Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

The flowering gene SINGLE FLOWER TRUSS drives heterosis for yield in tomato

Nature Genetics volume 42, pages 459–463 (2010)Cite this article

Subjects

Abstract

Intercrossing different varieties of plants frequently produces hybrid offspring with superior vigor and increased yields, in a poorly understood phenomenon known as heterosis1,2. One classical unproven model for heterosis is overdominance, which posits in its simplest form that improved vigor can result from a single heterozygous gene3,4,5,6,7,8. Here we report that heterozygosity for tomato loss-of-function alleles of SINGLE FLOWER TRUSS (SFT), which is the genetic originator of the flowering hormone florigen, increases yield by up to 60%. Yield overdominance from SFT heterozygosity is robust, occurring in distinct genetic backgrounds and environments. We show that several traits integrate pleiotropically to drive heterosis in a multiplicative manner9, and these effects derive from a suppression of growth termination mediated by SELF PRUNING (SP), an antagonist of SFT. Our findings provide the first example of a single overdominant gene for yield and suggest that single heterozygous mutations may improve productivity in other agricultural organisms.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Heterozygosity for loss-of-function mutations in SFT drives heterosis in tomato.
Figure 2: sft/+ heterozygosity causes heterosis in distinct genetic backgrounds and growth conditions.
Figure 3: SFT-dependent heterosis arises from multiple phenotypic changes on component traits that integrate to improve yield.
Figure 4: Overdominance for inflorescence production is based on a dosage-dependent suppression of growth termination mediated by SP.

Accession codes

Accessions

NCBI Reference Sequence

References

  1. Lippman, Z.B. & Zamir, D. Heterosis: revisiting the magic. Trends Genet. 23, 60–66 (2007).

    Article  CAS  Google Scholar 

  2. Crow, J.F. Mid-century controversies in population genetics. Annu. Rev. Genet. 42, 1–16 (2008).

    Article  CAS  Google Scholar 

  3. Shull, G.H. The composition of a field of maize. Am Breed Associ 4, 296–301 (1908).

    Google Scholar 

  4. Wallace, B. The effect of heterozygosity for new mutations on viability in Drosophila: a preliminary report. Proc. Natl. Acad. Sci. USA 43, 404–407 (1957).

    Article  CAS  Google Scholar 

  5. Wallace, B. The role of heterozygosity in Drosophila populations. Proc. 10th Intern. Cong. Genet. 1, 408–419 (1959).

    Google Scholar 

  6. Muller, H.J. & Falk, R. Are induced mutations in Drosophila overdominant? I. Experimental Design. Genetics 46, 727–735 (1961).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Muller, H.J. & Falk, R. Are induced mutations in Drosophila overdominant? II. Experimental Results. Genetics 46, 737–757 (1961).

    Google Scholar 

  8. Schwarz, D. Single gene heterosis for alcohol dehydrogenase in maize: the nature of the subunit interaction. Theor. Appl. Genet. 43, 117–120 (1973).

    Article  Google Scholar 

  9. Williams, W. Heterosis and the genetics of complex characters. Nature 184, 527–530 (1959).

    Article  CAS  Google Scholar 

  10. Darwin, C.E. The Effects of Cross- and Self-Fertilization in the Vegetable Kingdom (John Murray, London, 1876).

  11. Duvick, D.N. Heterosis: feeding people and protecting natural resources. in The Genetics and Exploitation of Heterosis in Crops (eds. Coors, J.G. & Pandey, S.) 19–29 (ASSA, CSSA, SSSA, Madison, 1999).

  12. Crow, J.F. Dominance and overdominance. in Heterosis 282–297 (Iowa State College Press, Ames, Iowa, USA, 1952).

  13. Birchler, J.A., Auger, D.L. & Riddle, N.C. In search of the molecular basis of heterosis. Plant Cell 15, 2236–2239 (2003).

    Article  CAS  Google Scholar 

  14. Charlesworth, D. & Willis, J.H. The genetics of inbreeding depression. Nat. Rev. Genet. 10, 783–796 (2009).

    Article  CAS  Google Scholar 

  15. Redei, G.P. Single locus heterosis. Z. Vererbungsl. 93, 164–170 (1962).

    Google Scholar 

  16. Semel, Y. et al. Overdominant quantitative trait loci for yield and fitness in tomato. Proc. Natl. Acad. Sci. USA 103, 12981–12986 (2006).

    Article  CAS  Google Scholar 

  17. Menda, N., Semel, Y., Peled, D., Eshed, Y. & Zamir, D. In silico screening of a saturated mutation library of tomato. Plant J. 38, 861–872 (2004).

    Article  CAS  Google Scholar 

  18. Lifschitz, E. et al. The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proc. Natl. Acad. Sci. USA 103, 6398–6403 (2006).

    Article  CAS  Google Scholar 

  19. Shalit, A. et al. The flowering hormone florigen functions as a general systemic regulator of growth and termination. Proc. Natl. Acad. Sci. USA 106, 8392–8397 (2009).

    Article  CAS  Google Scholar 

  20. Gur, A. & Zamir, D. Unused natural variation can lift yield barriers in plant breeding. PLoS Biol. 2, e245 (2004).

    Article  Google Scholar 

  21. Schauer, N. et al. Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement. Nat. Biotechnol. 24, 447–454 (2006).

    Article  CAS  Google Scholar 

  22. Whaley, W.G. A developmental analysis of heterosis in Lycopersicon I. The relation of growth rate to heterosis. Am. J. Bot. 26, 609–616 (1939).

    Article  Google Scholar 

  23. Pnueli, L. et al. The SELF-PRUNING gene of tomato regulates vegetative to reproductive switching of sympodial meristems and is the ortholog of CEN and TFL1. Development 125, 1979–1989 (1998).

    CAS  PubMed  Google Scholar 

  24. Lippman, Z.B. et al. The making of a compound inflorescence in tomato and related nightshades. PLoS Biol. 6, e288 (2008).

    Article  Google Scholar 

  25. Veitia, R.A., Bottani, S. & Birchler, J.A. Cellular reactions to gene dosage imbalance: genomic, transcriptomic and proteomic effects. Trends Genet. 24, 390–397 (2008).

    Article  CAS  Google Scholar 

  26. Kobayashi, Y. & Weigel, D. Move on up, it's time for change–mobile signals controlling photoperiod-dependent flowering. Genes Dev. 21, 2371–2384 (2007).

    Article  CAS  Google Scholar 

  27. Birchler, J.A., Yao, H. & Chudalayandi, S. Biological consequences of dosage dependent gene regulatory systems. Biochim. Biophys. Acta 1769, 422–428 (2007).

    Article  CAS  Google Scholar 

  28. Doebley, J.F., Gaut, B.S. & Smith, B.D. The molecular genetics of crop domestication. Cell 127, 1309–1321 (2006).

    Article  CAS  Google Scholar 

  29. McMullen, M.D. et al. Genetic properties of the maize nested association mapping population. Science 325, 737–740 (2009).

    Article  CAS  Google Scholar 

  30. Yu, S.B. et al. Importance of epistasis as the genetic basis of heterosis in an elite rice hybrid. Proc. Natl. Acad. Sci. USA 94, 9226–9231 (1997).

    Article  CAS  Google Scholar 

  31. Flint-Garcia, S.A., Buckler, E.S., Tiffin, P., Ersoz, E. & Springer, N.M. Heterosis is prevalent for multiple traits in diverse maize germplasm. PLoS One 4, e7433 (2009).

    Article  Google Scholar 

  32. Belo, A. et al. Allelic genome structural variations in maize detected by array comparative genome hybridization. Theor. Appl. Genet. 120, 355–357 (2009).

    Article  Google Scholar 

  33. Gemmell, N.J. & Slate, J. Heterozygote advantage for fecundity. PLoS One 1, e125 (2006).

    Article  Google Scholar 

  34. Delneri, D. et al. Identification and characterization of high-flux-control genes of yeast through competition analyses in continuous cultures. Nat. Genet. 40, 113–117 (2008).

    Article  CAS  Google Scholar 

  35. Doganlar, S., Frary, A., Ku, H.M. & Tanksley, S.D. Mapping quantitative trait loci in inbred backcross lines of Lycopersicon pimpinellifolium (LA1589). Genome 45, 1189–1202 (2002).

    Article  CAS  Google Scholar 

  36. Expósito-Rodríguez, M., Borges, A.A., Borges-Perez, A. & Perez, J.A. Selection of internal control genes for quantitative real-time RT-PCR studies during tomato development process. BMC Plant Biol. 8, 131 (2008).

    Article  Google Scholar 

Download references

Acknowledgements

We thank D. Jackson, R. Martienssen, Y. Semel, Y. Eshed and members of the Lippman laboratory for comments and discussion. We also thank the researchers and field crew at the Western Galilee experimental station in Akko, Israel, Kibbutz Kfar Masaryk, Israel and Cornell University's Long Island Horticultural Research and Extension Center in Riverhead, New York. This research was supported by individual grants from the European Commission EU-SOL Project and The Israel Science Foundation (ISF) to D.Z. and from a Heterosis Challenge Grant DBI-0922442 from the United States National Science Foundation Plant Genome Research Program to Z.B.L.

Author information

Authors and Affiliations

  1. The Hebrew University of Jerusalem Faculty of Agriculture, Institute of Plant Sciences, Rehovot, Israel

    Uri Krieger & Dani Zamir

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

    Zachary B Lippman

Authors
  1. Uri Krieger
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zachary B Lippman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dani Zamir
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

U.K., Z.B.L. and D.Z. planned and carried out all experiments, collected the data, performed the statistical analyses and wrote the paper.

Corresponding authors

Correspondence to Zachary B Lippman or Dani Zamir.

Ethics declarations

Competing interests

D.Z. is a cofounder of Phenom Networks, a privately held company that is serving as a repository and online statistical analysis platform for the raw heterosis field data.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–6 and Supplementary Tables 1–4 (PDF 3288 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Krieger, U., Lippman, Z. & Zamir, D. The flowering gene SINGLE FLOWER TRUSS drives heterosis for yield in tomato. Nat Genet 42, 459–463 (2010). https://doi.org/10.1038/ng.550

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ng.550

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing