Genomic estimation of complex traits reveals ancient maize adaptation to temperate North America

Swarts, Kelly; Gutaker, Rafał M.; Benz, Bruce F.; Blake, Michael; Bukowski, Robert; Holland, James B.; Kruse-Peeples, Melissa; Lepak, Nicholas; Prim, Lynda; Romay, M. Cinta; Ross‐Ibarra, Jeffrey; Sánchez-González, José de Jesús; Schmidt, Chris; Schuenemann, Verena J.; Krause, Johannes; Matson, R. G.; Weigel, Detlef; Buckler, Edward S.; Burbano, Hernán A.

doi:10.1126/science.aam9425

Cited by 183 publications

(204 citation statements)

References 64 publications

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“…Genomic analysis of crop landraces can help determine the basis of local adaptation (Lasky et al, 2015;Li et al, 2017;Lin et al, 2014;Swarts et al, 2017). The aims of this study were to characterize factors shaping the genomic variation of Senegalese sorghum landraces, map genomic regions shaped by agroclimatic adaptation, and identify genes that could play a role in local adaptation.…”

Section: Discussionmentioning

confidence: 99%

Genomic signatures of adaptation to Sahelian and Soudanian climates in sorghum landraces of Senegal

Faye

Maina

et al. 2019

Ecology and Evolution

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Uncovering the genomic basis of climate adaptation in traditional crop varieties can provide insight into plant evolution and facilitate breeding for climate resilience. In the African cereal sorghum (Sorghum bicolor L. [Moench]), the genomic basis of adaptation to the semiarid Sahelian zone versus the subhumid Soudanian zone is largely unknown. To address this issue, we characterized a large panel of 421 georeferenced sorghum landrace accessions from Senegal and adjacent locations at 213,916 single‐nucleotide polymorphisms (SNPs) using genotyping‐by‐sequencing. Seven subpopulations distributed along the north‐south precipitation gradient were identified. Redundancy analysis found that climate variables explained up to 8% of SNP variation, with climate collinear with space explaining most of this variation (6%). Genome scans of nucleotide diversity suggest positive selection on chromosome 2, 4, 5, 7, and 10 in durra sorghums, with successive adaptation during diffusion along the Sahel. Putative selective sweeps were identified, several of which colocalize with stay‐green drought tolerance (Stg) loci, and a priori candidate genes for photoperiodic flowering and inflorescence morphology. Genome‐wide association studies of photoperiod sensitivity and panicle compactness identified 35 and 13 associations that colocalize with a priori candidate genes, respectively. Climate‐associated SNPs colocalize with Stg3a, Stg1, Stg2, and Ma6 and have allelic distribution consistent with adaptation across Sahelian and Soudanian zones. Taken together, the findings suggest an oligogenic basis of adaptation to Sahelian versus Soudanian climates, underpinned by variation in conserved floral regulatory pathways and other systems that are less understood in cereals.

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Section: Discussionmentioning

confidence: 99%

Genomic signatures of adaptation to Sahelian and Soudanian climates in sorghum landraces of Senegal

Faye

Maina

et al. 2019

Ecology and Evolution

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“…A total of 19 archaeological maize samples were sequenced in the three studies, including four 5000-year-old maize specimens from the Tehuacan Valley[46, 47] and fifteen 1900-year-old maize cobs from Turkey Pen Shelter in the southwestern United States[48]. The read processing and mapping followed the previous studies[46–48]. Filtered reads were mapped to the maize reference genome AGPv3.29[63] using bwa mem v0.7.10[64].…”

Section: Methodsmentioning

confidence: 99%

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

et al. 2018

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SUMMARY 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 centre 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 (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 single nucleotide polymorphism (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.

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“…For maize, the VCF files of GBS data were used from Swarts et al. (). In the case of barley, VCF files for all barley accessions were obtained from Mascher et al.…”

Section: Methodsmentioning

confidence: 99%

“…In the case of the maize data set, we used the populations defined in Swarts et al. (). In the case of the barley data set, we used the pairwise distance matrix we generated from the VCF of Mascher et al.…”

Section: Methodsmentioning

confidence: 99%

A re‐evaluation of the domestication bottleneck from archaeogenomic evidence

Allaby

Ware

Kistler

2018

Evolutionary Applications

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Domesticated crops show a reduced level of diversity that is commonly attributed to the “domestication bottleneck”; a drastic reduction in the population size associated with subsampling the wild progenitor species and the imposition of selection pressures associated with the domestication syndrome. A prediction of the domestication bottleneck is a sharp decline in genetic diversity early in the domestication process. Surprisingly, archaeological genomes of three major annual crops do not indicate that such a drop in diversity occurred early in the domestication process. In light of this observation, we revisit the general assumption of the domestication bottleneck concept in our current understanding of the evolutionary process of domestication.

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Genomic estimation of complex traits reveals ancient maize adaptation to temperate North America

Cited by 183 publications

References 64 publications

Genomic signatures of adaptation to Sahelian and Soudanian climates in sorghum landraces of Senegal

Genomic signatures of adaptation to Sahelian and Soudanian climates in sorghum landraces of Senegal

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

A re‐evaluation of the domestication bottleneck from archaeogenomic evidence

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