Photosynthesis in C ₃–C ₄ intermediate Moricandia species

Abstract

Analysis of the genus Moricandia, which contains C ₃ and C ₃–C ₄ intermediate plants, reveals potential environmental and anatomical constraints to the evolution of C ₄ photosynthesis.

Abstract

Evolution of C ₄ photosynthesis is not distributed evenly in the plant kingdom. Particularly interesting is the situation in the Brassicaceae, because the family contains no C ₄ species, but several C ₃–C ₄ intermediates, mainly in the genus Moricandia. Investigation of leaf anatomy, gas exchange parameters, the metabolome, and the transcriptome of two C ₃–C ₄ intermediate Moricandia species, M. arvensis and M. suffruticosa, and their close C ₃ relative M. moricandioides enabled us to unravel the specific C ₃–C ₄ characteristics in these Moricandia lines. Reduced CO ₂ 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 C ₃ to C ₃–C ₄ 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 C ₃–C ₄ pathway was not accompanied by enhanced activity of the C ₄ cycle. Our results indicate that metabolic limitations connected to N metabolism or anatomical limitations connected to vein density could have constrained evolution of C ₄ in Moricandia.