Improving C4 photosynthesis to increase productivity under optimal and suboptimal conditions

Abstract

Although improving photosynthetic efficiency is widely recognised as an underutilized strategy to increase crop yields, research in this area is strongly biased towards species with C3 photosynthesis relative to C4 species. Here, we outline potential strategies for improving C4 photosynthesis to increase yields in crops by reviewing the major bottlenecks limiting the C4 NADP-ME pathway under optimal and suboptimal conditions. Recent experimental results demonstrate that steady state C4 photosynthesis under non-stressed conditions can be enhanced by increasing Rubisco content or electron transport capacity, both of which may also stimulate CO2 assimilation at supra-optimal temperatures. Several additional putative bottlenecks for photosynthetic performance under drought, heat or chilling stress or during photosynthetic induction await further experimental verification. Based on source-sink interactions in maize, sugarcane and sorghum, alleviating these photosynthetic bottlenecks during establishment and growth of the harvestable parts are expected to improve yield. The expected benefits are also shown to be augmented by the increasing trend in planting density, which increases the impact of photosynthetic source limitation on crop yields.

Can we improve the chilling tolerance of maize photosynthesis through breeding?

“…Rubisco has been speculated to be especially limiting in chilling conditions in C 4 species, since C 4 plants contain less Rubisco and because Rubisco is operating closer to its maximum capacity due to the high concentration of CO 2 created by the carbon-concentrating mechanism ( Sage and McKown, 2006 ). Furthermore, enhanced degradation of photosynthetic gene products under chilling stress reduces the amounts of enzymes in the leaf: protein breakdown is increased at low temperatures (reviewed by Sales et al , 2021 ). Specifically, the photosynthetic enzymes pyruvate, phosphate dikinase (PPDK; BRENDA: EC 2.7.9.1), PEPC, and Rubisco break down more easily under chilling conditions in C 4 species ( Kingston-Smith et al , 1997 ; Du et al , 1999 ; Chinthapalli et al , 2003 ).…”

“…While this review focuses on pre-existing variation in chilling tolerance of photosynthesis in maize, and the genomic regions related to this tolerance which may be utilized in breeding programmes, it is worth noting that genetic modification approaches also offer valuable tools for improving photosynthesis and chilling tolerance. For example, increasing Rubisco and electron transport capacity can improve the photosynthetic performance of C 4 plants; Rubisco is predicted to have a greater effect on chilling recovery than other photosynthetic enzymes in the C 4 pathway ( Sales et al , 2021 ). The overexpression of Rubisco large and small subunits, in concert with Rubisco Assembly Factor 1 (RAF1), increased maize Rubisco content by >30% (although Rubisco activase is probably a vital factor for translating this increased enzyme content into a proportional increase in photosynthetic activity); this overexpression of Rubisco can speed recovery following chilling stress ( Salesse-Smith et al , 2018 ).…”

Here comes the sun: How optimization of photosynthetic light reactions can boost crop yields

“…This review focuses on the photosynthetic light‐dependent reactions, the optimization of which is relevant to improving both C3 and C4 photosynthesis in plants and photosynthetic micro‐organisms (Leister, 2012; Ruban, 2015; von Caemmerer and Furbank, 2016; Cardona et al, 2018; Simkin et al, 2019; Batista‐Silva et al, 2020; Ermakova et al, 2021b; Sales et al, 2021; Santos‐Merino et al, 2021). Modeling studies have suggested that improving the quantum yield and electron transport capacity have a greater potential for increasing the productivity of crops than other photosynthetic mechanisms, such as improving Rubisco activity (Gu et al, 2014; Yin and Struik, 2015, 2021a; Wu et al, 2019).…”

Assessing heritability of biochemical limitations in photosynthesis can help elucidate new targets for improvement

“…However, previous studies have documented the potential benefit of improving crop performance by selecting for enhanced J max , which has been correlated with increased final biomass as well as increased levels of CO 2 assimilation (Gu et al, 2014; Sales et al, 2021). While it may be difficult to understand the role of source‐limitation in elevated [CO 2 ] within the context of this study, especially since the plants that were utilized were not acclimated to elevated [CO2], there is still much promise and merit in the selection of traits such as J max and V cmax as a method to improve overall photosynthetic performance.…”