Recruitment of pre-existing networks during the evolution of C ₄ photosynthesis

Abstract

During C 4 photosynthesis, CO 2 is concentrated around the enzyme RuBisCO. The net effect is to reduce photorespiration while increasing water and nitrogen use efficiencies. Species that use C 4 photosynthesis have evolved independently from their C 3 ancestors on more than 60 occasions. Along with mimicry and the camera-like eye, the C 4 pathway therefore represents a remarkable example of the repeated evolution of a highly complex trait. In this review, we provide evidence that the polyphyletic evolution of C 4 photosynthesis is built upon pre-existing metabolic and genetic networks. For example, cells around veins of C 3 species show similarities to those of the C 4 bundle sheath in terms of C 4 acid decarboxylase activity and also the photosynthetic electron transport chain. Enzymes of C 4 photosynthesis function together in gluconeogenesis during early seedling growth of C 3 Arabidopsis thaliana. Furthermore, multiple C 4 genes appear to be under control of both light and chloroplast signals in the ancestral C 3 state. We, therefore, hypothesize that relatively minor rewiring of pre-existing genetic and metabolic networks has facilitated the recurrent evolution of this trait. Understanding how these changes are likely to have occurred could inform attempts to install C 4 traits into C 3 crops.This article is part of the themed issue 'Enhancing photosynthesis in crop plants: targets for improvement'.

ZmbHLH80 and ZmbHLH90 transcription factors act antagonistically and contribute to regulatePEPC1cell‐specific gene expression in maize

“…It has been proposed that some mechanisms regulating C 4 genes were recruited from C 3 ancestors (Williams et al ., ; Reyna‐llorens and Hibberd, ). Therefore, we decided to search for OsbHLH112 maize homologues and assess whether they also bind to the ZmPEPC1 upstream region.…”

“…C 4 evolution has been shown to make use of pre‐existing mechanisms present in C 3 species (Kajala et al ., ; Williams et al ., ; Reyna‐llorens and Hibberd, ). However, only cis ‐elements co‐opted from C 3 ancestors have been identified so far.…”

“…Thus, C 3 isoforms of C 4 genes acquired new regulatory mechanisms that allowed them to encode C 4 isozymes. It has been shown that besides the new mechanisms, the C 4 evolution used metabolic and genetic networks already existing in C 3 plants (Reyna‐llorens and Hibberd, ).…”

Photosynthesis solutions to enhance productivity

“…The second paper is by Raines and co-workers [23], who describe how increasing the level of another enzyme involved in the Calvin-Benson cycle of CO 2 assimilation, sedoheptulose-1,7-biphosphatase (SBPase) leads to enhanced photosynthesis, increased total biomass and dry seed yield. The review by Hibberd & Reyna-Llorens [24] considers what can be learned from the evolution of C4 photosynthesis, a process that facilitates CO 2 concentration in the Rubisco environment leading not only to improved carbon capture but also to increasing water and nitrogen use efficiencies. This scholarly overview considers how the polyphyletic evolution of C4 photosynthesis is built upon pre-existing metabolic and genetic networks and considers how relatively changes in pre-existing genetic minor and metabolic networks underpin the recurrent evolution of this process.…”

The role of alanine and aspartate aminotransferases in C4 photosynthesis

“…An efficient C 4 shuttle mechanism is achieved by coordinated architectural and biochemical adjustments. The components required for such carbon shuttles are present already in all C 3 plant species (Aubry et al 2011;Reyna-Llorens & Hibberd 2017), they just acquire novel expression and activity patterns. This made it possible that despite its complexity, C 4 photosynthesis could evolve over 60 times independently in the plant kingdom (Sage et al 2011;Sage 2016).…”