A core genetic mechanism integrates growth hormone signals to control meristem fate and inflorescence architecture in setaria and maize

Inflorescence architecture in cereals is a major determinant of grain yield and harvestability. Architecture is determined by the number, arrangement and order of lateral branches, which are formed from clusters of stem cells called meristems. Variation in branching patterns arises from regulation of meristem determinacy, i.e., indeterminate meristems maintain meristematic activity allowing for higher order branching and determinate meristems form a terminal organ. The timing by which an indeterminate branch meristem acquires a determinate fate and transitions to a spikelet meristem (SM), ultimately forming the grain-bearing spikelet, defines architecture and grain yield potential. This study leverages the unique inflorescence morphology of model grass Setaria viridis (setaria) to identify factors controlling SM fate and determinacy and characterize their interactions. In setaria, axillary branches terminate either in a spikelet or sterile bristle, where the latter loses SM identity due to brassinosteroid (BR)-mediated disruption of organ boundary formation. A forward genetics screen identified two mutants with only bristles on their panicles; one defective in gibberellic acid (GA) signaling caused extreme elongation and disruption of spikelet development and the other homeotically converted spikelets to bristles. The latter named spikeletless (spkl) was mapped and validated as an ortholog of the maize determinacy factor ramosa1 (ra1). Genetic analyses showed that SvRa1 acts upstream of BR-mediated regulation of SM identity and determinacy. A model is proposed where SvRA1 maintains SM fate by modulating GA homeostasis, spatially restricting BR signaling and preserving boundary gene expression and determinacy. In bristle primordia, which are generally paired with spikelets, GA and BR act synergistically. Comparative analyses in maize highlight pathway conservation in inflorescence architecture with some specific variations.