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

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)
October 30, 2017
114 (46) E9999-E10008
Letter
Genome diversity of the potato
Binquan Huang, David M. Spooner, Qiqi Liang
Letter
Reply to Huang et al.: Avoiding “one-size-fits-all” approaches to variant discovery
Michael A. Hardigan, F. Parker E. Laimbeer [...] C. Robin Buell

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.

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Data Availability

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

Acknowledgments

We thank Koichi Sugimoto of the Michigan State University Plant Research Laboratory for kindly providing the tomato plants used to assess circadian rhythm and Joseph Coombs and Walter Amoros for photographs.

Supporting Information

Supporting Information (PDF)
Dataset_S01 (XLSX)
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Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 114 | No. 46
November 14, 2017
PubMed: 29087343

Classifications

Data Availability

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

Submission history

Published online: October 30, 2017
Published in issue: November 14, 2017

Keywords

  1. potato
  2. diversity
  3. domestication
  4. introgression
  5. adaptation

Acknowledgments

We thank Koichi Sugimoto of the Michigan State University Plant Research Laboratory for kindly providing the tomato plants used to assess circadian rhythm and Joseph Coombs and Walter Amoros for photographs.

Notes

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

Authors

Affiliations

Michael A. Hardigan
Department of Plant Biology, Michigan State University, East Lansing, MI 48824;
F. Parker E. Laimbeer
Department of Horticulture, Virginia Polytechnic University and State University, Blacksburg, VA 24061;
Linsey Newton
Department of Plant Biology, Michigan State University, East Lansing, MI 48824;
Emily Crisovan
Department of Plant Biology, Michigan State University, East Lansing, MI 48824;
John P. Hamilton
Department of Plant Biology, Michigan State University, East Lansing, MI 48824;
Brieanne Vaillancourt
Department of Plant Biology, Michigan State University, East Lansing, MI 48824;
Krystle Wiegert-Rininger
Department of Plant Biology, Michigan State University, East Lansing, MI 48824;
Joshua C. Wood
Department of Plant Biology, Michigan State University, East Lansing, MI 48824;
David S. Douches
Department of Plant, Soil, and Microbial Sciences, Michigan State University, East Lansing, MI 48824
Eva M. Farré
Department of Plant Biology, Michigan State University, East Lansing, MI 48824;
Richard E. Veilleux
Department of Horticulture, Virginia Polytechnic University and State University, Blacksburg, VA 24061;
C. Robin Buell1 [email protected]
Department of Plant Biology, Michigan State University, East Lansing, MI 48824;

Notes

1
To whom correspondence should be addressed. Email: [email protected].
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.

Competing Interests

The authors declare no conflict of interest.

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    Genome diversity of tuber-bearing Solanum uncovers complex evolutionary history and targets of domestication in the cultivated potato
    Proceedings of the National Academy of Sciences
    • Vol. 114
    • No. 46
    • pp. 12087-12349

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