A genetic program for rapid initiation of axillary meristems at the onset of flowering

Shoot branching patterns and their diversity arise from variable activities of axillary meristems (AMs). A common feature of flowering plants is delayed AM initiation and growth during the vegetative phase, followed by a sudden and rapid acceleration of apical AM initiation during the reproductive phase. The mechanisms underlying this pronounced developmental shift are poorly understood. During tomato floral transition, the primary shoot meristem (PSM) terminates in a flower after producing two spatially adjacent AMs: one that will generate a flower and the other a vegetative side shoot. In plants lacking the universal floral-promoting mobile protein florigen, these processes are uncoupled: The vegetative AM initiation is delayed, even though termination of the PSM into a flower is largely unaffected. To identify factors that promote AM initiation in response to flowering induction signals, we analyzed a high-temporal-density single-meristem transcriptome profile from wild-type and florigen-defective plants. Our analysis revealed two genes, PUCHI and LOB30, induced by florigen in incipient AMs. These genes promote rapid initiation of both the vegetative and reproductive AMs, with the latter facilitating formation of a multi-flower inflorescence. Counterintuitively, these genes act in parallel with a PSM maturation program that limits production of reproductive AMs. Together, our findings uncover a florigen-induced regulatory mechanism that controls the reproductive-specific timing of AM initiation and provides a framework for understanding plasticity and diversification of shoot branching patterns.