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Low number of fixed somatic mutations in a long-lived oak tree

Nature Plants volume 3, pages 926–929 (2017)Cite this article

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Abstract

Because plants do not possess a defined germline, deleterious somatic mutations can be passed to gametes, and a large number of cell divisions separating zygote from gamete formation may lead to many mutations in long-lived plants. We sequenced the genome of two terminal branches of a 234-year-old oak tree and found several fixed somatic single-nucleotide variants whose sequential appearance in the tree could be traced along nested sectors of younger branches. Our data suggest that stem cells of shoot meristems in trees are robustly protected from the accumulation of mutations.

To identify fixed somatic variants (those present in an entire sector of the Napoleon Oak) and to reconstruct their origin and distribution among branches, we collected 26 leaf samples from different locations on the tree. We first sequenced the genome from leaves sampled on terminal ramets of one lower and one upper branch of the tree. We then used a combination of short-read Illumina and single-molecule real-time (SMRT, Pacific Biosciences) sequencing to generate a de novo assembly of the oak genome. After removing contigs <1,000 bp, we established a draft sequence of approximately 720 megabases (Mb) at a coverage of approximately 70×, with 85,557 scaffolds and the minimum length to cover 50% of the genome (N50) of 17,014. Our sequence is thus in broad agreement with the published estimated genome size of 740 Mbp5. The oak genome is predicted to encode 49,444 predicted protein-coding loci (Supplementary Table 1).

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Fig. 1: Distribution of fixed somatic mutations in the Napoleon Oak.

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Acknowledgements

This work was funded by the University of Lausanne through a supportive grant from the University rectorate and by the Swiss National Science Foundation (Agora Grant CRAGI3_145652). The Pacific Biosciences RS II sequencing was performed at the Lausanne Genomic Technologies Facility (GTF). The purchase of the GTF’s RS II instrument was financed in part by the Loterie Romande through the Fondation pour la Recherche en Médecine Génétique. We thank K. Harshman, J. Weber and M. Dupasquier from the GTF for sequencing. We thank C. Kuhlemeier for sharing unpublished results, J. Tercier for tree-ring analysis, Transistor communication for graphical production of the 3D oak, Woodtli + Leuba SA for sample collection, N. Guex for advice on SNV identification and J.-J. Strahm and M. Bonetti for providing oak images.

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Author notes

  1. Emanuel Schmid-Siegert, Namrata Sarkar, Christian Iseli, Christian Fankhauser, Christian S. Hardtke, Laurent Keller, John R. Pannell, Alexandre Reymond, Marc Robinson-Rechavi and Ioannis Xenarios contributed equally to this work.

Authors and Affiliations

  1. Vital-IT Competence Center, Swiss Institute of Bioinformatics, Lausanne, Switzerland

    Emanuel Schmid-Siegert, Christian Iseli, Sandra Calderon, Marco Pagni & Ioannis Xenarios

  2. Center for Integrative Genomics, University of Lausanne, Lausanne, Switzerland

    Namrata Sarkar, Jacqueline Chrast, Frédéric Schütz, Christian Fankhauser, Alexandre Reymond & Ioannis Xenarios

  3. Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland

    Namrata Sarkar, Laurent Keller, John R. Pannell & Marc Robinson-Rechavi

  4. Evolutionary Bioinformatics Group, Swiss Institute of Bioinformatics, Lausanne, Switzerland

    Namrata Sarkar & Marc Robinson-Rechavi

  5. Department of Plant Molecular Biology, University of Lausanne, Lausanne, Switzerland

    Caroline Gouhier-Darimont, Pietro Cattaneo, Christian S. Hardtke & Philippe Reymond

  6. Fasteris SA, Plan-les-Ouates, Switzerland

    Laurent Farinelli

  7. Swiss-Prot group, Swiss Institute of Bioinformatics, Geneva, Switzerland

    Michel Schneider & Ioannis Xenarios

  8. Risk Analysis Group, Institute of Earth Sciences, University of Lausanne, Lausanne, Switzerland

    Jérémie Voumard & Michel Jaboyedoff

Authors
  1. Emanuel Schmid-Siegert
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Contributions

L.F. sequenced the genome. E.S.-S., S.C. and M.P. assembled and annotated the genome. N.S., E.S.-S. and C.I. identified SNVs. C.G.-D. and J.C. extracted DNA and confirmed SNVs. E.S.-S. and M.R.-R. analysed genome duplication. P.C. produced cross-sections of oak apical meristems. M.S. established a list of DNA repair genes. F.S. provided statistical help with the analyses. J.V. and M.J. produced a 3D model of the oak tree. C.H., C.F., L.K., I.X., M.R.-R., J.P., A.R. and P.R. conceived the project and wrote the manuscript.

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Correspondence to Philippe Reymond.

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The authors declare no competing financial interests.

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Supplementary Information

Supplementary Figures 1–9, Supplementary Tables 1–4, Supplementary Methods, Supplementary Discussion

Life Sciences Reporting Summary

Supplementary Table 5

DNA repair genes

Supplementary Table 6

Arabidopsis DNA repair genes

Supplementary Table 7

Duplicated DNA repair genes

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Schmid-Siegert, E., Sarkar, N., Iseli, C. et al. Low number of fixed somatic mutations in a long-lived oak tree. Nature Plants 3, 926–929 (2017). https://doi.org/10.1038/s41477-017-0066-9

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