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Title: ZmCCT and the genetic basis of day-length adaptation underlying the postdomestication spread of maize

Author
item HUNG, HSIAO-YI - North Carolina State University
item SHANNON, LAURA - University Of Wisconsin
item TIAN, FENG - Cornell University
item Bradbury, Peter
item CHEN, CHARLES - Cornell University
item Flint-Garcia, Sherry
item McMullen, Michael
item Ware, Doreen
item Buckler, Edward - Ed
item DOEBLEY, JOHN - University Of Wisconsin
item Holland, Jim - Jim

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/28/2012
Publication Date: 6/18/2012
Citation: Hung, H., Shannon, L.M., Tian, F., Bradbury, P., Chen, C., Flint Garcia, S.A., McMullen, M.D., Ware, D., Buckler IV, E.S., Doebley, J.F., Holland, J.B. 2012. ZmCCT and the genetic basis of day-length adaptation underlying the postdomestication spread of maize. Proceedings of the National Academy of Sciences. 109:E1913–E1921.

Interpretive Summary: Maize was domesticated from the tropical grass teosinte, a species restricted to tropical environments in Mexico and Central America (1). Maize-growing culture spread from its Meso-American center of origin to current day Canada and Chile before the arrival of Columbus. The transition to flowering in teosinte is highly sensitive to small changes in daylengths that occur in its native range, perhaps as a way to coordinate flowering with rainfall patterns. In contrast, reproductive fitness for maize of the higher latitudes depends on its capacity to flower even under the much longer summer daylengths of these environments. Thus, the spread of maize from its tropical center of origin to the higher latitudes of the Americas required selection for adaptation to longer daylengths. In this paper we studied the genome regions controlling the response to photoperiod in maize. We identified a single gene with the largest effect on photoperiod response in both maize and teosinte. The gene, ZmCCT, is similar to the Ghd7 gene which regulates photoperiod response in rice. We showed that all teosintes tested carry the photoperiod responsive allele at this gene and that the gene is expressed at higher levels than temperate maize alleles in maize-teosinte hybrids under long daylengths, as expected for a gene that represses flowering under long daylengths.

Technical Abstract: Teosinte, the progenitor of maize, is restricted to tropical environments in Mexico and Central America. The pre-Columbian spread of maize from its center of origin in tropical Southern Mexico to the higher latitudes of the Americas required post-domestication selection for adaptation to longer daylengths. Flowering time of teosinte and tropical maize is delayed under long daylengths, whereas temperate maize evolved a reduced sensitivity to photoperiod. We measured flowering time of the maize nested association mapping population and a diverse maize association panel in the field under both short and long daylengths, and of a maize-teosinte mapping population under long daylengths. Flowering time in maize is a complex trait affected by many genes and the environment. Photoperiod response is controlled by fewer genes with larger phenotypic effects that appear to be a subset of overall flowering time genes. Genome-wide association and targeted high resolution linkage mapping identified ZmCCT, a homolog of the rice photoperiod response regulator Ghd7, as the most important gene affecting photoperiod response in maize. Functional analysis of this gene revealed that it is expressed at high levels and confers later flowering under long daylengths in diverse teosinte compared to temperate maize inbred lines. Many maize inbred lines, including some adapted to tropical regions, carry ZmCCT alleles with no sensitivity to daylength. Prehistoric plant breeders were remarkably successful at selecting on genetic variation at key genes affecting the photoperiod response to create maize varieties adapted to vastly diverse environments despite the hindrance of the geographic axis of the Americas and the complex genetic control of flowering time.