Aluminum tolerance in maize is associated with higher MATE1 gene copy number

Lyza G. Maron, Claudia T. Guimarães, Matias Kirst, Patrice S. Albert, James A. Birchler, Peter J. Bradbury, Edward S. Buckler, Alison E. Coluccio, Tatiana V. Danilova, David A Kudrna, Jurandir V. Magalhaes, Miguel A. Piñeros, Michael C. Schatz, Rod A Wing, Leon V. Kochian

Research output: Contribution to journalArticle

140 Citations (Scopus)

Abstract

Genome structure variation, including copy number variation and presence/absence variation, comprises a large extent of maize genetic diversity; however, its effect on phenotypes remains largely unexplored. Here, we describe how copy number variation underlies a rare allele that contributes to maize aluminum (Al) tolerance. Al toxicity is the primary limitation for crop production on acid soils, which make up 50% of the world's potentially arable lands. In a recombinant inbred linemapping population, copy number variation of the Al tolerance gene multidrug and toxic compound extrusion 1 (MATE1) is the basis for the quantitative trait locus of largest effect on phenotypic variation. This expansion in MATE1 copy number is associated with higher MATE1 expression, which in turn results in superior Al tolerance. The three MATE1 copies are identical and are part of a tandem triplication. Only three maize inbred lines carrying the three-copy allele were identified from maize and teosinte diversity panels, indicating that copy number variation for MATE1 is a rare, and quite likely recent, event. These maize lines with higher MATE1 copy number are also Al-tolerant, have high MATE1 expression, and originate from regions of highly acidic soils. Our findings show a role for copy number variation in the adaptation of maize to acidic soils in the tropics and suggest that genome structural changes may be a rapid evolutionary response to new environments.

Original languageEnglish (US)
Pages (from-to)5241-5246
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume110
Issue number13
DOIs
StatePublished - Mar 26 2013

Fingerprint

Gene Dosage
Poisons
Aluminum
Zea mays
Soil
Alleles
Genome
Quantitative Trait Loci
Phenotype
Acids
Population
Genes

Keywords

  • Abiotic stress
  • Selection

ASJC Scopus subject areas

  • General

Cite this

Maron, L. G., Guimarães, C. T., Kirst, M., Albert, P. S., Birchler, J. A., Bradbury, P. J., ... Kochian, L. V. (2013). Aluminum tolerance in maize is associated with higher MATE1 gene copy number. Proceedings of the National Academy of Sciences of the United States of America, 110(13), 5241-5246. https://doi.org/10.1073/pnas.1220766110

Aluminum tolerance in maize is associated with higher MATE1 gene copy number. / Maron, Lyza G.; Guimarães, Claudia T.; Kirst, Matias; Albert, Patrice S.; Birchler, James A.; Bradbury, Peter J.; Buckler, Edward S.; Coluccio, Alison E.; Danilova, Tatiana V.; Kudrna, David A; Magalhaes, Jurandir V.; Piñeros, Miguel A.; Schatz, Michael C.; Wing, Rod A; Kochian, Leon V.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 110, No. 13, 26.03.2013, p. 5241-5246.

Research output: Contribution to journalArticle

Maron, LG, Guimarães, CT, Kirst, M, Albert, PS, Birchler, JA, Bradbury, PJ, Buckler, ES, Coluccio, AE, Danilova, TV, Kudrna, DA, Magalhaes, JV, Piñeros, MA, Schatz, MC, Wing, RA & Kochian, LV 2013, 'Aluminum tolerance in maize is associated with higher MATE1 gene copy number', Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 13, pp. 5241-5246. https://doi.org/10.1073/pnas.1220766110
Maron, Lyza G. ; Guimarães, Claudia T. ; Kirst, Matias ; Albert, Patrice S. ; Birchler, James A. ; Bradbury, Peter J. ; Buckler, Edward S. ; Coluccio, Alison E. ; Danilova, Tatiana V. ; Kudrna, David A ; Magalhaes, Jurandir V. ; Piñeros, Miguel A. ; Schatz, Michael C. ; Wing, Rod A ; Kochian, Leon V. / Aluminum tolerance in maize is associated with higher MATE1 gene copy number. In: Proceedings of the National Academy of Sciences of the United States of America. 2013 ; Vol. 110, No. 13. pp. 5241-5246.
@article{05d3aeaf811f4d4cb7185b704b313e20,
title = "Aluminum tolerance in maize is associated with higher MATE1 gene copy number",
abstract = "Genome structure variation, including copy number variation and presence/absence variation, comprises a large extent of maize genetic diversity; however, its effect on phenotypes remains largely unexplored. Here, we describe how copy number variation underlies a rare allele that contributes to maize aluminum (Al) tolerance. Al toxicity is the primary limitation for crop production on acid soils, which make up 50{\%} of the world's potentially arable lands. In a recombinant inbred linemapping population, copy number variation of the Al tolerance gene multidrug and toxic compound extrusion 1 (MATE1) is the basis for the quantitative trait locus of largest effect on phenotypic variation. This expansion in MATE1 copy number is associated with higher MATE1 expression, which in turn results in superior Al tolerance. The three MATE1 copies are identical and are part of a tandem triplication. Only three maize inbred lines carrying the three-copy allele were identified from maize and teosinte diversity panels, indicating that copy number variation for MATE1 is a rare, and quite likely recent, event. These maize lines with higher MATE1 copy number are also Al-tolerant, have high MATE1 expression, and originate from regions of highly acidic soils. Our findings show a role for copy number variation in the adaptation of maize to acidic soils in the tropics and suggest that genome structural changes may be a rapid evolutionary response to new environments.",
keywords = "Abiotic stress, Selection",
author = "Maron, {Lyza G.} and Guimar{\~a}es, {Claudia T.} and Matias Kirst and Albert, {Patrice S.} and Birchler, {James A.} and Bradbury, {Peter J.} and Buckler, {Edward S.} and Coluccio, {Alison E.} and Danilova, {Tatiana V.} and Kudrna, {David A} and Magalhaes, {Jurandir V.} and Pi{\~n}eros, {Miguel A.} and Schatz, {Michael C.} and Wing, {Rod A} and Kochian, {Leon V.}",
year = "2013",
month = "3",
day = "26",
doi = "10.1073/pnas.1220766110",
language = "English (US)",
volume = "110",
pages = "5241--5246",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "13",

}

TY - JOUR

T1 - Aluminum tolerance in maize is associated with higher MATE1 gene copy number

AU - Maron, Lyza G.

AU - Guimarães, Claudia T.

AU - Kirst, Matias

AU - Albert, Patrice S.

AU - Birchler, James A.

AU - Bradbury, Peter J.

AU - Buckler, Edward S.

AU - Coluccio, Alison E.

AU - Danilova, Tatiana V.

AU - Kudrna, David A

AU - Magalhaes, Jurandir V.

AU - Piñeros, Miguel A.

AU - Schatz, Michael C.

AU - Wing, Rod A

AU - Kochian, Leon V.

PY - 2013/3/26

Y1 - 2013/3/26

N2 - Genome structure variation, including copy number variation and presence/absence variation, comprises a large extent of maize genetic diversity; however, its effect on phenotypes remains largely unexplored. Here, we describe how copy number variation underlies a rare allele that contributes to maize aluminum (Al) tolerance. Al toxicity is the primary limitation for crop production on acid soils, which make up 50% of the world's potentially arable lands. In a recombinant inbred linemapping population, copy number variation of the Al tolerance gene multidrug and toxic compound extrusion 1 (MATE1) is the basis for the quantitative trait locus of largest effect on phenotypic variation. This expansion in MATE1 copy number is associated with higher MATE1 expression, which in turn results in superior Al tolerance. The three MATE1 copies are identical and are part of a tandem triplication. Only three maize inbred lines carrying the three-copy allele were identified from maize and teosinte diversity panels, indicating that copy number variation for MATE1 is a rare, and quite likely recent, event. These maize lines with higher MATE1 copy number are also Al-tolerant, have high MATE1 expression, and originate from regions of highly acidic soils. Our findings show a role for copy number variation in the adaptation of maize to acidic soils in the tropics and suggest that genome structural changes may be a rapid evolutionary response to new environments.

AB - Genome structure variation, including copy number variation and presence/absence variation, comprises a large extent of maize genetic diversity; however, its effect on phenotypes remains largely unexplored. Here, we describe how copy number variation underlies a rare allele that contributes to maize aluminum (Al) tolerance. Al toxicity is the primary limitation for crop production on acid soils, which make up 50% of the world's potentially arable lands. In a recombinant inbred linemapping population, copy number variation of the Al tolerance gene multidrug and toxic compound extrusion 1 (MATE1) is the basis for the quantitative trait locus of largest effect on phenotypic variation. This expansion in MATE1 copy number is associated with higher MATE1 expression, which in turn results in superior Al tolerance. The three MATE1 copies are identical and are part of a tandem triplication. Only three maize inbred lines carrying the three-copy allele were identified from maize and teosinte diversity panels, indicating that copy number variation for MATE1 is a rare, and quite likely recent, event. These maize lines with higher MATE1 copy number are also Al-tolerant, have high MATE1 expression, and originate from regions of highly acidic soils. Our findings show a role for copy number variation in the adaptation of maize to acidic soils in the tropics and suggest that genome structural changes may be a rapid evolutionary response to new environments.

KW - Abiotic stress

KW - Selection

UR - http://www.scopus.com/inward/record.url?scp=84875508685&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84875508685&partnerID=8YFLogxK

U2 - 10.1073/pnas.1220766110

DO - 10.1073/pnas.1220766110

M3 - Article

C2 - 23479633

AN - SCOPUS:84875508685

VL - 110

SP - 5241

EP - 5246

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 - 13

ER -