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

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 of KNOX1 genes OSH15 and OSH1, 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 regulator YABBY genes in internodal vasculatures. YABBY expression, which normally extends from leaves to nodes along vasculatures, promotes nodal vascular differentiation and limits stem elongation. It expands in knox1 mutants, and the loss of YABBY genes reverts their dwarfism. OSH15 also represses node-specific KNOX1 subclade genes OSH6 and OSH71 to allow internode elongation. Importantly, both YABBY and node-specific KNOX1 genes 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 that KNOX1 sub-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 and KNOX1-YABBY regulatory module may be linked to seed plant leaf evolution.