Photosynthesis in C3-C4 intermediate Moricandia species.

Urte Schlüter,Pascal-Antoine Christin,Udo Gowik,Andrea Bräutigam,Samantha Kurz,Tabea Mettler-Altmann,Michael Melzer,Andreas Pm Weber

doi:10.1093/jxb/erw391

Abstract

Evolution of C4 photosynthesis is not distributed evenly in the plant kingdom. Particularly interesting is the situation in the Brassicaceae, because the family contains no C4 species, but several C3-C4 intermediates, mainly in the genus Moricandia Investigation of leaf anatomy, gas exchange parameters, the metabolome, and the transcriptome of two C3-C4 intermediate Moricandia species, M. arvensis and M. suffruticosa, and their close C3 relative M. moricandioides enabled us to unravel the specific C3-C4 characteristics in these Moricandia lines. Reduced CO2 compensation points in these lines were accompanied by anatomical adjustments, such as centripetal concentration of organelles in the bundle sheath, and metabolic adjustments, such as the balancing of C and N metabolism between mesophyll and bundle sheath cells by multiple pathways. Evolution from C3 to C3-C4 intermediacy was probably facilitated first by loss of one copy of the glycine decarboxylase P-protein, followed by dominant activity of a bundle sheath-specific element in its promoter. In contrast to recent models, installation of the C3-C4 pathway was not accompanied by enhanced activity of the C4 cycle. Our results indicate that metabolic limitations connected to N metabolism or anatomical limitations connected to vein density could have constrained evolution of C4 in Moricandia.

Highlights

C4 plants evolved in warm, open, and often arid regions, where the C4 concentrating mechanism leads to enhanced photosynthetic carbon fixation efficiency (Sage, 2004)
Potential C3–C4 intermediates were identified by their CO2 compensation point, which lay between the values of C3 and C4 species, as well as some C4-like anatomical features in the bundle sheath (BS) cells (Kennedy and Laetsch, 1974; Krenzer et al, 1975)
A C3 group (M. moricandioides, M. foetida) was sister to the C3–C4 intermediate species (M. arvensis, M. suffruticosa, M. nitens, M. sinaica, M. spinosa; Fig. 1A), indicating that the evolution of the C3–C4 intermediate character is mostparsimoniously explained by a single event in the Moricandia genus

Summary

Introduction

C4 plants evolved in warm, open, and often arid regions, where the C4 concentrating mechanism leads to enhanced photosynthetic carbon fixation efficiency (Sage, 2004). Potential C3–C4 intermediates were identified by their CO2 compensation point, which lay between the values of C3 and C4 species, as well as some C4-like anatomical features in the BS cells (Kennedy and Laetsch, 1974; Krenzer et al, 1975). The Brassicaceae species Moricandia arvensis was among the first species classified as a potential C3–C4 intermediate (Krenzer et al, 1975)

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Discussion

Conclusion