The genetic architecture of teosinte catalyzed and constrained maize domestication

Chin Jian Yang, Luis Fernando Samayoa, Peter J Bradbury, Bode A Olukolu, Wei Xue, Alessandra M York, Michael R Tuholski, Weidong Wang, Lora L Daskalska, Michael A Neumeyer, Jose de Jesus Sanchez-Gonzalez, Maria Cinta Romay, Jeffrey C Glaubitz, Qi Sun, Edward S Buckler, James B Holland, John F Doebley*

*Corresponding author for this work

Research output: Contribution to journalArticleResearchpeer-review

2 Citations (Scopus)

Abstract

The process of evolution under domestication has been studied using phylogenetics, population genetics–genomics, quantitative trait locus (QTL) mapping, gene expression assays, and archaeology. Here, we apply an evolutionary quantitative genetic approach to understand the constraints imposed by the genetic architecture of trait variation in teosinte, the wild ancestor of maize, and the consequences of domestication on genetic architecture. Using modern teosinte and maize landrace populations as proxies for the ancestor and domesticate, respectively, we estimated heritabilities, additive and dominance genetic variances, genetic-by-environment variances, genetic correlations, and genetic covariances for 18 domestication-related traits using realized genomic relationships estimated from genome-wide markers. We found a reduction in heritabilities across most traits, and the reduction is stronger in reproductive traits (size and numbers of grains and ears) than vegetative traits. We observed larger depletion in additive genetic variance than dominance genetic variance. Selection intensities during domestication were weak for all traits, with reproductive traits showing the highest values. For 17 of 18 traits, neutral divergence is rejected, suggesting they were targets of selection during domestication. Yield (total grain weight) per plant is the sole trait that selection does not appear to have improved in maize relative to teosinte. From a multivariate evolution perspective, we identified a strong, nonneutral divergence between teosinte and maize landrace genetic variance–covariance matrices (G-matrices). While the structure of G-matrix in teosinte posed considerable genetic constraint on early domestication, the maize landrace G-matrix indicates that the degree of constraint is more unfavorable for further evolution along the same trajectory.
Original languageEnglish
Pages (from-to)5643-5652
Number of pages10
JournalProceedings of the National Academy of Sciences of the United States of America
Volume116
Issue number12
Early online date6 Mar 2019
DOIs
Publication statusPrint publication - 19 Mar 2019
Externally publishedYes

Fingerprint

Zea
domestication
corn
genetic variance
landraces
reproductive traits
dominance (genetics)
ancestry
heritability
genetic covariance
selection intensity
quantitative genetics
genetic correlation
trajectories
ears
quantitative trait loci
genomics
gene expression
genome
phylogeny

Bibliographical note

Copyright © 2019 the Author(s). Published by PNAS.

Keywords

  • Agriculture
  • Chromosome Mapping/methods
  • Chromosomes, Plant/physiology
  • Domestication
  • Edible Grain/genetics
  • Evolution, Molecular
  • Genetics, Population/methods
  • Genomics
  • Phenotype
  • Plant Proteins/genetics
  • Quantitative Trait Loci
  • Selection, Genetic/genetics
  • Zea mays/genetics

Cite this

Yang, Chin Jian ; Samayoa, Luis Fernando ; Bradbury, Peter J ; Olukolu, Bode A ; Xue, Wei ; York, Alessandra M ; Tuholski, Michael R ; Wang, Weidong ; Daskalska, Lora L ; Neumeyer, Michael A ; Sanchez-Gonzalez, Jose de Jesus ; Romay, Maria Cinta ; Glaubitz, Jeffrey C ; Sun, Qi ; Buckler, Edward S ; Holland, James B ; Doebley, John F. / The genetic architecture of teosinte catalyzed and constrained maize domestication. In: Proceedings of the National Academy of Sciences of the United States of America. 2019 ; Vol. 116, No. 12. pp. 5643-5652.
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title = "The genetic architecture of teosinte catalyzed and constrained maize domestication",
abstract = "The process of evolution under domestication has been studied using phylogenetics, population genetics–genomics, quantitative trait locus (QTL) mapping, gene expression assays, and archaeology. Here, we apply an evolutionary quantitative genetic approach to understand the constraints imposed by the genetic architecture of trait variation in teosinte, the wild ancestor of maize, and the consequences of domestication on genetic architecture. Using modern teosinte and maize landrace populations as proxies for the ancestor and domesticate, respectively, we estimated heritabilities, additive and dominance genetic variances, genetic-by-environment variances, genetic correlations, and genetic covariances for 18 domestication-related traits using realized genomic relationships estimated from genome-wide markers. We found a reduction in heritabilities across most traits, and the reduction is stronger in reproductive traits (size and numbers of grains and ears) than vegetative traits. We observed larger depletion in additive genetic variance than dominance genetic variance. Selection intensities during domestication were weak for all traits, with reproductive traits showing the highest values. For 17 of 18 traits, neutral divergence is rejected, suggesting they were targets of selection during domestication. Yield (total grain weight) per plant is the sole trait that selection does not appear to have improved in maize relative to teosinte. From a multivariate evolution perspective, we identified a strong, nonneutral divergence between teosinte and maize landrace genetic variance–covariance matrices (G-matrices). While the structure of G-matrix in teosinte posed considerable genetic constraint on early domestication, the maize landrace G-matrix indicates that the degree of constraint is more unfavorable for further evolution along the same trajectory.",
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author = "Yang, {Chin Jian} and Samayoa, {Luis Fernando} and Bradbury, {Peter J} and Olukolu, {Bode A} and Wei Xue and York, {Alessandra M} and Tuholski, {Michael R} and Weidong Wang and Daskalska, {Lora L} and Neumeyer, {Michael A} and Sanchez-Gonzalez, {Jose de Jesus} and Romay, {Maria Cinta} and Glaubitz, {Jeffrey C} and Qi Sun and Buckler, {Edward S} and Holland, {James B} and Doebley, {John F}",
note = "Copyright {\circledC} 2019 the Author(s). Published by PNAS.",
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doi = "10.1073/pnas.1820997116",
language = "English",
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Yang, CJ, Samayoa, LF, Bradbury, PJ, Olukolu, BA, Xue, W, York, AM, Tuholski, MR, Wang, W, Daskalska, LL, Neumeyer, MA, Sanchez-Gonzalez, JDJ, Romay, MC, Glaubitz, JC, Sun, Q, Buckler, ES, Holland, JB & Doebley, JF 2019, 'The genetic architecture of teosinte catalyzed and constrained maize domestication', Proceedings of the National Academy of Sciences of the United States of America, vol. 116, no. 12, pp. 5643-5652. https://doi.org/10.1073/pnas.1820997116

The genetic architecture of teosinte catalyzed and constrained maize domestication. / Yang, Chin Jian; Samayoa, Luis Fernando; Bradbury, Peter J; Olukolu, Bode A; Xue, Wei; York, Alessandra M; Tuholski, Michael R; Wang, Weidong; Daskalska, Lora L; Neumeyer, Michael A; Sanchez-Gonzalez, Jose de Jesus; Romay, Maria Cinta; Glaubitz, Jeffrey C; Sun, Qi; Buckler, Edward S; Holland, James B; Doebley, John F.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 116, No. 12, 19.03.2019, p. 5643-5652.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - The genetic architecture of teosinte catalyzed and constrained maize domestication

AU - Yang, Chin Jian

AU - Samayoa, Luis Fernando

AU - Bradbury, Peter J

AU - Olukolu, Bode A

AU - Xue, Wei

AU - York, Alessandra M

AU - Tuholski, Michael R

AU - Wang, Weidong

AU - Daskalska, Lora L

AU - Neumeyer, Michael A

AU - Sanchez-Gonzalez, Jose de Jesus

AU - Romay, Maria Cinta

AU - Glaubitz, Jeffrey C

AU - Sun, Qi

AU - Buckler, Edward S

AU - Holland, James B

AU - Doebley, John F

N1 - Copyright © 2019 the Author(s). Published by PNAS.

PY - 2019/3/19

Y1 - 2019/3/19

N2 - The process of evolution under domestication has been studied using phylogenetics, population genetics–genomics, quantitative trait locus (QTL) mapping, gene expression assays, and archaeology. Here, we apply an evolutionary quantitative genetic approach to understand the constraints imposed by the genetic architecture of trait variation in teosinte, the wild ancestor of maize, and the consequences of domestication on genetic architecture. Using modern teosinte and maize landrace populations as proxies for the ancestor and domesticate, respectively, we estimated heritabilities, additive and dominance genetic variances, genetic-by-environment variances, genetic correlations, and genetic covariances for 18 domestication-related traits using realized genomic relationships estimated from genome-wide markers. We found a reduction in heritabilities across most traits, and the reduction is stronger in reproductive traits (size and numbers of grains and ears) than vegetative traits. We observed larger depletion in additive genetic variance than dominance genetic variance. Selection intensities during domestication were weak for all traits, with reproductive traits showing the highest values. For 17 of 18 traits, neutral divergence is rejected, suggesting they were targets of selection during domestication. Yield (total grain weight) per plant is the sole trait that selection does not appear to have improved in maize relative to teosinte. From a multivariate evolution perspective, we identified a strong, nonneutral divergence between teosinte and maize landrace genetic variance–covariance matrices (G-matrices). While the structure of G-matrix in teosinte posed considerable genetic constraint on early domestication, the maize landrace G-matrix indicates that the degree of constraint is more unfavorable for further evolution along the same trajectory.

AB - The process of evolution under domestication has been studied using phylogenetics, population genetics–genomics, quantitative trait locus (QTL) mapping, gene expression assays, and archaeology. Here, we apply an evolutionary quantitative genetic approach to understand the constraints imposed by the genetic architecture of trait variation in teosinte, the wild ancestor of maize, and the consequences of domestication on genetic architecture. Using modern teosinte and maize landrace populations as proxies for the ancestor and domesticate, respectively, we estimated heritabilities, additive and dominance genetic variances, genetic-by-environment variances, genetic correlations, and genetic covariances for 18 domestication-related traits using realized genomic relationships estimated from genome-wide markers. We found a reduction in heritabilities across most traits, and the reduction is stronger in reproductive traits (size and numbers of grains and ears) than vegetative traits. We observed larger depletion in additive genetic variance than dominance genetic variance. Selection intensities during domestication were weak for all traits, with reproductive traits showing the highest values. For 17 of 18 traits, neutral divergence is rejected, suggesting they were targets of selection during domestication. Yield (total grain weight) per plant is the sole trait that selection does not appear to have improved in maize relative to teosinte. From a multivariate evolution perspective, we identified a strong, nonneutral divergence between teosinte and maize landrace genetic variance–covariance matrices (G-matrices). While the structure of G-matrix in teosinte posed considerable genetic constraint on early domestication, the maize landrace G-matrix indicates that the degree of constraint is more unfavorable for further evolution along the same trajectory.

KW - Agriculture

KW - Chromosome Mapping/methods

KW - Chromosomes, Plant/physiology

KW - Domestication

KW - Edible Grain/genetics

KW - Evolution, Molecular

KW - Genetics, Population/methods

KW - Genomics

KW - Phenotype

KW - Plant Proteins/genetics

KW - Quantitative Trait Loci

KW - Selection, Genetic/genetics

KW - Zea mays/genetics

U2 - 10.1073/pnas.1820997116

DO - 10.1073/pnas.1820997116

M3 - Article

VL - 116

SP - 5643

EP - 5652

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 12

ER -