ZmSPL13 and ZmSPL29 act together to promote vegetative and reproductive transition in maize

Flowering time is a key agronomic trait determining environmental adaptation and yield potential of crops. The regulatory mechanisms of flowering in maize still remain rudimentary. In this study, we combine expressional, genetic, and molecular studies to identify two homologous SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) transcription factors ZmSPL13 and ZmSPL29 as positive regulators of juvenile-to-adult vegetative transition and floral transition in maize. We show that both ZmSPL13 and ZmSPL29 are preferentially expressed in leaf phloem, vegetative and reproductive meristem. We show that vegetative phase change and flowering time are moderately delayed in the Zmspl13 and Zmspl29 single knockout mutants and more significantly delayed in the Zmspl13/29 double mutants. Consistently, the ZmSPL29 overexpression plants display precocious vegetative phase transition and floral transition, thus early flowering. We demonstrate that ZmSPL13 and ZmSPL29 directly upregulate the expression of ZmMIR172C and ZCN8 in the leaf, and of ZMM3 and ZMM4 in the shoot apical meristem, to induce juvenile-to-adult vegetative transition and floral transition. These findings establish a consecutive signaling cascade of the maize aging pathway by linking the miR156-SPL and the miR172-Gl15 regulatory modules and provide new targets for genetic improvement of flowering time in maize cultivars.