Natural Variation within a Species for Traits Underpinning C4 Photosynthesis.

Gregory Reeves,E.O Deedi Sogbohossou,Pallavi Singh,Julian M Hibberd,M Eric Schranz,Timo A Rossberg

doi:10.1104/pp.18.00168

Gregory Reeves, E.O Deedi Sogbohossou + Show 4 more

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https://doi.org/10.1104/pp.18.00168

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Abstract

Engineering C4 photosynthesis into C3 crops could substantially increase their yield by alleviating photorespiratory losses. This objective is challenging because the C4 pathway involves complex modifications to the biochemistry, cell biology, and anatomy of leaves. Forward genetics has provided limited insight into the mechanistic basis of these properties, and there have been no reports of significant quantitative intraspecific variation of C4 attributes that would allow trait mapping. Here, we show that accessions of the C4 species Gynandropsis gynandra collected from locations across Africa and Asia exhibit natural variation in key characteristics of C4 photosynthesis. Variable traits include bundle sheath size and vein density, gas-exchange parameters, and carbon isotope discrimination associated with the C4 state. The abundance of transcripts encoding core enzymes of the C4 cycle also showed significant variation. Traits relating to water use showed more quantitative variation than those associated with carbon assimilation. We propose that variation in these traits likely adapted the hydraulic system for increased water use efficiency rather than improving carbon fixation, indicating that selection pressure may drive C4 diversity in G. gynandra by modifying water use rather than photosynthesis. The accessions analyzed can be easily crossed and produce fertile offspring. Our findings, therefore, indicate that natural variation within this C4 species is sufficiently large to allow genetic mapping of key C4 traits and regulators.

Highlights

Engineering C4 photosynthesis into C3 crops could substantially increase their yield by alleviating photorespiratory losses
Despite the complex modifications associated with C4 photosynthesis, current estimates are that the C4 pathway has independently evolved more than 60 times in angiosperms (Sage, 2016), which suggests that a relatively straightforward route may allow the transition from the ancestral C3 state to the derived C4 state
After a binary categorization of phenotypes into either C3 or C4, mathematical modeling indicates that there is likely more than one route from which to acquire the C4 state (Williams et al, 2013) but that subsequent modifications, many of which are associated with rebalancing photorespiration, reinforce these improvements in photosynthesis and fitness (Heckmann et al, 2013; Mallmann et al, 2014; Bräutigam and Gowik, 2016)

Summary

Introduction

Engineering C4 photosynthesis into C3 crops could substantially increase their yield by alleviating photorespiratory losses. We show that accessions of G. gynandra show significant variation in both anatomical and physiological traits associated with C4 photosynthesis.

Results

Conclusion