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Research Article

Genome diversity of tuber-bearing Solanum uncovers complex evolutionary history and targets of domestication in the cultivated potato

Michael A. Hardigan, F. Parker E. Laimbeer, Linsey Newton, Emily Crisovan, John P. Hamilton, Brieanne Vaillancourt, Krystle Wiegert-Rininger, Joshua C. Wood, David S. Douches, Eva M. Farré, Richard E. Veilleux, and C. Robin Buell
PNAS November 14, 2017 114 (46) E9999-E10008; first published October 30, 2017; https://doi.org/10.1073/pnas.1714380114
Michael A. Hardigan
aDepartment of Plant Biology, Michigan State University, East Lansing, MI 48824;
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F. Parker E. Laimbeer
bDepartment of Horticulture, Virginia Polytechnic University and State University, Blacksburg, VA 24061;
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Linsey Newton
aDepartment of Plant Biology, Michigan State University, East Lansing, MI 48824;
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Emily Crisovan
aDepartment of Plant Biology, Michigan State University, East Lansing, MI 48824;
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John P. Hamilton
aDepartment of Plant Biology, Michigan State University, East Lansing, MI 48824;
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Brieanne Vaillancourt
aDepartment of Plant Biology, Michigan State University, East Lansing, MI 48824;
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Krystle Wiegert-Rininger
aDepartment of Plant Biology, Michigan State University, East Lansing, MI 48824;
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Joshua C. Wood
aDepartment of Plant Biology, Michigan State University, East Lansing, MI 48824;
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David S. Douches
cDepartment of Plant, Soil, and Microbial Sciences, Michigan State University, East Lansing, MI 48824
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Eva M. Farré
aDepartment of Plant Biology, Michigan State University, East Lansing, MI 48824;
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Richard E. Veilleux
bDepartment of Horticulture, Virginia Polytechnic University and State University, Blacksburg, VA 24061;
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C. Robin Buell
aDepartment of Plant Biology, Michigan State University, East Lansing, MI 48824;
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  • For correspondence: buell@msu.edu
  1. Edited by Esther van der Knaap, University of Georgia, and accepted by Editorial Board Member June B. Nasrallah October 5, 2017 (received for review August 21, 2017)

This article has a Letter. Please see:

  • Genome diversity of the potato - June 22, 2018

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Significance

Worldwide, potato is the third most important crop grown for direct human consumption, but breeders have struggled to produce new varieties that outperform those released over a century ago, as evidenced by the most widely grown North American cultivar (Russet Burbank) released in 1876. Despite its importance, potato genetic diversity at the whole-genome level remains largely unexplored. Analysis of cultivated potato and its wild relatives using modern genomics approaches can provide insight into the genomic diversity of extant germplasm, reveal historic introgressions and hybridization events, and identify genes targeted during domestication that control variance for agricultural traits, all critical information to address food security in 21st century agriculture.

Abstract

Cultivated potatoes (Solanum tuberosum L.), domesticated from wild Solanum species native to the Andes of southern Peru, possess a diverse gene pool representing more than 100 tuber-bearing relatives (Solanum section Petota). A diversity panel of wild species, landraces, and cultivars was sequenced to assess genetic variation within tuber-bearing Solanum and the impact of domestication on genome diversity and identify key loci selected for cultivation in North and South America. Sequence diversity of diploid and tetraploid S. tuberosum exceeded any crop resequencing study to date, in part due to expanded wild introgressions following polyploidy that captured alleles outside of their geographic origin. We identified 2,622 genes as under selection, with only 14–16% shared by North American and Andean cultivars, showing that a limited gene set drove early improvement of cultivated potato, while adaptation of upland (S. tuberosum group Andigena) and lowland (S. tuberosum groups Chilotanum and Tuberosum) populations targeted distinct loci. Signatures of selection were uncovered in genes controlling carbohydrate metabolism, glycoalkaloid biosynthesis, the shikimate pathway, the cell cycle, and circadian rhythm. Reduced sexual fertility that accompanied the shift to asexual reproduction in cultivars was reflected by signatures of selection in genes regulating pollen development/gametogenesis. Exploration of haplotype diversity at potato’s maturity locus (StCDF1) revealed introgression of truncated alleles from wild species, particularly S. microdontum in long-day–adapted cultivars. This study uncovers a historic role of wild Solanum species in the diversification of long-day–adapted tetraploid potatoes, showing that extant natural populations represent an essential source of untapped adaptive potential.

  • potato
  • diversity
  • domestication
  • introgression
  • adaptation

Footnotes

  • ↵1To whom correspondence should be addressed. Email: buell{at}msu.edu.
  • Author contributions: M.A.H., D.S.D., and C.R.B. designed research; M.A.H., L.N., E.C., K.W.-R., J.C.W., E.M.F., and C.R.B. performed research; M.A.H., F.P.E.L., E.C., J.P.H., B.V., E.M.F., R.E.V., and C.R.B. analyzed data; and M.A.H., F.P.E.L., E.M.F., R.E.V., and C.R.B. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission. E.v.d.K. is a guest editor invited by the Editorial Board.

  • Data deposition: The data reported in this paper have been deposited in the BioProject database (ID PRJNA378971).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1714380114/-/DCSupplemental.

  • Copyright © 2017 the Author(s). Published by PNAS.

This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

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Potato domestication study
Michael A. Hardigan, F. Parker E. Laimbeer, Linsey Newton, Emily Crisovan, John P. Hamilton, Brieanne Vaillancourt, Krystle Wiegert-Rininger, Joshua C. Wood, David S. Douches, Eva M. Farré, Richard E. Veilleux, C. Robin Buell
Proceedings of the National Academy of Sciences Nov 2017, 114 (46) E9999-E10008; DOI: 10.1073/pnas.1714380114

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Potato domestication study
Michael A. Hardigan, F. Parker E. Laimbeer, Linsey Newton, Emily Crisovan, John P. Hamilton, Brieanne Vaillancourt, Krystle Wiegert-Rininger, Joshua C. Wood, David S. Douches, Eva M. Farré, Richard E. Veilleux, C. Robin Buell
Proceedings of the National Academy of Sciences Nov 2017, 114 (46) E9999-E10008; DOI: 10.1073/pnas.1714380114
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