ZmMADS69 functions as a flowering activator through the ZmRap2.7-ZCN8 regulatory module and contributes to maize flowering time adaptation

Flowering time is a major determinant of the local adaptation of plants. Although numerous loci affecting flowering time have been mapped in maize, their underlying molecular mechanisms and roles in adaptation remain largely unknown. Here, we report the identification and characterization of MADS-box transcription factor ZmMADS69 that functions as a flowering activator through the ZmRap2.7-ZCN8 regulatory module and contributes to adaptation. We show that ZmMADS69 underlies a quantitative trait locus controlling the difference in flowering time between maize and its wild ancestor, teosinte. Maize ZmMADS69 allele is expressed at a higher level at floral transition and confers earlier flowering than the teosinte allele under long days and short days. Overexpression of ZmMADS69 causes early flowering, while a transposon insertion mutant of ZmMADS69 exhibits delayed flowering. ZmMADS69 shows pleiotropic effects for multiple traits of agronomic importance. ZmMADS69 functions upstream of the flowering repressor ZmRap2.7 to downregulate its expression, thereby relieving the repression of the florigen gene ZCN8 and causing early flowering. Population genetic analyses showed that ZmMADS69 was a target of selection and may have played an important role as maize spread from the tropics to temperate zones. Our findings provide important insights into the regulation and adaptation of flowering time.