The role of photorespiration during the evolution of C4 photosynthesis in the genus Flaveria.

Julia Mallmann,Martin J Lercher,Peter Westhoff,Andreas P M Weber,Udo Gowik,Andrea Bräutigam,David Heckmann

doi:10.7554/elife.02478

Julia Mallmann, Martin J Lercher + Show 5 more

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https://doi.org/10.7554/elife.02478

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Abstract

C4 photosynthesis represents a most remarkable case of convergent evolution of a complex trait, which includes the reprogramming of the expression patterns of thousands of genes. Anatomical, physiological, and phylogenetic and analyses as well as computational modeling indicate that the establishment of a photorespiratory carbon pump (termed C2 photosynthesis) is a prerequisite for the evolution of C4. However, a mechanistic model explaining the tight connection between the evolution of C4 and C2 photosynthesis is currently lacking. Here we address this question through comparative transcriptomic and biochemical analyses of closely related C3, C3-C4, and C4 species, combined with Flux Balance Analysis constrained through a mechanistic model of carbon fixation. We show that C2 photosynthesis creates a misbalance in nitrogen metabolism between bundle sheath and mesophyll cells. Rebalancing nitrogen metabolism requires anaplerotic reactions that resemble at least parts of a basic C4 cycle. Our findings thus show how C2 photosynthesis represents a pre-adaptation for the C4 system, where the evolution of the C2 system establishes important C4 components as a side effect.

Highlights

The dual-specific enzyme ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) catalyzes two opposing reactions—the carboxylation and the oxygenation of ribulose 1,5-bisphosphate
To study the evolution of the expression of photorespiratory and C4 cycle genes during the transition from C3 to C4 photosynthesis in the genus Flaveria, nine species reflecting the evolutionary trajectory taken were selected, including two C3 (F. robusta and F. pringlei), two C4 (F. bidentis and F. trinervia), and five C3–C4 intermediate species (Figure 1D). According to their CO2 compensation points and the percentage of carbon initially fixed into malate and aspartate, F. chloraefolia and F. pubescens were earlier classified as type I C3–C4 intermediates
F. anomala and F. ramosissima belong to the type II C3–C4 intermediates and F. brownii is classified as a C4-like species (Edwards and Ku, 1987; Moore et al, 1987; Cheng et al, 1988; Ku et al, 1991)

Summary

Introduction

The dual-specific enzyme ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) catalyzes two opposing reactions—the carboxylation and the oxygenation of ribulose 1,5-bisphosphate. The former reaction yields 3-phosphoglycerate (3-PGA), whereas the latter produces 2-phosphoglycolate (2-PG). 2-PG is regenerated to 3-PGA, but it involves the release of formerly assimilated CO2 and NH3, entails energy costs for the plants and reduces the efficiency of photosynthesis by up to 30% (Ehleringer et al, 1991; Bauwe et al, 2010; Raines, 2011; Fernie et al, 2013). Eight core enzymes are required for photorespiration, which in higher plants are located in the chloroplast, the peroxisome, and the mitochondrion (Bauwe et al, 2010; Figure 1A). Ammonia refixation in the chloroplast by the combined activities of glutamine synthase (GS) and glutamine oxoglutarate aminotransferase (GOGAT) is an integral part of photorespiration

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