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Curr Biol. 2018 Sep 24;28(18):3005-3015.e4. doi: 10.1016/j.cub.2018.07.029. Epub 2018 Sep 13.

Stepwise cis-Regulatory Changes in ZCN8 Contribute to Maize Flowering-Time Adaptation.

Author information

1
National Maize Improvement Center, Key Laboratory of Biology and Genetic Improvement of Maize (MOA), Beijing Key Laboratory of Crop Genetic Improvement, Joint International Research Laboratory of Crop Molecular Breeding, China Agricultural University, Beijing 100193, China.
2
Department of Genetics, University of Wisconsin, Madison, WI 53706, USA.
3
National Maize Improvement Center, Key Laboratory of Biology and Genetic Improvement of Maize (MOA), Beijing Key Laboratory of Crop Genetic Improvement, Joint International Research Laboratory of Crop Molecular Breeding, China Agricultural University, Beijing 100193, China; Department of Genetics, University of Wisconsin, Madison, WI 53706, USA.
4
National Maize Improvement Center, Key Laboratory of Biology and Genetic Improvement of Maize (MOA), Beijing Key Laboratory of Crop Genetic Improvement, Joint International Research Laboratory of Crop Molecular Breeding, China Agricultural University, Beijing 100193, China. Electronic address: ft55@cau.edu.cn.

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 [2-4], 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.

KEYWORDS:

QTL; adaptation; domestication; flowering time; maize; selection; teosinte

PMID:
30220503
PMCID:
PMC6537595
DOI:
10.1016/j.cub.2018.07.029
[Indexed for MEDLINE]
Free PMC Article

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