Perspectives on improving photosynthesis to increase crop yield

Abstract

Improving photosynthesis, the fundamental process by which plants convert light energy into chemical energy, is a key area of research with great potential for enhancing sustainable agricultural productivity and addressing global food security challenges. This perspective delves into the latest advancements and approaches aimed at optimizing photosynthetic efficiency. Our discussion encompasses the entire process, beginning with light harvesting and its regulation and progressing through the bottleneck of electron transfer. We then delve into the carbon reactions of photosynthesis, focusing on strategies targeting the enzymes of the Calvin-Benson-Bassham (CBB) cycle. Additionally, we explore methods to increase carbon dioxide (CO2) concentration near the Rubisco, the enzyme responsible for the first step of CBB cycle, drawing inspiration from various photosynthetic organisms, and conclude this section by examining ways to enhance CO2 delivery into leaves. Moving beyond individual processes, we discuss two approaches to identifying key targets for photosynthesis improvement: systems modeling and the study of natural variation. Finally, we revisit some of the strategies mentioned above to provide a holistic view of the improvements, analyzing their impact on nitrogen use efficiency and on canopy photosynthesis.

Figure 1.

Solar spectrum on the top (yellow) and bottom (brown) of a crop canopy (adapted from Mirkovic et al. 2017). The absorption spectra of three cyanobacteria containing Chl a (black), Chl a and Chl f (red), and Chl d (blue) are also shown.

Figure 2.

Phenotypes of the hus1 mutant and control plants grown under field conditions at Azienda Agraria Sperimentale, Stuard (Parma, Italy). A) The hus1 mutant and the control Sebastian variety at the tillering stage. B)hus1 plants at the heading stage. Courtesy of Lorenzo Genesio (National Research Council, Rome, Italy).

Figure 3.

Engineering NPQ kinetics via VDE, PsbS, and ZEP overexpression. A) Schematic describing the relationships between VDE, PsbS, and ZEP in inducing and relaxing qE and qZ via the interconversion of zeaxanthin (Zea) and violaxanthin (Vio). B) Table summarizing differences in published VPZ phenotypes in tobacco (Kromdijk et al. 2016), soybean (De Souza et al. 2022), Arabidopsis (Garcia-Molina and Leister 2020), and potato (Lehretz et al. 2022), based on fluctuating light and field/growth chamber measurements. Triangles describe the directionality of the phenotype relative to wild type (WT). Green triangles indicate hypothesized beneficial photosynthetic efficiency phenotypes, maroon triangles indicate potentially deleterious phenotypes, and yellow lines describe neutral phenotypes. One asterisk (*) indicates NPQ phenotypes assessed at fluctuations of 500/50 µmol photons m⁻² s⁻¹ rather than 2,000/200 µmol photons m⁻² s⁻¹. Two asterisks (**) indicate phenotypes reported by Küster et al. (2023). Gray box indicates data not collected in its respective study.

Figure 4.

Increasing abundance of Cyt b₆f to accelerate electron transport and enhance the rate of C₃ and C₄ photosynthesis: models’ predictions and results from plants overexpressing Rieske FeS subunit of Cyt b₆f (Rieske-OE). Models’ predictions schematically depict simulations obtained with the C₃ photosynthesis model of Farquhar et al. (1980) and C₄ photosynthesis model of von Caemmerer and Furbank (1999). Schematic representations of Rieske-OE results are based on studies conducted in model C₃ plant A. thaliana (Simkin et al. 2017b), model C₄ plant S. viridis (Ermakova et al. 2019), model C₃ crop N. tabacum Petit Havana (Heyno et al. 2022), and model C₄ crop S. bicolor Tx430 (Ermakova et al. 2023). In model plants, in line with the models’ predictions, Rieske-OE stimulates steady-state electron transport, which results in increased CO₂ assimilation rates at high light and nonlimiting CO₂. In model crops, Rieske-OE provides transient increases of electron transport, which result in enhanced CO₂ assimilation rate only in the C₄ plant.

Figure 5.

The CBB cycle. Energy in the form of ATP and NADPH (dashed lines) needed to drive the CBB cycle is produced in the thylakoid membrane located electron transport chain. The first step in the CBB cycle is carboxylation (green arrow) catalyzed by Rubisco resulting in the formation of 3-PGA. The next two reactions form the reductive phase (purple arrows) and are catalyzed by phosphoglycerate kinase, forming glycerate 1,3-bisphosphate (BPGA) using ATP and glyceraldehyde 3-phosphate dehydrogenase which forms glyceraldehyde-3-phosphate (GAP) consuming NADPH. Triose phosphate isomerase (TPI) catalyzes the production of dihydroxyacetone phosphate and together with GAP enters the regenerative phase of the cycle (black arrows) catalyzed by fructose 1,6-bisphosphate/sedoheptulose 1,7-bisphosphate aldolase (FBPA), forming sedoheptulose 1,7-bisphosphate (S1,7-BP) and fructose 1,6-bisphosphate (F1,6-BP). SBPase and fructose 1,6-bisphosphatase (FBPase) then produce sedoheptulose 7-phosphate (S7-P) and fructose 6-phosphate (F6-P) which are converted to 5C compounds in reactions catalyzed by TK, ribose 5-P isomerase (RPI), and ribulose 5-phosphate epimerase (RPE) resulting in the formation ribulose 5-P (Ru5P). The final step in the cycle is catalyzed by ribulose 5-phosphate kinase producing the CO₂ acceptor molecule RuBP. The products of the CBB cycle are exported to several biosynthetic pathways for the biosynthesis of isoprenoids, starch, sucrose, shikimate, thiamine, and nucleotides. Rubisco has a competing oxygenase reaction, which results in the formation of 2-phosphoglycerate which enters the photorespiratory pathway (red arrows) (adapted from Raines 2003).

Figure 6.

Improving Rubisco activity in crops. A) The activity of Rubisco in a crop leaf can be enhanced by increasing the enzyme abundance, improving its catalytic properties, or optimizing its regulation. Increasing the abundance of Rubisco requires more nitrogen and carbon allocation to Rubisco; some versions of Rubisco show faster rates of carboxylation or higher specificity for CO₂ over O₂; regulation of the enzyme activity can be enhanced by optimizing the interaction with Rca and ensuring the chloroplast stroma environment is favorable for carboxylation. B) To achieve Rubisco-driven crop yield improvements requires consideration of the whole plant. The canopy of the crop will determine which strategy is most promising to improve Rubisco and obtain increased yields and climate resilience. Coordination between photosynthetic sub-processes as well as a productive integration with central and specialized metabolism, plant development, and environmental responses is essential to ensure efficient and sustainable agricultural crop production in present and future climates. A, Rca; C, carbon; N, nitrogen; R, Rubisco; Sugar-P, sugar phosphate derivative.

Figure 7.

Overview of the requirements for introducing biophysical CCMs into plants. A) Engineering a functional pyrenoid-based CCM condensate into a MC chloroplast requires condensation of Rubisco with a linker protein, such as EPYC1 in Chlamydomonas, into a pyrenoid-like matrix (shown as a green sphere) that is traversed by thylakoid membranes containing a specialized lumenal carbonic anhydrase (CAH3, shown in blue) and bestrophin-like bicarbonate (HCO₃⁻) channels on the thylakoid membrane (BST1-3, shown in orange). The addition of a diffusion barrier (e.g. a starch sheath shown in yellow) and an algal HCO₃⁻ channel on the chloroplast envelope (LCIA, shown in red) are predicted to increase the efficiency of CO₂ capture by Rubisco. B) A functional carboxysome-based CCM requires the correct assembly of carboxysome shells that encapsulate cyanobacterial Rubisco and a specialized carboxysomal CA (shown as green hexagons), and active bicarbonate (HCO₃⁻) transporters (such as SbtA and/or BicA, shown in dark blue) on the chloroplast envelope that elevate stromal HCO₃⁻ concentrations. Chloroplast stromal CA must be removed to prevent the loss of accumulated HCO₃⁻.

Figure 8.

Schematic representation of C₃, C₄, and C₃–C₄ intermediate photosynthesis. A) C₃ photosynthesis and photorespiration. Both mesophyll (M) and BSCs contain a fully functional photorespiratory pathway. B) C₄ photosynthesis. The process of photosynthetic carbon assimilation is divided into two cell types, M and BSCs. M cells act as carbon pumps that increase the CO₂ concentration in BSCs. In BSCs, the CBB cycle operates under elevated CO₂ concentration, which reduces the rate of photorespiration [photorespiratory (PR) pathway not shown; the distribution of the PR pathway between cell types in C₄ is likely equivalent to C₃–C₄ intermediate photosynthesis, as shown in Fig. 1C]. C) C₃–C₄ intermediate photosynthesis. Photorespiration is shared between M and BSCs, with mitochondrial glycine decarboxylation restricted to the BSCs. Glycine decarboxylation in BSCs locally increases the CO₂ concentration and allows for a more efficient carbon assimilation in this cell type. Please note that many details, cofactors, and pathway intermediates are not shown for clarity. Clp, chloroplast; Gly, glycine; Glyc, glycolate; HP, hydroxypyruvate; Mito, mitochondrion Perox, Peroxisome; Pyr, pyruvate; Rubisco, ribulose 1,5-bisphosphate carboxylase/oxygenase; RuBP, ribulose 1,5-bisphosphate; Ser, serine; TP, triose phosphates.

Figure 9.

Schematic diagrams. A) Illustrating kinetic responses of A and g_s to a change in light intensity from low (gray shading) to high intensity (white area). Stomatal responses (blue line) are an order of magnitude slower than A (red line). The shaded green area represents lost CO₂ due to diffusional constraints of slow stomatal opening, while the blue shading represents unnecessary water loss as a result of slow stomatal closure. B) Illustrating known mechanisms that increase the rapidity of g_s responses, including smaller stomata (top), dumbbell-shaped GC (middle), and manipulation of ion transport between GC and SC, at both the plasma membrane and the tonoplast (bottom).

Figure 10.

Systems approach to identify options to engineer photosynthesis for higher efficiency. A) Multi-scale models of photosynthesis. Models for photosynthesis at different organismal scales spanning from organelle, cell, leaf, up to canopy scales, have been developed. These models are used to define the architectural, anatomical, biophysical, and biochemical parameters controlling photosynthetic efficiency. B) Options to engineering photosynthesis for greater efficiency, divided into three categories: (i) increase the delivery of CO₂, (ii) optimize light distribution across a canopy, and (iii) manipulate photosynthetic machinery.