Leaf- and diverged shoot meristem programs shape the stem in rice

Abstract

The stem is the shoot axis in seed plants and has been a primary target in breeding to regulate crop height. However, early processes of stem development remain elusive. Here we show that regulators for shoot meristems and leaves determine the node-internode pattern in rice. Mutants ofKNOX1genesOSH15andOSH1, known to maintain shoot meristem indeterminacy1,2, showed dwarfism due to enlarged nodes and diminished internodes. These genes confine node differentiation by repressing leaf developmental regulatorYABBYgenes in internodal vasculatures.YABBYexpression, which normally extends from leaves to nodes along vasculatures, promotes nodal vascular differentiation and limits stem elongation. It expands inknox1mutants, and the loss ofYABBYgenes reverts their dwarfism.OSH15also represses node-specificKNOX1subclade genesOSH6andOSH71to allow internode elongation. Importantly, bothYABBYand node-specificKNOX1genes are required for pulvinus formation at the leaf base, further elaborating the nodal structure for gravitropism. Thus, intersections between leaf and sub-functionalized shoot meristem programs shape nodes and internodes along the stem. Phylogenetic analysis showed thatKNOX1sub-functionalization likely occurred in the progenitor of gymnosperms and angiosperms. Given that seed plants acquired their leaves independently from other vascular plant lineages3,4, the emergence of the node-internode pattern andKNOX1-YABBYregulatory module may be linked to seed plant leaf evolution.