A transcription factor module mediating C2 photosynthesis in the Brassicaceae

Abstract

C4 photosynthesis has arisen from the ancestral C3 state in over sixty lineages of angiosperms. It is widely accepted that an early step in C4 evolution is associated with the appearance of so-called C2 photosynthesis caused by loss of glycine decarboxylase activity from mesophyll cells followed by activation in the bundle sheath. Although changes in cis to a distal enhancer upstream of the P-subunit of GLYCINE DECARBOXYLASE (GLDP) from C2 Moricandia enable loss of expression from mesophyll cells, the mechanism then allowing GLDP expression in the bundle sheath is not known. Here we identify a MYC-MYB transcription factor module previously associated with the control of glucosinolate biosynthesis as the basis of this foundational event in the evolution of C2 photosynthesis. Specifically, we find that in the C3 state this MYC-MYB module already patterns GLDP expression to bundle sheath cells. As a consequence, when GLDP expression is lost from the mesophyll, the MYC-MYB dependent expression in the bundle sheath is revealed. Evolution of C2 photosynthesis is thus associated with a MYC-MYB based transcriptional network already present in the C3 state. This work identifies a molecular genetic mechanism underlying the bundle sheath accumulation of glycine decarboxylase required for C2 photosynthesis and thus a fundamental step in the evolution of C4 photosynthesis.