetic community for decades, in part because artificial photosynthesis might one day serve to generate hydrogen-based fuels (Gust et al., 2009). Chen and Blankenship briefly review advances from this research, but its brevity limits the depth the authors are able to develop.

Johannes Kromdijk follows in Chapter 5 with an examination of the dynamic mechanisms governing photoprotection in thylakoids, which are critical for avoiding high-light damage but can potentially reduce light-harvesting and photosynthetic efficiency by quenching too much light. As Kromdijk explains, an intriguing means of improving photosynthesis is to match photoprotection better with the light environment by enabling rapid induction of photoprotective light quenching when the light intensity suddenly increases and accelerating reduction of photoprotection when the light intensity drops. Rapid activation and deactivation of photoprotection will be particularly useful in the fluctuating light environments present in most crop canopies. The thorough introduction provided by Kromdijk allows readers to appreciate the logic and challenges of photoprotective manipulation.

In a related Chapter (Chapter 7), Anthony Digrado and Lisa Ainsworth review ways to improve canopy architecture, which, via plant breeding, has been one of the most successful strategies for enhancing light interception and conversion efficiency over the growing season. Canopy architecture determines the light distribution within canopies and is a critical controller of radiation use efficiency (the biomass produced per incident light). Failure to achieve optimal design of the crop canopy reduces radiation use efficiency and thus yield. For example, canopy underinvestment can reduce light interception, whereas overinvestment wastes resources because too much leaf area causes excessive self-shading while consuming nitrogen reserves. The authors first explain the significance of canopy architecture and its influence over light interception, after which they address breeding improvements in canopy display. The second half of the chapter addresses manipulation of leaf distribution, number, shape and angle as strategies for improving canopy photosynthesis. In addition, the chapter addresses energy balance, nitrogen allocation within the canopy and water use to provide a more holistic understanding of canopy dynamics.

The final section of the book emphasizes carbon fixation and utilization reactions, which directly influence energy-conversion efficiency and represent the greatest possibilities for photosynthetic improvement. The section lists three chapters but should really include a fourth, which is Chapter 6, an assessment of modifying mesophyll conductance by Coralie Salesse-Smith, Steven Driever and Victoria Clarke, which seems out of place in the light-harvesting section. Mesophyll conductance (g_m) refers to the series of conductances in the transport pathway for CO₂ from the intercellular air spaces to the site of carboxylation in the chloroplast stroma. Understanding g_m has been one of the more active research areas on the carbon-fixation side of photosynthesis for the past 25 years, because it was realized that g_m limitation can rival that imposed by stomata. Selesse-Smith et al. present a nice overview of g_m limitations, including use of an illustrative diagram of the CO₂ journey inside a leaf that would be suitable for upper-level classrooms. This is followed by a description of the relative importance of each part of the conductance pathway, wherein we are informed that membranes account for ≤50 % of the resistance in the g_m pathway. This discussion nicely sets up an assessment of mechanisms to enhance g_m and why stacking multiple mechanisms allows for the greatest improvement. However, the chapter does not address the costs of high mesophyll conductance, which becomes important if elevated CO₂ reduces the relative benefits of high g_m (Mizokami et al., 2022).

Chapter 8, by Xinyu Fu et al. from the laboratory of Berkeley Walker at Michigan State University, presents a discussion of strategies to offset the costs of photorespiration. Photorespiration is an inevitable limitation on carbon gain owing to the propensity of Rubisco to oxygenate RuBP rather than to carboxylate it in the relatively low-CO₂ atmospheres of recent geological time. The chapter provides a nice overview of photorespiration and mechanisms for reducing its inhibition of carbon gain in C₃ plants, although it does not address improvements from Rubisco engineering or the introduction of carbon-concentrating mechanisms into C₃ plants. Improvement strategies emphasized are: (1) to maintain high flux potential through the photorespiratory pathway to prevent feedbacks that can slow photosynthesis; and (2) the use of photorespiratory bypasses. The advantage of bypass metabolism is that photorespiratory CO₂ is released in the chloroplast rather than mitochondria, allowing for rapid refixation by Rubisco before CO₂ escapes the cell.

As atmospheric CO₂ increases, photosynthesis in the C₃ flora will increasingly shift from a world where carboxylation capacity is limiting to one where RuBP regeneration capacity increasingly limits carbon gain. Limitations to RuBP regeneration include turnover of the Calvin cycle, regeneration of inorganic phosphate by starch and sucrose synthesis, and light harvesting and transduction into ATP and NADPH. In an illuminating chapter, Tom Sharkey explains the details of RuBP regeneration limitations. The chapter emphasizes an optimality approach, using photosynthetic theory to explain how the leading components of the photosynthetic apparatus can equally limit carbon gain, reflecting an optimal investment strategy, and how conditions that disrupt optimal investment patterns lead to single limitations. A nice touch is that the chapter explains the consequences of single limitations on photosynthetic efficiency; for example, disruptions of linkages between carbon metabolism and electron transport can lead to excessive non-photochemical quenching and greater potential for photoinhibition.

The book closes with Chapter 10, by James Moroney and colleagues, addressing strategies to improve carbon gain by introducing algal-type CO₂-concentrating mechanisms into terrestrial C₃ plants. Three great CO₂-concentrating mechanisms of photosynthesis are known: C₄ photosynthesis, CAM photosynthesis and inorganic carbon concentration in algae. In algae, dissolved inorganic carbon in the form of CO₂, bicarbonate or carbonate is actively pumped from surrounding water into pyrenoids or carboxysomes and concentrated around Rubisco, enhancing enzyme carboxylation efficiency. The book does not address efforts to improve photosynthesis by engineering C₄ or CAM photosynthesis into C₃ plants, which seems a bit of an oversight given that these objectives have been the focus of multimillion dollar research efforts over the past decade. However, this deficiency is made up for by the insightful review of Moroney et al., which addresses the advantages of the algal CO₂-concentrating mechanisms and the potential challenges to engineering the key steps into terrestrial C₃ plants. In addition to a clear and logical overview of the leading strategies, the authors discuss the technical challenges, and in doing so, provide additional insights into the function of the various algal-type mechanisms for enhancing photosynthesis. This further highlights the importance of learning from natural diversity to find transformative means to enhance crop yield.

Understanding and Improving Crop Photosynthesis is the 130^th volume in the Burleigh Dodds series in Agricultural Science. The series typically emphasizes applied topics in sustainable crop production and management, such as volume 20, Achieving Sustainable Cultivation of Cassava, and volume 115, Energy-smart Climate Farming. Volume 130 represents one of the cross-over texts in the series, where instead of emphasizing cultivation strategies, the chapters present a substantial amount of basic science to explain improvement strategies, which are now being investigated at the molecular level but, in most cases, are not yet introduced into field crops. I imagine that a follow-up volume in a decade or two will describe field outcomes of the many promising developments reviewed in the present text. The chapters in Understanding and Improving Crop Photosynthesis follow well the Burleigh Dodd’s model of providing a rich assortment of references, particularly recent references representing the state of the art for each subject. The chapters also close by highlighting key reviews and websites where readers can seek additional updates and information. These additional resources bridge the gap between the advanced topics discussed in each chapter and general introductions, such as found in a textbook. By providing this information, the chapters in Understanding and Improving Crop Photosynthesis will assist readers wishing to build a better understanding of photosynthesis and its manipulation. The book will be appreciated by a wide range of scholars, from advanced undergraduates to established experts looking to keep abreast of developments in the field.

LITERATURE CITED