Recent advances in understanding photosynthesis

Introduction

Photosynthesis is a process that all life on earth depends on. Photosynthetic organisms convert more than 10⁹ metric tons of atmospheric CO₂ into biomass per year. With the global human population rising from ~7 billion now to 9–10 billion by 2050, the worldwide trend towards a more meat-rich human diet, the loss of harvest and grazing land, and the negative effects of global warming on crop production have put forward the question of whether this incredibly high amount of biomass production can be further increased.

Crop yield is determined by the available solar irradiation energy across the growing season (0.487 S_t), the genetically encoded properties of how the radiation is intercepted (ε_i), the efficiency by which the light energy is converted into biomass (ε_c), and what fraction of the total biomass is partitioned into the harvestable part of the plant (harvest index, ε_p). This results in the Monteith equation: yield = 0.487 • S_t • ε_i• ε_c• ε_p^1–3.

The Green Revolution raised the yield potential of the major grain crops mainly by increasing the harvest index, which is now about 0.6. Breeders were also able to improve the light interception efficiency, which in modern cultivars is up to about 0.8–0.9. All available evidence suggests that additional grain yields by further increasing the harvest index or optimizing light interception are rather unlikely; they appear to be close to their biological limits already. In contrast, the best light conversion efficiency (ε_c) observed in field experiments (0.24 in C₃- and 0.37 in C₄-crops) is far below the theoretical maxima (0.46 in C₃- and 0.6 in C₄-plants) and thus not yet close to its biological limit. Enhancing, and in the long term re-designing, photosynthesis with respect to light energy conversion efficiency is therefore a prime target when aiming to increase crop yield^3–6.

In general, photosynthesis can be described as a cellular trait that uses light energy to convert atmospheric CO₂ into carbohydrates. At a higher level, photosynthesis is determined by the activity of leaves and by the canopy structure. And, finally, photosynthesis is related to the capacities of source and sink tissues, i.e. mature leaves and heterotrophic organs, respectively (Figure 1).

Figure 1. The process of photosynthesis viewed from different perspectives.

Here, we will discuss the process of photosynthesis from these various perspectives and address putative targets for the improvement of photosynthetic performance.

Photosynthesis as a cellular trait: (1) light-dependent reactions

Photosynthesis as a cellular trait: (2) assimilation reactions

During photosynthesis, plants capture energy from sunlight and turn it into biochemical energy in the form of ATP and reducing equivalents, NADPH. In C₃-plants, the first product of the CO₂-fixing ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO), the C₃-compound 3-phosphoglycerate, is transformed to a C₃-sugar (triose phosphate) as part of the Calvin-Benson cycle using both ATP and NADPH as products of the light reaction. In most plants, triose phosphates are subsequently converted into sucrose as the main photoassimilate exported from photosynthetically active leaves (the source tissue). The long-distance transport of photosynthates to heterotrophic organs (the sink tissue) serves to supply these organs with carbon and energy. In harvestable organs, carbon can be stored as, e.g., sucrose, starch, oil, or, in combination with nitrogen, protein.

In C₃-plants, the category to which most of our crop plants belong to, RuBisCO is CO₂ limited and works, at best, at half of its maximal reaction velocity⁴⁰. The oxygenase activity of RuBisCO initiates the wasteful process of photorespiration that finally results in the release of previously photoassimilated CO₂ and ammonia⁴¹. Multiple efforts have been or are still being undertaken to improve RuBisCO activity either directly⁴², albeit with very limited success so far⁶, or by targeting auxiliary proteins, for instance RuBisCO activase⁴³. Alternatively, by introducing CO₂ pumping devices into C₃-species, the limitations of RuBisCO are expected to be reduced. These CO₂ pumps are to operate via either a C₄ cycle⁴⁴ or inorganic carbon-concentrating devices of cyanobacterial origin⁴⁵. There were also attempts to reduce photorespiratory losses by introducing alternative salvage pathways^46,47. In addition, promising approaches have also been initiated to overcome bottlenecks in the Calvin-Benson cycle^48,49.

Photosynthesis: leaves as target for photosynthesis improvement

Leaves are the plant’s organs that are dedicated to photosynthesis. Under high-light conditions, e.g. at midday, plants receive excess energy that they are not able to cope with. It was proposed earlier that photosynthetic efficiency could be maximized by improving the plants’ canopy light distribution in a way that minimizes light saturation of the upper leaves and light starvation of the lower leaves⁶. This could be achieved by (i) varying the angle of the leaves in the canopy, (ii) altering the size of LHCs per photosystem, i.e. fewer LHCs in the upper leaves and larger LHCs in lower leaves, and/or (iii) extending the light absorption spectrum of photosynthetic pigments into the near-infrared region in the lower leaves in order to use this light quality more efficiently^6,50,51.

The leaves of the angiosperms vary greatly in size and shape, from single and entire to highly complex compound leaves⁵². However, the role and importance of leaf anatomy in contributing to the photosynthetic output of leaves is largely unexplored. It was suggested earlier that both leaf shape and leaf anatomy contribute to the photosynthetic output of leaves⁵³ and are therefore promising targets for improving photosynthesis⁵⁴. Genetic studies with rice support this notion by demonstrating that in rice the anatomy of leaves is closely associated with leaf photosynthesis^55,56 and, moreover, with crop yield^57,58. Unfortunately, global genetic analyses, preferably with easily accessible genetic model plants, which aim to identify genes affecting the inner anatomy of leaves and concomitantly their photosynthetic output, are still missing.

One approach to tackle this issue would be to compare leaf form and anatomy in established model systems, e.g. A. thaliana and Cardamine hirsuta, which both belong to the Brassicaceae. In contrast to A. thaliana, C. hirsuta has complex leaves subdivided into leaflets. Major steps in understanding the genetic basis for variation in leaf shape both within and between species have already been made^59–63. Both species have been documented to be suitable for an easy identification of genes and their functions. In both species, genes could be identified that affect primarily leaf form and/or the structure and organization of palisade and spongy parenchyma tissues of the leaf. A second step would be to investigate how and to which degree these genes can be used to optimize the photosynthetic output of leaves. The forward genetic approaches could rely on either mutagenesis or the available natural genetic diversity. Both photosynthesis and leaf differentiation are rather conserved in evolution, at least among the angiosperms. The transfer of knowledge from these model systems to the major crop species of this plant family, namely the Brassicas, should therefore be relatively straightforward.

Photosynthesis and the interaction with source-sink metabolism

Photosynthesis is part of a superordinate system, namely the whole plant. From the system’s perspective, the production of goods and their utilization have to be coupled, i.e. previous to the storage of products derived from photosynthetic assimilation processes in sink tissues (i.e. in harvestable organs), and carbon and nitrogen have to be assimilated in the source tissue (i.e. in mature leaves). To increase biomass production, strengthening the capacities of both source and sink tissues have been aimed at, although with varying success^64–71. Molecular targets were mainly related to genes involved in sugar and starch metabolism. A promising approach was recently suggested comprising the simultaneous boosting of both source and sink capacities using the crop plant potato as an example⁷². Here, the moderate repression of the leaf ADP-glucose pyrophosphorylase, a key enzyme of transitory starch formation or, alternatively, the mesophyll-specific expression of a bacterial pyrophosphate to stimulate sucrose synthesis and to prevent sucrose breakdown were combined with plants that had an increased sink strength. An increase in sink strength was accomplished by tuber-specific overexpression of two plastidic transporters responsible for the import of carbon (glucose 6-phosphate⁷³) and energy (ATP⁷⁴), respectively, into starch-storing amyloplasts. Both procedures resulted in an enhanced allocation of sucrose from source to sink tissues at the expense of leaf starch accumulation. The combined push-pull approach resulted in doubling the tuber starch yield⁷². This way of proceeding is currently being transferred to cassava, an important staple food in developing countries (Bill & Melinda Gates Foundation, CASS, OPP1113365).

It remains to be elucidated whether or not the push-pull approach can be combined with recent knowledge on novel photosynthetic components, e.g. by novel combinations of photosystem cores and LHC antenna complexes or by modifying light harvesting and regulators of photosynthetic electron flow to improve photosynthetic efficiency (Table 1). In addition, the push-pull strategy could potentially be teamed up with approaches to alter leaf form and/or anatomy to further improve ε_c, i.e. photosynthetic performance and biomass production.