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Variation in the flowering gene SELF PRUNING 5G promotes day-neutrality and early yield in tomato

Nature Genetics volume 49, pages 162–168 (2017)Cite this article

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Abstract

Plants evolved so that their flowering is triggered by seasonal changes in day length1. However, day-length sensitivity in crops limits their geographical range of cultivation, and thus modification of the photoperiod response was critical for their domestication2,3,4,5,6,7,8,9,10,11. Here we show that loss of day-length-sensitive flowering in tomato was driven by the florigen paralog and flowering repressor SELF-PRUNING 5G (SP5G). SP5G expression is induced to high levels during long days in wild species, but not in cultivated tomato because of cis-regulatory variation. CRISPR/Cas9-engineered mutations in SP5G cause rapid flowering and enhance the compact determinate growth habit of field tomatoes, resulting in a quick burst of flower production that translates to an early yield. Our findings suggest that pre-existing variation in SP5G facilitated the expansion of cultivated tomato beyond its origin near the equator in South America, and they provide a compelling demonstration of the power of gene editing to rapidly improve yield traits in crop breeding.

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Figure 1: Reduced SP5G expression in long days explains the loss of photoperiod-sensitive flowering in cultivated tomato.
Figure 2: CRISPR/Cas9-engineered mutations in SP5G cause rapid flowering regardless of day length.
Figure 3: The flower-repressing activity of SP5G is mediated by repression of the florigen gene SFT.
Figure 4: Introducing CR-sp5g mutations into the sp determinate background results in highly compact 'double-determinate' plants with early yields.

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Acknowledgements

We thank all members of the Lippman lab and Y. Eshed for valuable discussions. We also thank M. Koornneef for his constant support and useful discussions. We thank C. Brooks, A. Krainer and J. Dalrymple for technical support; T. Mulligan; S. Vermylen; A. Krainer from CSHL; K. Dunn and M. Treat from Robert Treat Farm in Milford, Connecticut; and staff from Cornell University's Long Island Horticultural Research and Extension Center in Riverhead, New York, for assistance with plant care. We thank U. Tartler and A. Lautscham for their help at the Max Planck Institute for Plant Breeding Research. This research was supported by an EMBO Long-Term Fellowship (ALTF 1589-2014 to S.S.), the Next-Generation BioGreen 21 Program (PMBC, PJ011912012016 to S.J.P.), the German Research Foundation (DFG project number SCHM2793/1-1 to I.S.), the Max Planck Society (I.S.), the German Research Foundation under the German-Israeli Project Cooperation program (DFG DIP project number FE552/12-1 to J.M.J.-G.), the National Science Foundation Plant Genome Research Program (IOS-1237880 to J.V.E. and Z.B.L.), BARD (IS-4818-15 to Z.B.L.), the US-Israel Binational Agricultural Research & Development fund (Z.B.L.), and an Agriculture and Food Research Initiative competitive grant from the USDA National Institute of Food and Agriculture (2016-67013-24452 to Z.B.L.).

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Author notes

  1. Niels A Müller, Ke Jiang & Ryosuke Hayama

    Present address: Present addresses: Copenhagen Plant Science Centre, University of Copenhagen, Frederiksberg, Denmark (N.A.M.); Dow AgroSciences, Indianapolis, Indiana, USA (K.J.); Department of Natural Science, International Christian University, Tokyo, Japan (R.H.).,

Authors and Affiliations

  1. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, USA

    Sebastian Soyk, Ke Jiang & Zachary B Lippman

  2. Department of Plant Breeding and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany

    Niels A Müller, Inga Schmalenbach, Lei Zhang & José M Jiménez-Gómez

  3. Division of Biological Sciences, Wonkwang University, Iksan, Republic of Korea

    Soon Ju Park

  4. Department of Plant Developmental Biology, Max Planck Institute for Plant Breeding Research, Cologne, Germany

    Ryosuke Hayama

  5. The Boyce Thompson Institute, Ithaca, New York, USA

    Joyce Van Eck

  6. Institut Jean-Pierre Bourgin, INRA, AgroParisTech, CNRS, Université Paris-Saclay, Versailles, France

    José M Jiménez-Gómez

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Contributions

S.S., N.A.M., S.J.P., I.S., K.J., R.H., L.Z., J.V.E., J.M.J.-G. and Z.B.L. designed and planned experiments. S.S., N.A.M., S.J.P., I.S., K.J., R.H., L.Z., J.M.J.-G. and Z.B.L. performed experiments and collected the data. S.S., N.A.M., S.J.P., I.S., K.J., R.H., J.M.J.-G. and Z.B.L. analyzed the data. S.S., N.A.M., J.M.J.-G. and Z.B.L designed the research. S.S. and Z.B.L. wrote the paper.

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Correspondence to José M Jiménez-Gómez or Zachary B Lippman.

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Competing interests

S.S., S.J.P. and Z.B.L. have filed a PCT patent application based in part on this work (US Provisional Application No. 62/320,439) with the US Patent and Trademark Office.

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Soyk, S., Müller, N., Park, S. et al. Variation in the flowering gene SELF PRUNING 5G promotes day-neutrality and early yield in tomato. Nat Genet 49, 162–168 (2017). https://doi.org/10.1038/ng.3733

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