Stepwise cis-regulatory changes in ZCN8 contribute to maize flowering-time adaptation

Li Guo, Xuehan Wang, Min Zhao, Cheng Huang, Cong Li, Dan Li, Chin Jian Yang, Alessandra M York, Wei Xue, Guanghui Xu, Yameng Liang, Qiuyue Chen, John F Doebley, Feng Tian*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

23 Citations (Scopus)

Abstract

Maize (Zea mays ssp. mays) was domesticated in southwestern Mexico ∼9,000 years ago from its wild ancestor, teosinte (Zea mays ssp. parviglumis) [1]. From its center of origin, maize experienced a rapid range expansion and spread over 90° of latitude in the Americas [2, 3, 4], which required a novel flowering-time adaptation. ZEA CENTRORADIALIS 8 (ZCN8) is the maize florigen gene and has a central role in mediating flowering [5, 6]. Here, we show that ZCN8 underlies a major quantitative trait locus (QTL) (qDTA8) for flowering time that was consistently detected in multiple maize-teosinte experimental populations. Through association analysis in a large diverse panel of maize inbred lines, we identified a SNP (SNP-1245) in the ZCN8 promoter that showed the strongest association with flowering time. SNP-1245 co-segregated with qDTA8 in maize-teosinte mapping populations. We demonstrate that SNP-1245 is associated with differential binding by the flowering activator ZmMADS1. SNP-1245 was a target of selection during early domestication, which drove the pre-existing early flowering allele to near fixation in maize. Interestingly, we detected an independent association block upstream of SNP-1245, wherein the early flowering allele that most likely originated from Zea mays ssp. mexicana introgressed into the early flowering haplotype of SNP-1245 and contributed to maize adaptation to northern high latitudes. Our study demonstrates how independent cis-regulatory variants at a gene can be selected at different evolutionary times for local adaptation, highlighting how complex cis-regulatory control mechanisms evolve. Finally, we propose a polygenic map for the pre-Columbian spread of maize throughout the Americas.
Original languageEnglish
Pages (from-to)3005-3015
Number of pages11
JournalCurrent Biology
Early online date13 Sep 2018
DOIs
Publication statusFirst published - 13 Sep 2018
Externally publishedYes

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