Regulation of Leaf Maturation by Chromatin-Mediated Modulation of Cytokinin Responses

Plant shoots display indeterminate growth, while their evolutionary decedents, the leaves, are determinate. Determinate leaf growth is conditioned by the CIN-TCP transcription factors, which promote leaf maturation and are negatively regulated by miR319 in leaf primordia. Here we show that CIN-TCPs reduce leaf sensitivity to cytokinin (CK), a phytohormone implicated in inhibition of differentiation in the shoot. We identify the SWI/SNF chromatin remodeling ATPase BRAHMA (BRM) as a genetic mediator of CIN-TCP activities and CK responses. An interactome screen further revealed that SWI/SNF complex components including BRM preferentially interacted with basic-helix-loop-helix (bHLH) transcription factors and the bHLH-related CIN-TCPs. Indeed, TCP4 and BRM interacted in planta. Both TCP4 and BRM bound the promoter of an inhibitor of CK responses, ARR16, and induced its expression. Reconstituting ARR16 levels in leaves with reduced CIN-TCP activity restored normal growth. Thus, CIN-TCP and BRM together promote determinate leaf growth by stage-specific modification of CK responses. ► CIN-TCP transcription factors such as TCP4 modulate Arabidopsis leaf response to CK ► A genetic screen identifies the chromatin remodeler BRM as required for TCP4 action ► An interactome screen identifies TCPs as preferential BRM interactors ► TCP4 and BRM directly induce ARR16, a negative CK response regulator CIN-TCP transcription factors and the hormone cytokinin (CK) play opposing roles in leaf maturation. Efroni et al. show that the CIN-TCP factor TCP4 interacts with SWI/SNF chromatin remodeler BRM to modulate sensitivity to CK. BRM and TCP4 induce the CK response inhibitor ARR16, determining leaf growth by stage-specific modification of CK responses.