Photosynthesis in C(3)–C(4) intermediate Moricandia species

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.