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 journalArticleResearchpeer-review

5 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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Zea mays
Florigen
Genes
flowering
corn
Single Nucleotide Polymorphism
Zea
Zea mays subsp. parviglumis
Zea mays subsp. mays
florigen
alleles
center of origin
early selection
domestication
inbred lines
Alleles
quantitative trait loci
haplotypes
ancestry
genes

Cite this

Guo, Li ; Wang, Xuehan ; Zhao, Min ; Huang, Cheng ; Li, Cong ; Li, Dan ; Yang, Chin Jian ; York, Alessandra M ; Xue, Wei ; Xu, Guanghui ; Liang, Yameng ; Chen, Qiuyue ; Doebley, John F ; Tian, Feng. / Stepwise cis-regulatory changes in ZCN8 contribute to maize flowering-time adaptation. In: Current Biology. 2018 ; pp. 3005-3015.
@article{f196217813a948e793267126b93d7243,
title = "Stepwise cis-regulatory changes in ZCN8 contribute to maize flowering-time adaptation",
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.",
author = "Li Guo and Xuehan Wang and Min Zhao and Cheng Huang and Cong Li and Dan Li and Yang, {Chin Jian} and York, {Alessandra M} and Wei Xue and Guanghui Xu and Yameng Liang and Qiuyue Chen and Doebley, {John F} and Feng Tian",
year = "2018",
month = "9",
day = "13",
doi = "10.1016/j.cub.2018.07.029",
language = "English",
pages = "3005--3015",
journal = "Current Biology",
issn = "0960-9822",
publisher = "Cell Press",

}

Guo, L, Wang, X, Zhao, M, Huang, C, Li, C, Li, D, Yang, CJ, York, AM, Xue, W, Xu, G, Liang, Y, Chen, Q, Doebley, JF & Tian, F 2018, 'Stepwise cis-regulatory changes in ZCN8 contribute to maize flowering-time adaptation', Current Biology, pp. 3005-3015. https://doi.org/10.1016/j.cub.2018.07.029

Stepwise cis-regulatory changes in ZCN8 contribute to maize flowering-time adaptation. / Guo, Li ; Wang, Xuehan; Zhao, Min; Huang, Cheng; Li, Cong; Li, Dan; Yang, Chin Jian; York, Alessandra M; Xue, Wei; Xu, Guanghui; Liang, Yameng; Chen, Qiuyue; Doebley, John F; Tian, Feng.

In: Current Biology, 13.09.2018, p. 3005-3015.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Stepwise cis-regulatory changes in ZCN8 contribute to maize flowering-time adaptation

AU - Guo, Li

AU - Wang, Xuehan

AU - Zhao, Min

AU - Huang, Cheng

AU - Li, Cong

AU - Li, Dan

AU - Yang, Chin Jian

AU - York, Alessandra M

AU - Xue, Wei

AU - Xu, Guanghui

AU - Liang, Yameng

AU - Chen, Qiuyue

AU - Doebley, John F

AU - Tian, Feng

PY - 2018/9/13

Y1 - 2018/9/13

N2 - 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.

AB - 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.

U2 - 10.1016/j.cub.2018.07.029

DO - 10.1016/j.cub.2018.07.029

M3 - Article

SP - 3005

EP - 3015

JO - Current Biology

JF - Current Biology

SN - 0960-9822

ER -