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Natural allelic variation underlying a major fitness trade-off in Arabidopsis thaliana

Nature volume 465, pages 632–636 (2010)Cite this article

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Abstract

Plants can defend themselves against a wide array of enemies, from microbes to large animals, yet there is great variability in the effectiveness of such defences, both within and between species. Some of this variation can be explained by conflicting pressures from pathogens with different modes of attack1. A second explanation comes from an evolutionary ‘tug of war’, in which pathogens adapt to evade detection, until the plant has evolved new recognition capabilities for pathogen invasion2,3,4,5. If selection is, however, sufficiently strong, susceptible hosts should remain rare. That this is not the case is best explained by costs incurred from constitutive defences in a pest-free environment6,7,8,9,10,11. Using a combination of forward genetics and genome-wide association analyses, we demonstrate that allelic diversity at a single locus, ACCELERATED CELL DEATH 6 (ACD6)12,13, underpins marked pleiotropic differences in both vegetative growth and resistance to microbial infection and herbivory among natural Arabidopsis thaliana strains. A hyperactive ACD6 allele, compared to the reference allele, strongly enhances resistance to a broad range of pathogens from different phyla, but at the same time slows the production of new leaves and greatly reduces the biomass of mature leaves. This allele segregates at intermediate frequency both throughout the worldwide range of A. thaliana and within local populations, consistent with this allele providing substantial fitness benefits despite its marked impact on growth.

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Figure 1: Identification of a natural ACD6 allele affecting growth and defence traits.
Figure 2: Effects of a natural ACD6 allele on leaf biomass, pathogen susceptibility and metabolite content.
Figure 3: Effects of a natural ACD6 allele on pathogen susceptibility.
Figure 4: ACD6 sequence diversity in Arabidopsis.
Figure 5: Correlation between late-onset necrosis, growth and defence traits.

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Accession codes

Primary accessions

GenBank/EMBL/DDBJ

Data deposits

DNA sequences have been deposited in GenBank under accession numbers HM053468 and HM053469 and HM214805 to HM214897.

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Acknowledgements

We thank S.-W. Park and D. Klessig for the nahG clone; J. Greenberg, the NSF-supported Arabidopsis Biological Resource Centre (ABRC) and the European Arabidopsis Stock Centre (NASC) for seeds; and S. Atwell, K. Broman and Y.-L. Guo for advice. We are grateful to K. Bomblies and L. Yant for establishing the Tübingen A. thaliana collection. This work was supported by NIH NRSA fellowship F23-GM65032-1 (C.S.), an EMBO Long-Term Fellowship (S.B.), NIH grants GM62932 (J.C. and D.W.), GM057171 (J.L.D.), GM057994 (J.B.) and GM073822 (J.O.B.), NSF grants DEB-0519961 (J.B. and M.N.) and NSF MCB0603515 (J.B.), HFSPO grant RGP0057/2007-C (J.L.D. and D.W.), DFG grant LI 1317/2-1 (V.L.), the Gatsby Foundation (V.L.), the Dropkin Foundation (J.B.), the Howard Hughes Medical Institute (J.C.), Marie Curie RTN SY-STEM (D.W.), ERA-PG (BMBF) grant ARABRAS (D.W.), FP6 IP AGRON-OMICS (contract LSHG-CT-2006-037704, D.W.), a Gottfried Wilhelm Leibniz Award of the DFG (D.W.), and the Max Planck Society (D.W.).

Author information

Author notes

  1. Sureshkumar Balasubramanian, Tina T. Hu & Sridevi Sureshkumar

    Present address: Present addresses: School of Biological Sciences, University of Queensland, St Lucia, Queensland 4072, Australia (S.B., S.S.); Lewis-Sigler Institute, Princeton University, Princeton, New Jersey 08544, USA (T.T.H.).,

  2. Marco Todesco and Sureshkumar Balasubramanian: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Molecular Biology, Max Planck Institute for Developmental Biology, 72076 Tübingen, Germany

    Marco Todesco, Sureshkumar Balasubramanian, Sridevi Sureshkumar, Christa Lanz, Roosa A. E. Laitinen & Detlef Weigel

  2. Molecular and Computational Biology, University of Southern California, Los Angeles, California 90089, USA ,

    Tina T. Hu, Yu Huang & Magnus Nordborg

  3. Department of Biological Sciences, University of Pittsburgh, Pittsburgh, Pennsylvania 15238, USA,

    M. Brian Traw

  4. Department of Ecology and Evolution, University of Chicago, Chicago, Illinois 60637, USA,

    Matthew Horton, Justin O. Borevitz & Joy Bergelson

  5. Department of Biology, University of North Carolina, Chapel Hill, North Carolina 27599, USA,

    Petra Epple & Jeffery L. Dangl

  6. The Sainsbury Laboratory, John Innes Centre, Colney, Norwich NR4 7UH, UK ,

    Christine Kuhns & Volker Lipka

  7. Albrecht von Haller Institute for Plant Sciences, Georg August University Göttingen, 37073 Göttingen, Germany

    Christine Kuhns & Volker Lipka

  8. Plant Biology Laboratory, The Salk Institute for Biological Studies, La Jolla, California 92037, USA ,

    Christopher Schwartz & Joanne Chory

  9. Department of Biochemistry, University of Wisconsin, Madison, Wisconsin 53706, USA,

    Christopher Schwartz

  10. Howard Hughes Medical Institute, The Salk Institute for Biological Studies, La Jolla, California 92037, USA ,

    Joanne Chory

  11. Department of Microbiology and Immunology, Curriculum in Genetics and Carolina Center for Genome Sciences, University of North Carolina, Chapel Hill, North Carolina 27599, USA,

    Jeffery L. Dangl

  12. Gregor Mendel Institute, 1030 Vienna, Austria

    Magnus Nordborg

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  1. Marco Todesco
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Contributions

M.T., S.B., J.C., V.L., J.O.B., J.L.D., J.B., M.N. and D.W. conceived the study; M.T., S.B., M.B.T., M.H., P.E., C.K., S.S., C.S., C.L. and R.A.E.L. performed the experiments; M.T., S.B., T.T.H., M.B.T., Y.H., J.B., M.N. and D.W. analysed the data; and M.T., S.B. and D.W. wrote the paper with contributions from all authors.

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Correspondence to Detlef Weigel.

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The authors declare no competing financial interests.

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Todesco, M., Balasubramanian, S., Hu, T. et al. Natural allelic variation underlying a major fitness trade-off in Arabidopsis thaliana. Nature 465, 632–636 (2010). https://doi.org/10.1038/nature09083

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