Abstract

Breeding of crops over millennia for yield and productivity1 has led to reduced genetic diversity. As a result, beneficial traits of wild species, such as disease resistance and stress tolerance, have been lost2. We devised a CRISPR–Cas9 genome engineering strategy to combine agronomically desirable traits with useful traits present in wild lines. We report that editing of six loci that are important for yield and productivity in present-day tomato crop lines enabled de novo domestication of wild Solanum pimpinellifolium. Engineered S. pimpinellifolium morphology was altered, together with the size, number and nutritional value of the fruits. Compared with the wild parent, our engineered lines have a threefold increase in fruit size and a tenfold increase in fruit number. Notably, fruit lycopene accumulation is improved by 500% compared with the widely cultivated S. lycopersicum. Our results pave the way for molecular breeding programs to exploit the genetic diversity present in wild plants.

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Acknowledgements

We are grateful to S. Schültke for technical assistance. This work was supported by funding from the Agency for the Support and Evaluation of Graduate Education (CAPES, Brazil), the National Council for Scientific and Technological Development (CNPq, Brazil) and Foundation for Research Assistance of the São Paulo State (FAPESP, Brazil), and the German Federal Ministry of Education and Research (BMBF, Germany). We thank CAPES for studentships granted to E.R.N. and FAPESP for the studentship granted to M.M.N. (2013/12209-1). L.F. was supported by FAPESP grant 2013/18056-2. FAPESP and BMBF provided a grant for L.E.P.P. (2015/50220-2) and J.K. (031B0334). L.E.P.P. acknowledges a grant from CNPq (grant 307040/2014-3).

Author information

Author notes

    • Tomáš Čermák

    Present address: Inari Agriculture, Cambridge, Massachusetts, USA.

    • Agustin Zsögön
    •  & Tomáš Čermák

    These authors contributed equally to this work.

Affiliations

  1. Departamento de Biologia Vegetal, Universidade Federal de Viçosa, Viçosa, Brazil.

    • Agustin Zsögön
    •  & Emmanuel Rezende Naves
  2. Department of Genetics, Cell Biology and Development, Center for Genome Engineering, University of Minnesota, Minneapolis, Minnesota, USA.

    • Tomáš Čermák
    •  & Daniel F Voytas
  3. Departamento de Ciências Biológicas, Escola Superior de Agricultura “Luiz de Queiroz,” Universidade de São Paulo, Piracicaba, Brazil.

    • Marcela Morato Notini
    •  & Lázaro Eustáquio Pereira Peres
  4. Institut für Biologie und Biotechnologie der Pflanzen, Universität Münster, Münster, Germany.

    • Kai H Edel
    • , Stefan Weinl
    •  & Jörg Kudla
  5. Instituto de Biociências, Universidade de São Paulo, São Paulo, Brazil.

    • Luciano Freschi

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Contributions

A.Z., T.C., D.F.V., J.K. and L.E.P.P. designed the study. A.Z., T.C., M.M.N., E.R.N., K.H.E., S.W. and L.F. performed experiments. A.Z., T.C. and K.H.E. analyzed data. A.Z., K.H.E., J.K. and L.E.P.P. prepared the manuscript. All authors have revised and approved the final version of the manuscript.

Competing interests

After completion of this work in the laboratory of D.F.V., T.C. became an employee of Inari Agriculture, a company that uses novel technologies for crop breeding. D.F.V. is a founder and Chief Science Officer of Calyxt, a company applying genome editing to plants.

Corresponding authors

Correspondence to Jörg Kudla or Lázaro Eustáquio Pereira Peres.

Supplementary information

PDF files

  1. 1.

    Supplementary Text and Figures

    Supplementary Figures 1–11

  2. 2.

    Life Sciences Reporting Summary

  3. 3.

    Supplementary Tables

    Supplementary Tables 1–12

Text files

  1. 1.

    Supplementary Note 1

    Annotated sequence for pTC321

  2. 2.

    Supplementary Note 2

    Annotated sequence for pTC603

Zip files

  1. 1.

    Supplementary Dataset 1

    Raw sequence files and alignments corresponding to Supplementary Figure 2 and Supplementary Tables 3 and 5

  2. 2.

    Supplementary Dataset 2

    Raw sequence files and alignments corresponding to Figures 1–3, Supplementary Figures 3, 4, 5 and 7, and Supplementary Table 2

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DOI

https://doi.org/10.1038/nbt.4272