Fuelling life: recent advances in photosynthesis research

Abstract

Photosynthesis is the process by which light energy is converted to chemical energy and organic matter while releasing oxygen to the atmosphere. Consequently, photosynthesis fuels the entire planet. With the current demands to feed a growing population, to find alternatives to fossil fuels, and to increase the strengths of both terrestrial and oceanic carbon sinks, manipulations of photosynthetic mechanisms have never been more topical. However, photosynthetic carbon assimilation is complex and relies on diffusion of CO2 from the atmosphere to the site of fixation, appropriate light absorption and conversion to energy, and efficient conversion of CO2 into organic molecules. This Special Issue collects a series of reviews that cover all of these different aspects of photosynthesis. CO2, as the substrate for photosynthetic assimilation (A), must diffuse from the atmosphere through the stomatal pore to the substomatal cavity. Stomata hence provide the initial controlling point for gaseous flux, as these pores adjust aperture in response to a number of environmental factors and internal cues in order to balance CO2 uptake for photosynthesis with water loss through transpiration. Therefore, stomatal behaviour is pivotal in carbon assimilation, plant water status, maintenance of leaf temperature, and plant water-use efficiency. In the first article of this Special Issue, Brodribb et al. (2020) outline stomatal behaviour and the selective pressure that drove stomatal evolution and discuss this in the context of improving photosynthetic water use. The authors describe the progression from passive stomatal behaviour in early land plants to active mechanisms, as well as outlining the primary regulators of stomatal aperture. Within this context, Brodribb et al. (2020) consider the adaptive processes that have coupled the regulation of plant water and carbon fluxes in vascular plants. They demonstrate this via the evolution of proteins involved in guard cell osmoregulation, including the presence and absence of key proteins involved in stomatal regulations as well as functional differences in different phyla. The second article in this Special Issue (Harrison et al., 2020) highlights the contribution of stomatal density, size, and distribution to overall stomatal conductance and the impact on photosynthesis. The relationship between maximum stomatal conductance, determined by anatomical features, and A is explored alongside the manipulation of a number of morphological traits to maximize CO2 uptake for photosynthesis. Alterations in stomatal aperture are brought about by changes in turgor pressure and guard cells that make up the stomatal pore must overcome the backpressure of the subsidiary cells surrounding them in order to open, and this is the focus of the next article in the series. Nunes et al. (2020) explore a genetic and mechanistic perspective on the unique anatomy of graminoid lateral subsidiary cells, which are thought to be involved in faster stomatal responses observed in the Poaceae. In the review the authors provide an extremely valuable list of the key players in stomatal development and function and discuss the potential to use this information for improving water stress resilience in agriculturally relevant plants. The diffusion of CO2 continues from the substomatal cavity to the sites of carboxylation inside chloroplast stroma through a complex pathway including intercellular air spaces, cell wall, plasmalemma, cytoplasm, chloroplast envelope, and the chloroplast stroma before being fixed by RuBisCO. The conductance through this complex pathway is often termed mesophyll conductance (gm) and is the focus of several articles in this Special Issue. For all terrestrial plants, including C3, C4 and crassulacean acid metabolism (CAM), photosynthetic performance depends greatly on plant water status. In order to function optimally, plants are faced with the challenge of maximizing CO2 uptake while minimizing water loss. The review by Xiong and Nadal (2020) explores the link between photosynthesis and water relations. Specifically these authors focus on the relationship between the hydraulic capacity of the leaf, gm and A, particularly in a dynamic environment. They review recent studies that indicate that water transport and CO2 movement inside the leaf share a common pathway and that this co-ordination impacts on carbon assimilation. Within this context, the influence of leaf capacitance and the bulk modulus of elasticity (ε; defined as a change in turgor pressure per volume decrease) is evaluated and the role of ε on diffusion, gm and photosynthetic performance is examined. In the final sections, the authors provide insights into current opportunities for further research in this area. In the next review, Cousins et al. (2020) discuss the processes involved in mesophyll conductance. While gm has been the subject of several reviews in the past, only recently have methodological developments allowed proper estimations of this parameter in C4 species. Hence, this is the first review specifically comparing gm in C3, C4, and CAM species. In addition, Cousins et al. (2020) highlight the recent advances in moving from a classical 1-D or 2-D perspective to more realistic – yet more difficult to parameterize – 3-D models for gm. They discuss several mechanisms involved in the regulation of gm, including carbonic anhydrases (CAs). The latter are the focus of next review by Momayyezi et al. (2020). In their review, the authors explain what is known about the major isoforms and families of CAs, highlighting how reaction-diffusion models and empirical data provide evidence for their involvement in the regulation of gm. They also review the involvement of CAs in other processes related to photosynthesis, including some mechanisms for stomata regulation. Besides CAs, gm is known to strongly depend on additional anatomical and biochemical features of the leaves. In this context, Lundgren and Fleming (2020) review the possibility of modifying gm by manipulating some of these characteristics. On the biochemical side they provide an updated review of the possible role of aquaporins in gm, as well as a novel insight into the possible role of cell wall composition. The core of their review focuses on anatomical traits, and a perspective is provided as to how gm could be improved by modifying genes to lead to altered leaf internal anatomy, for example changing the distribution of intercellular air spaces, mesophyll cells size, and division rates. All these reviews highlight the now recognized key importance of gm in regulating photosynthesis rates. However, when scaling-up from leaf level to land surface level, most current models include a module for photosynthesis parameterization that neglects gm. Knauer et al. (2020) review approaches to account for gm explicitly in land surface models and show that neglecting gm results in a significant underestimation of the responses of gross primary productivity and transpiration to environmental variables, especially to CO2 and temperature, for which these findings may have crucial implications for modelling ecosystem responses to ongoing climate change. Light in excess of that used for photosynthesis can result in damage to the photosystems and reduce productivity, but under-saturating light also limits photosynthesis. Wang et al. (2020) focus on the fact that photosynthesis often occurs under fluctuating light, and that transitions from low to high light require induction times whose shortening can open significant opportunities for improving photosynthesis in natural environments. Conversely, the article by Murchie and Ruban (2020) explores dynamic non-photochemical processes and highlights that major photoprotective mechanisms, including non-photochemical quenching (NPQ), determine whole canopy photosynthesis and ultimately biomass and yield. The authors argue that this phenomenon is not well characterized or quantified, due mostly to the different methods used. The article reviews our understanding of the different approaches from the molecular mechanisms of NPQ to its regulation in dynamic environments and how fine tuning of these can contribute to improving dynamic NPQ and yield in key crop species. Once CO2 has diffused from the atmosphere to the chloroplast stroma and light has been converted into chemical energy, CO2 is fixed into carbohydrates. The photosynthetic reactions involved in the process are multiple and interconnected, but in C3 plants the initial step is carboxylation by RuBisCO. Iñiguez et al. (2020) review current knowledge on RuBisCO kinetic properties, with a special focus on how these change with phylogeny. In their paper, they use an extended database to provide new insights in the diversity of possible relationships among the catalytic traits of RuBisCO and how these catalytic traits have co-evolved with the appearance of carbon-concentrating mechanisms along the evolutionary history of photosynthetic organisms. A major inefficiency of RuBisCO is caused by its oxygenase activity, which is the initial step of the so-called photorespiratory pathway that leads to energy consumption and CO2 losses. Busch (2020) presents an original perspective on the meaning of this process, highlighting the distinction between RuBisCO oxygenation and photorespiratory CO2 release and reviewing the interactions between photorespiration and mesophyll conductance, nitrogen metabolism, and C1 metabolism, among others. In light of its multiple functions, photorespiration might not be a wasteful process. Nevertheless, C4 photosynthesis is an efficient CO2 concentration mechanism, whose main function is to minimize photorespiration. Ermakova et al. (2020) provide an update review on the work of the international C4 rice consortium, which aims to introduce the C4 pathway into rice to improve yield. They describe the components required and the new molecular tools available that have substantially speeded up the process. The authors explain the progress made in the important step of bundle sheath functionalization and the need for a greater understanding of the energetic requirement of C4 photosynthesis, including the higher ATP requirement. Ermakova et al. (2020) explain that high vein density is required for efficient C4 rice, however the authors’ model shows that small increases in C4 photosynthesis around existing veins could be sufficient to improve productivity. In the next review, Chomthong and Griffiths (2020) focus on the other major carbon-concentrating photosynthetic metabolism, that is the CAM. In their review, they provide a novel perspective illustrating how integrating molecular and empirical approaches through modelling have speeded our current understanding of CAM. Among several aspects, they attempt to identify the internal and environmental signals leading to the distinctive stomatal aperture by night and closure during the day that CAM plants exhibit. Most of the findings in the reviews to this point are based on empirical evidence obtained when working with leaves of selected plant species, notably angiosperms. Flexas and Carriqui (2020) review the expansion of knowledge towards other phylogenetic groups and present a comparative analysis of photosynthetic limitations and photosynthetic water-use – and nitrogen-use – efficiency across the land plant phylogeny. They show an increasing tendency of maximum photosynthetic rates and efficiencies from bryophytes to angiosperms that is largely explained by anatomically-driven amelioration of mesophyll conductance limitations to photosynthesis. Many non-vascular – but also some specially adapted vascular – plants inhabit some of the most inhospitable environments. The molecular and physiological mechanisms that drive photosynthesis in vascular species from extreme environments still remain largely unknown. Fernández-Marín et al. (2020) review the adaptations that enable these plants to succeed under their typical habitats characterized by short and harsh growing seasons. Altogether, these species display not a unique ‘solution’, but rather a highly diverse and co-ordinated combination of different strategies from the whole plant level to the molecular scale, enabling them to sustain a positive carbon balance in some of the most hostile environments on Earth. Conversely, in most plant species, leaves are not the only photosynthetic organs. In the last article Simkin et al. (2020) explain that photosynthesis in non-leaf tissues has generally been neglected as a potential target to increase crop photosynthesis. Significant levels of carbon assimilation have been demonstrated in a range of non-leaf green material and this could provide a substantial contribution to yield in some species, particularly under stressful conditions. The review also examines the role of stomata in these non-foliar tissues and their importance in gaseous exchange, maintenance of appropriate tissue temperature, and thus photosynthetic carbon gain. The authors conclude with a discussion on the possibility to manipulate the photosynthetic and stomatal component of these tissues and the potential to use these unexploited novel traits for breeding programmes with the aim to increase yield. As a collection, the Special Issue addresses novel aspects of knowledge on photosynthesis. Compared with classic compilations about this subject, this Special Issue extends the scope of topics covered: spanning from molecular to whole plant perspectives, scaling from subcellular to land surface levels, broadening the perspective on how photosynthesis components change along the land’s plant phylogeny, and covering non-usual aspects such as the interconnection between hydraulics and mesophyll conductance, photosynthesis in extreme environments and non-foliar photosynthesis. We believe it provides a wide and updated perspective on a subject of crucial importance for life on Earth.

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