The genome of the stress-tolerant wild tomato species Solanum pennellii

Journal name:
Nature Genetics
Volume:
46,
Pages:
1034–1038
Year published:
DOI:
doi:10.1038/ng.3046
Received
Accepted
Published online

Solanum pennellii is a wild tomato species endemic to Andean regions in South America, where it has evolved to thrive in arid habitats. Because of its extreme stress tolerance and unusual morphology, it is an important donor of germplasm for the cultivated tomato Solanum lycopersicum1. Introgression lines (ILs) in which large genomic regions of S. lycopersicum are replaced with the corresponding segments from S. pennellii can show remarkably superior agronomic performance2. Here we describe a high-quality genome assembly of the parents of the IL population. By anchoring the S. pennellii genome to the genetic map, we define candidate genes for stress tolerance and provide evidence that transposable elements had a role in the evolution of these traits. Our work paves a path toward further tomato improvement and for deciphering the mechanisms underlying the myriad other agronomic traits that can be improved with S. pennellii germplasm.

At a glance

Figures

  1. Genomic landscape of S. pennellii chromosome 1.
    Figure 1: Genomic landscape of S. pennellii chromosome 1.

    (ad) Densities of genes (a), retrotransposons (b), DNA transposons (c) and simple repeats (d) are shown for a 500-kb window. (e) Average RNA sequencing coverage in a 500-kb window. (fh) Percentages of variants relative to S. pimpinellifolium (f), S. lycopersicum (g) and S. tuberosum (h).

  2. Expression of cuticle biosynthesis-related genes.
    Figure 2: Expression of cuticle biosynthesis–related genes.

    (ad) The expression of genes related to cutin biosynthesis (a) and wax biosynthesis (b) and of genes putatively (c) or known to be (d) associated with the formation of cuticular aromatic components was analyzed using quantitative PCR to validate data from RNA sequencing experiments and biochemical analysis. Statistical analysis was performed using a two-tailed t test. *P < 0.05, **P < 0.01, ***P < 0.001. Gene expression shown is relative to that for actin (Solyc05g054480). Error bars, s.e.m.; four biological replicates, each with three technical replicates.

  3. Chromosome mapping of stress-related candidate genes.
    Figure 3: Chromosome mapping of stress-related candidate genes.

    Candidate genes related to salt stress and drought are visualized on their respective IL QTLs for selected ILs 2-5, 7-4-1, 8-3 and 9-1. Colored squares next to each gene represent the magnitude of differential expression (log2) across a range of different tissues and conditions. Red indicates higher expression in S. pennellii, and blue indicates higher expression in S. lycopersicum. Underlined genes are those characterized by large differences in expression between S. lycopersicum cv. M82 and S. pennellii at the promoter and/or coding sequence level. Large differences are characterized as large (>30-bp) indels in the promoter region and/or at least one significant amino acid change in the coding sequence as determined by the P value predicted by SIFT Blink45. Brix × yield, total agronomic yield.

Accession codes

Primary accessions

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Author information

Affiliations

  1. Department of Metabolic Networks, Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm, Germany.

    • Anthony Bolger,
    • Marie E Bolger,
    • Rainer Schwacke,
    • Malgorzata Ryngajllo,
    • Zhangjun Fei &
    • Björn Usadel
  2. Institute for Biology I, Institute for Botany and Molecular Genetics (IBMG), RWTH Aachen University, Aachen, Germany.

    • Anthony Bolger,
    • Alexander Vogel &
    • Björn Usadel
  3. Department of Molecular Physiology, Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm, Germany.

    • Federico Scossa,
    • Takayuki Tohge,
    • Saleh Alseekh,
    • Sonia Osorio &
    • Alisdair R Fernie
  4. Consiglio per la Ricerca e la Sperimentazione in Agricoltura, Centro di Ricerca per l'Orticoltura, Pontecagnano, Italy.

    • Federico Scossa
  5. Institut für Bio- und Geowissenschaften 2 (IBG-2) Plant Sciences, Forschungszentrum Jülich, Jülich, Germany.

    • Marie E Bolger,
    • Rainer Schwacke &
    • Björn Usadel
  6. Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany.

    • Christa Lanz,
    • Heike Keller,
    • Korbinian Schneeberger,
    • Daniel Koenig &
    • Detlef Weigel
  7. French National Institute for Agricultural Research (INRA), UR1164 Research Unit in Genomics Info (URGI), INRA de Versailles-Grignon, Versailles, France.

    • Florian Maumus &
    • Hadi Quesneville
  8. Department of Plant Biology, Cornell University, Ithaca, New York, USA.

    • Iben Sørensen,
    • Eric A Fich &
    • Jocelyn K C Rose
  9. Instituto de Biotecnología, Centro de Investigación en Ciencias Veterinarias y Agronómicas (CICVyA)–Instituto Nacional de Tecnología Agropecuaria (INTA) and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Castelar, Argentina.

    • Gabriel Lichtenstein,
    • Mariana Conte &
    • Fernando Carrari
  10. Department of Plant Developmental Biology, Max Planck Institute for Plant Breeding Research, Cologne, Germany.

    • Korbinian Schneeberger
  11. Faculty of Agriculture, Hebrew University of Jerusalem, Rehovot, Israel.

    • Itai Ofner &
    • Dani Zamir
  12. Boyce Thompson Institute for Plant Research, Cornell University, Ithaca, New York, USA.

    • Julia Vrebalov,
    • Yimin Xu,
    • Linyong Mao,
    • Zhangjun Fei &
    • James J Giovannoni
  13. Instituto de Hortofruticultura Subtropical y Mediterránea 'La Mayora', Department of Molecular Biology and Biochemistry, University of Málaga, Málaga, Spain.

    • Sonia Osorio
  14. Plant Research International, Wageningen University and Research Centre, Wageningen, the Netherlands.

    • Saulo Alves Aflitos,
    • Elio Schijlen,
    • Roeland C H J van Ham &
    • René Klein Lankhorst
  15. Department of Plant Breeding and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany.

    • José M Jiménez-Goméz
  16. INRA, UMR 1318, Institut Jean-Pierre Bourgin, Versailles, France.

    • José M Jiménez-Goméz
  17. Department of Plant Biology, University of California, Davis, Davis, California, USA.

    • Seisuke Kimura,
    • Ravi Kumar,
    • Daniel Koenig,
    • Lauren R Headland,
    • Julin N Maloof &
    • Neelima Sinha
  18. Entwicklungs und Molekularbiologie der Pflanzen, Heinrich Heine Universität, Düsseldorf, Germany.

    • Borjana Arsova
  19. Institute for Biology I, Unit of Plant Molecular Cell Biology, RWTH Aachen University, Aachen, Germany.

    • Ralph Panstruga
  20. US Department of Agriculture Robert W. Holley Centre for Agriculture and Health, Ithaca, New York, USA

    • Zhangjun Fei &
    • James J Giovannoni
  21. Present address: Keygene, Wageningen, the Netherlands.

    • Roeland C H J van Ham

Contributions

A.B., B.U. and A.R.F. managed the project. A.B., F.S., M.E.B., F.M., T.T., K.S., R.S., I.O., J.N.M., N.S., Z.F., J.K.C.R., D.Z., F.C., J.J.G., D.W., B.U. and A.R.F. designed the analysis. F.S., M.E.B., H.K., C.L., M.C., Y.X., S.A.A., M.R., B.U. and A.V. conducted DNA and RNA preparation and sequencing. C.L., J.M.J.-G., S.K., J.V., E.S., R.K., D.K., L.R.H., R.C.H.J.v.H., R.K.L., R.P., D.W. contributed new reagents and analytical tools. A.B., F.S., G.L., F.M., R.S., B.U. and A.R.F. conducted the data analyses. H.Q., S.A., I.S., E.A.F., S.O., L.M. and B.A. identified and evaluated candidate genes. B.U., A.B., M.E.B., F.S., D.W., F.M., J.K.C.R. and A.R.F. wrote the manuscript with help from all authors.

Competing financial interests

D.Z. is a cofounder of the company Phenom Networks, which develops phenotype bioinformatics tools.

Corresponding author

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Supplementary information

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