A transcription factor module mediating C2 photosynthesis

Abstract

C4 photosynthesis has arisen from the ancestral C3 state in over sixty lineages of angio-sperms. It is widely accepted that an early step in C4 evolution is restriction of glycine decarboxylase activity to bundle sheath cells to generate the so-called C2 pathway. In C2 Moricandia species, changes to the cis-regulatory region controlling expression of the P-subunit of GLYCINE DECARBOXYLASE (GLDP) in mesophyll cells enables this trait, but the mechanism underpinning GLDP expression in the bundle sheath is not known. We identify a MYC-MYB transcription factor module previously associated with the control of glucosinolate bio-synthesis as the basis of GLDP expression in bundle sheath cells. In C3 Arabidopsis thaliana this module drives GLDP expression in bundle sheath cells along with as yet unidentified factors driving expression in mesophyll cells. In the C2 species Moricandia arvensis, GLDP expression is lost from mesophyll cells and 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 foundational step in the evolution of C4 photosynthesis.