Rice osa-miR171c Mediates Phase Change from Vegetative to Reproductive Development and Shoot Apical Meristem Maintenance by Repressing Four OsHAM Transcription Factors

Phase change from vegetative to reproductive development is one of the critical developmental steps in plants, and it is regulated by both environmental and endogenous factors. The maintenance of shoot apical meristem (SAM) identity, miRNAs and flowering integrators are involved in this phase change process. Here, we report that the miRNA osa-miR171c targets four GRAS (GAI-RGA-SCR) plant-specific transcription factors (OsHAM1, OsHAM2, OsHAM3, and OsHAM4) to control the floral transition and maintenance of SAM indeterminacy in rice (Oryza sativa). We characterized a rice T-DNA insertion delayed heading (dh) mutant, where the expression of OsMIR171c gene is up-regulated. This mutant showed pleiotropic phenotypic defects, including especially prolonged vegetative phase, delayed heading date, and bigger shoot apex. Parallel expression analysis showed that osa-miR171c controlled the expression change of four OsHAMs in the shoot apex during floral transition, and responded to light. In the dh mutant, the expression of the juvenile-adult phase change negative regulator osa-miR156 was up-regulated, expression of the flowering integrators Hd3a and RFT1 was inhibited, and expression of FON4 negative regulators involved in the maintenance of SAM indeterminacy was also inhibited. From these data, we propose that the inhibition of osa-miR171c-mediated OsHAM transcription factors regulates the phase transition from vegetative to reproductive development by maintaining SAM indeterminacy and inhibiting flowering integrators.