Genome sequence and analysis of the tuber crop potato

Journal name:
Nature
Volume:
475,
Pages:
189–195
Date published:
DOI:
doi:10.1038/nature10158
Received
Accepted
Published online

Abstract

Potato (Solanum tuberosum L.) is the world’s most important non-grain food crop and is central to global food security. It is clonally propagated, highly heterozygous, autotetraploid, and suffers acute inbreeding depression. Here we use a homozygous doubled-monoploid potato clone to sequence and assemble 86% of the 844-megabase genome. We predict 39,031 protein-coding genes and present evidence for at least two genome duplication events indicative of a palaeopolyploid origin. As the first genome sequence of an asterid, the potato genome reveals 2,642 genes specific to this large angiosperm clade. We also sequenced a heterozygous diploid clone and show that gene presence/absence variants and other potentially deleterious mutations occur frequently and are a likely cause of inbreeding depression. Gene family expansion, tissue-specific expression and recruitment of genes to new pathways contributed to the evolution of tuber development. The potato genome sequence provides a platform for genetic improvement of this vital crop.

At a glance

Figures

  1. The potato genome.
    Figure 1: The potato genome.

    a, Ideograms of the 12 pseudochromosomes of potato (in Mb scales). Each of the 12 pachytene chromosomes from DM was digitally aligned with the ideogram (the amount of DNA in each unit of the pachytene chromosomes is not in proportion to the scales of the pseudochromosomes). b, Gene density represented as number of genes per Mb (non-overlapping, window size = 1Mb). c, Percentage of coverage of repetitive sequences (non-overlapping windows, window size = 1Mb). d, Transcription state. The transcription level for each gene was estimated by averaging the fragments per kb exon model per million mapped reads (FPKM) from different tissues in non-overlapping 1-Mb windows. e, GC content was estimated by the per cent G+C in 1-Mb non-overlapping windows. f, Distribution of the subtelomeric repeat sequence CL14_cons.

  2. Comparative analyses and evolution of the potato genome.
    Figure 2: Comparative analyses and evolution of the potato genome.

    a, Clusters of orthologous and paralogous gene families in 12 plant species as identified by OrthoMCL33. Gene family number is listed in each of the components; the number of genes within the families for all of the species within the component is noted within parentheses. b, Genome duplication in dicot genomes as revealed through 4DTv analyses. c, Syntenic blocks between A. thaliana, potato, and V. vinifera (grape) demonstrating a high degree of conserved gene order between these taxa.

  3. Haplotype diversity and inbreeding depression.
    Figure 3: Haplotype diversity and inbreeding depression.

    a, Plants and tubers of DM and RH showing that RH has greater vigour. b, Illumina K-mer volume histograms of DM and RH. The volume of K-mers (y-axis) is plotted against the frequency at which they occur (x-axis). The leftmost truncated peaks at low frequency and high volume represent K-mers containing essentially random sequencing errors, whereas the distribution to the right represents proper (putatively error-free) data. In contrast to the single modality of DM, RH exhibits clear bi-modality caused by heterozygosity. c, Genomic distribution of premature stop, frameshift and presence/absence variation mutations contributing to inbreeding depression. The hypothetical RH pseudomolecules were solely inferred from the corresponding DM ones. Owing to the inability to assign heterozygous PS and FS of RH to a definite haplotype, all heterozygous PS and FS were arbitrarily mapped to the left haplotype of RH. d, A zoom-in comparative view of the DM and RH genomes. The left and right alignments are derived from the euchromatic and heterochromatic regions of chromosome 5, respectively. Most of the gene annotations, including PS and RH-specific genes, are supported by transcript data.

  4. Gene expression of selected tissues and genes.
    Figure 4: Gene expression of selected tissues and genes.

    a, KTI gene organization across the potato genome. Black arrows indicate the location of individual genes on six scaffolds located on four chromosomes. b, Phylogenetic tree and KTI gene expression heat map. The KTI genes were clustered using all potato and tomato genes available with the Populus KTI gene as an out-group. The tissue specificity of individual members of the highly expanded potato gene family is shown in the heat map. Expression levels are indicated by shades of red, where white indicates no expression or lack of data for tomato and poplar. c, A model of starch synthesis showing enzyme activities is shown on the left. AGPase, ADP-glucose pyrophosphorylase; F16BP, fructose-1,6-biphosphatase; HexK, hexokinase; INV, invertase; PFK, phosphofructokinase; PFPP, pyrophosphate-fructose-6-phosphate-1-phosphotransferase; PGI, phosphoglucose isomerase; PGM, phosphoglucomutase; SBE, starch branching enzyme; SP, starch phosphorylase; SPP, sucrose phosphate phosphatase; SS, starch synthase; SuSy, sucrose synthase; SUPS, sucrose phosphate synthase; UDP-GPP, UDP-glucose pyrophosphorylase. The grey background denotes substrate (sucrose) and product (starch) and the red background indicates genes that are specifically upregulated in RH versus DM. On the right, a heat map of the genes involved in carbohydrate metabolism is shown. ADP-glucose pyrophosphorylase large subunit,AGPase (l); ADP-glucose pyrophosphorylase small subunit,AGPase (s); ADP-glucose pyrophosphorylase small subunit 3,AGPase 3 (s); cytosolic fructose-1,6-biphosphatase,F16BP (c); granule bound starch synthase,GBSS; leaf type L starch phosphorylase,Leaf type SP; plastidic phosphoglucomutase,pPGM; starch branching enzyme II,SBE II; soluble starch synthase,SSS; starch synthase V,SSV; three variants of plastidic aldolase,PA.

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Author information

Affiliations

  1. BGI-Shenzhen, Chinese Ministry of Agricultural, Key Lab of Genomics, Beishan Industrial Zone, Yantian District, Shenzhen 518083, China.

    • Xun Xu,
    • Shengkai Pan,
    • Shifeng Cheng,
    • Bo Zhang,
    • Desheng Mu,
    • Peixiang Ni,
    • Gengyun Zhang,
    • Shuang Yang (Principal Investigator),
    • Ruiqiang Li (Principal Investigator) &
    • Jun Wang (Principal Investigator)
  2. Cayetano Heredia University, Genomics Research Unit, Av Honorio Delgado 430, Lima 31, Peru and San Cristobal of Huamanga University, Biotechnology and Plant Genetics Laboratory, Ayacucho, Peru.

    • Gisella Orjeda (Principal Investigator),
    • Frank Guzman,
    • Michael Torres,
    • Roberto Lozano,
    • Olga Ponce,
    • Diana Martinez &
    • Germán De la Cruz
  3. Central Potato Research Institute, Shimla 171001, Himachal Pradesh, India.

    • S. K. Chakrabarti (Principal Investigator) &
    • Virupaksh U. Patil
  4. Centre Bioengineering RAS, Prospekt 60-letya Oktyabrya, 7-1, Moscow 117312, Russia.

    • Konstantin G. Skryabin (Principal Investigator),
    • Boris B. Kuznetsov,
    • Nikolai V. Ravin,
    • Tatjana V. Kolganova,
    • Alexey V. Beletsky &
    • Andrei V. Mardanov
  5. Center for Genome Regulation and Center for Mathematical Modeling, Universidad de Chile (UMI 2807 CNRS), Chile.

    • Alex Di Genova
  6. College of Life Sciences, University of Dundee, Dow Street, Dundee DD1 5EH, UK.

    • Daniel M. Bolser &
    • David M. A. Martin (Principal Investigator)
  7. High Technology Research Center, Shandong Academy of Agricultural Sciences, 11 Sangyuan Road, Jinan 250100, P. R. China.

    • Guangcun Li &
    • Yu Yang
  8. Huazhong Agriculture University, Ministry of Education, College of Horticulture and Forestry, Department of Vegetable Crops, Key Laboratory of Horticulture Biology, Wuhan 430070, P. R. China.

    • Hanhui Kuang &
    • Qun Hu
  9. Hunan Agricultural University, College of Horticulture and Landscape, Changsha, Hunan 410128, China.

    • Xingyao Xiong
  10. Imperial College London, Division of Biology, South Kensington Campus, London SW7 1AZ, UK.

    • Gerard J. Bishop
  11. Instituto de Investigaciones Agropecuarias, Avda. Salamanca s/n, Km 105 ruta 5 sur, sector Los Choapinos. Rengo, Región del Libertador Bernardo O’Higgins, Código Postal 2940000, Chile.

    • Boris Sagredo (Principal Investigator) &
    • Nilo Mejía
  12. Institute of Biochemistry and Biophysics, DNA Sequencing and Oligonucleotides Synthesis Laboratory, PAS ul. Pawinskiego 5a, 02-106 Warsaw, Poland.

    • Wlodzimierz Zagorski (Principal Investigator),
    • Robert Gromadka,
    • Jan Gawor &
    • Pawel Szczesny
  13. Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Key Laboratory of Horticultural Crops Genetic Improvement of Ministry of Agriculture, Sino-Dutch Joint Lab of Horticultural Genomics Technology, Beijing 100081, China.

    • Sanwen Huang (Principal Investigator),
    • Zhonghua Zhang,
    • Chunbo Liang,
    • Jun He,
    • Ying Li,
    • Ying He,
    • Jianfei Xu,
    • Youjun Zhang,
    • Binyan Xie,
    • Yongchen Du &
    • Dongyu Qu (Principal Investigator)
  14. International Potato Center, P.O. Box 1558, Lima 12, Peru.

    • Merideth Bonierbale,
    • Marc Ghislain &
    • Maria del Rosario Herrera
  15. Italian National Agency for New Technologies, Energy and Sustainable Development (ENEA), Casaccia Research Center, Via Anguillarese 301, 00123 Roma, Italy and Trisaia Research Center, S.S. 106 Ionica - Km 419,50 75026 Rotondella (Matera), Italy.

    • Giovanni Giuliano (Principal Investigator),
    • Marco Pietrella,
    • Gaetano Perrotta &
    • Paolo Facella
  16. J Craig Venter Institute, 9712 Medical Center Dr, Rockville, Maryland 20850, USA.

    • Kimberly O’Brien
  17. Laboratorio de Agrobiotecnología, Estación Experimental Agropecuaria Balcarce, Instituto Nacional de Tecnología Agropecuaria (INTA) cc276 (7620) Balcarce, Argentina.

    • Sergio E. Feingold (Principal Investigator),
    • Leandro E. Barreiro &
    • Gabriela A. Massa
  18. Laboratorio de Biología de Sistemas, CREG, Universidad Nacional de LaPlata, 1888, Argentina.

    • Luis Diambra
  19. Michigan State University, East Lansing, Michigan 48824, USA.

    • Brett R. Whitty,
    • Brieanne Vaillancourt,
    • Haining Lin,
    • Alicia N. Massa,
    • Michael Geoffroy,
    • Steven Lundback,
    • Dean DellaPenna &
    • C. Robin Buell (Principal Investigator)
  20. Scottish Crop Research Institute, Genetics Programme, Invergowrie, Dundee DD2 5DA, UK.

    • Sanjeev Kumar Sharma,
    • David F. Marshall,
    • Robbie Waugh &
    • Glenn J. Bryan (Principal Investigator)
  21. Teagasc Crops Research Centre, Oak Park, Carlow, Ireland.

    • Marialaura Destefanis,
    • Istvan Nagy &
    • Dan Milbourne (Principal Investigator)
  22. The New Zealand Institute for Plant & Food Research Ltd., Private Bag 4704, Christchurch 8140, New Zealand.

    • Susan J. Thomson,
    • Mark Fiers &
    • Jeanne M. E. Jacobs (Principal Investigator)
  23. University of Aalborg (AAU), Department of Biotechnology, Chemistry and Environmental Engineering, Sohngaardsholmsvej 49, 9000 Aalborg, Denmark.

    • Kåre L. Nielsen (Principal Investigator) &
    • Mads Sønderkær
  24. University of Wisconsin-Madison, Department of Horticulture, 1575 Linden Drive, Madison, Wisconsin 53706, USA.

    • Marina Iovene,
    • Giovana A. Torres &
    • Jiming Jiang (Principal Investigator)
  25. Virginia Polytechnic Institute and State University, Department of Horticulture, 544 Latham Hall, Blacksburg, Virginia 24061, USA.

    • Richard E. Veilleux
  26. Wageningen University and Research Centre, Dept. of Plant Sciences, Laboratory of Plant Breeding, Droevendaalsesteeg 1, 6708PB Wageningen, Netherlands.

    • Christian W. B. Bachem (Principal Investigator),
    • Jan de Boer,
    • Theo Borm,
    • Bjorn Kloosterman,
    • Herman van Eck &
    • Richard G. F. Visser
  27. Wageningen University and Research Centre, Applied Bioinformatics, Plant Research International, Droevendaalsesteeg 1, 6708PB Wageningen, Netherlands.

    • Erwin Datema,
    • Bas te Lintel Hekkert &
    • Roeland C. H. J. van Ham
  28. Centre for BioSystems Genomics, Droevendaalsesteeg 1, 6708PB Wageningen, Netherlands.

    • Aska Goverse,
    • Roeland C. H. J. van Ham &
    • Richard G. F. Visser
  29. Wageningen University and Research Centre, Dept. of Plant Sciences, Laboratory of Nematology, Droevendaalsesteeg 1, 6708PB Wageningen, Netherlands.

    • Aska Goverse
  30. Present address: The James Hutton Institute, Invergowrie, Dundee, DD2 5DA, UK (S.K.S., D.F.M., R.W., G.J. Bryan).

    • Sanjeev Kumar Sharma,
    • David F. Marshall,
    • Robbie Waugh &
    • Glenn J. Bryan (Principal Investigator)

Consortia

  1. The Potato Genome Sequencing Consortium

  2. The Potato Genome Consortium (Participants are listed alphabetically by institution.)

  3. BGI-Shenzhen

    • Xun Xu,
    • Shengkai Pan,
    • Shifeng Cheng,
    • Bo Zhang,
    • Desheng Mu,
    • Peixiang Ni,
    • Gengyun Zhang,
    • Shuang Yang (Principal Investigator),
    • Ruiqiang Li (Principal Investigator) &
    • Jun Wang (Principal Investigator)
  4. Cayetano Heredia University

    • Gisella Orjeda (Principal Investigator),
    • Frank Guzman,
    • Michael Torres,
    • Roberto Lozano,
    • Olga Ponce,
    • Diana Martinez &
    • Germán De la Cruz
  5. Central Potato Research Institute

    • S. K. Chakrabarti (Principal Investigator) &
    • Virupaksh U. Patil
  6. Centre Bioengineering RAS

    • Konstantin G. Skryabin (Principal Investigator),
    • Boris B. Kuznetsov,
    • Nikolai V. Ravin,
    • Tatjana V. Kolganova,
    • Alexey V. Beletsky &
    • Andrei V. Mardanov
  7. CGR-CMM, Universidad de Chile

    • Alex Di Genova
  8. College of Life Sciences, University of Dundee

    • Daniel M. Bolser &
    • David M. A. Martin (Principal Investigator)
  9. High Technology Research Center, Shandong Academy of Agricultural Sciences

    • Guangcun Li &
    • Yu Yang
  10. Huazhong Agriculture University

    • Hanhui Kuang &
    • Qun Hu
  11. Hunan Agricultural University

    • Xingyao Xiong
  12. Imperial College London

    • Gerard J. Bishop
  13. Instituto de Investigaciones Agropecuarias

    • Boris Sagredo (Principal Investigator) &
    • Nilo Mejía
  14. Institute of Biochemistry & Biophysics

    • Wlodzimierz Zagorski (Principal Investigator),
    • Robert Gromadka,
    • Jan Gawor &
    • Pawel Szczesny
  15. Institute of Vegetables & Flowers, Chinese Academy of Agricultural Sciences

    • Sanwen Huang (Principal Investigator),
    • Zhonghua Zhang,
    • Chunbo Liang,
    • Jun He,
    • Ying Li,
    • Ying He,
    • Jianfei Xu,
    • Youjun Zhang,
    • Binyan Xie,
    • Yongchen Du &
    • Dongyu Qu (Principal Investigator)
  16. International Potato Center

    • Merideth Bonierbale,
    • Marc Ghislain &
    • Maria del Rosario Herrera
  17. Italian National Agency for New Technologies, Energy & Sustainable Development

    • Giovanni Giuliano (Principal Investigator),
    • Marco Pietrella,
    • Gaetano Perrotta &
    • Paolo Facella
  18. J Craig Venter Institute

    • Kimberly O’Brien
  19. Laboratorio de Agrobiotecnología, Instituto Nacional de Tecnología Agropecuaria

    • Sergio E. Feingold (Principal Investigator),
    • Leandro E. Barreiro &
    • Gabriela A. Massa
  20. Laboratorio de Biología de Sistemas, Universidad Nacional de LaPlata

    • Luis Diambra
  21. Michigan State University

    • Brett R. Whitty,
    • Brieanne Vaillancourt,
    • Haining Lin,
    • Alicia N. Massa,
    • Michael Geoffroy,
    • Steven Lundback,
    • Dean DellaPenna &
    • C. Robin Buell (Principal Investigator)
  22. Scottish Crop Research Institute

    • Sanjeev Kumar Sharma,
    • David F. Marshall,
    • Robbie Waugh &
    • Glenn J. Bryan (Principal Investigator)
  23. Teagasc Crops Research Centre

    • Marialaura Destefanis,
    • Istvan Nagy &
    • Dan Milbourne (Principal Investigator)
  24. The New Zealand Institute for Plant & Food Research Ltd

    • Susan J. Thomson,
    • Mark Fiers &
    • Jeanne M. E. Jacobs (Principal Investigator)
  25. University of Aalborg

    • Kåre L. Nielsen (Principal Investigator) &
    • Mads Sønderkær
  26. University of Wisconsin

    • Marina Iovene,
    • Giovana A. Torres &
    • Jiming Jiang (Principal Investigator)
  27. Virginia Polytechnic Institute & State University

    • Richard E. Veilleux
  28. Wageningen University & Research Centre

    • Christian W. B. Bachem (Principal Investigator),
    • Jan de Boer,
    • Theo Borm,
    • Bjorn Kloosterman,
    • Herman van Eck,
    • Erwin Datema,
    • Bas te Lintel Hekkert,
    • Aska Goverse,
    • Roeland C. H. J. van Ham &
    • Richard G. F. Visser

Contributions

A.D.G., A.G., A.N.M., A.V.B., A.V.M., B.B.K., B.K., B.R.W., B.S., B.t.L.H., B.V., B.X., B.Z., C.L., C.R.B., C.W.B.B., D.F.M., D. Martinez, D. Milbourne, D.M.A.M., D.M.B., D.D., D.M., E.D., F.G., G.A.M., G.A.T., G.D.l.C., G.G., G.J. Bishop, G.J. Bryan, G.L., G.O., G.P., G.Z., H.K., H.L., H.v.E., I.N., J.d.B., J.G., J.H., J.J., J.M.E.J., J.W., J.X., K.L.N., K.O’B., L.D., L.E.B., M.B., M.D., M.d.R.H., M.F., M. Geoffroy, M.Ghislain, M.I., M.P., M.S., M.T., N.M., N.V.R., O.P., P.F., P.N., P.S., Q.H., R.C.H.J.v.H., R.E.V., R.G., R.G.F.V., R. Lozano, R. Li, S.C., S.E.F., S.H., S.J.T., S.K.C., S.K.S., S.L., S.P., S.Y., T.B., T.V.K., V.U.P., X. Xiong, X. Xu, Y.D., Y.H., Y.L., Y.Y., Y.Z. and Z.Z. were involved in experimental design, data generation and/or data analysis. A.N.M., B.K., C.R.B., C.W.B.B., D.D., D. Milbourne, D.M.A.M., D.M.B., E.D., G.G., G.J. Bishop, G.J. Bryan, G.O., H.L., I.N., J.d.B., J.J., J.M.E.J., K.L.N., M.B., M.F., M.D., M.S., O.P., R.C.H.J.v.H., R.E.V., R.G.F.V., R. Lozano, R.W., S.E.F., S.H., S.J.T., S.K.S., T.B. and X. Xu wrote the manuscript. B.S., C.R.B., C.W.B.B., D.F.M., D. Milbourne, D.M.A.M., D.Q., G.G., G.J. Bishop, G.J. Bryan, G.O., G.P., J.M.E.J., J.W., K.G.S., R.G.F.V., R. Li, R.W., S.E.F., S.H., S.K.C., S.Y., W.Z. and Y.D. supervised data generation/analysis and managed the project. C.R.B., C.W.B.B., G.J. Bryan, G.O., J.M.E.J. and S.H. are members of The Potato Genome Sequencing Consortium Steering Committee.

Competing financial interests

The authors declare no competing financial interests.

BAC and fosmid end sequences have been deposited in the GSS division of GenBank (BAC: GS025503–GS026177, GS262924–GS365942, GS504213–GS557003; fosmid: FI900795–FI901529, FI907952–FI927051, GS557234–GS594339, GS635316–GS765761). DM Illumina GA2 WGS and Roche 454 sequences have been deposited in the NCBI Sequence Read Archive (SRA029323) and EBI Short Read Archive (ERP000411) respectively. RH NGS sequences have been deposited in the EBI Short Read Archive (ERP000627). DM and RH RNA-Seq reads have been deposited in the NCBI Sequence Read Archive (SRA030516; study SRP005965) and the European Nucleotide Database ArrayExpress Database (E-MTAB-552; study ERP000527), respectively. The DM Whole Genome Shotgun project has been deposited at DDBJ/EMBL/GenBank under the accession AEWC00000000. The version described in this paper is the First Version, AEWC01000000. Genome sequence and annotation can be obtained and viewed at http://potatogenome.net.

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    Supplementary information

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    1. Supplementary Information (20.2 MB)

      The file contains Supplementary Text, Supplementary Figures 1-15 with legends and Supplementary Tables 1-18 and 20-34. This is a 500-page document and may take a short while to download. This file was replaced on 9 May 2014 as Supplementary Figure 12 was corrupted.

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    1. Supplementary Tables (12.4 MB)

      The zipped file contains two Supplementary Tables:
      Supplementary Table 19A displaying FPKM levels in DM tissues.
      Supplementary Table 19B displaying FPKM levels in RH tissues.

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