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

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. Access through your institution Buy or subscribe This is a preview of subscription content, access via your institution ACCESS OPTIONS

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institutional subscriptions * Read our FAQs * Contact customer support SIMILAR CONTENT BEING VIEWED BY OTHERS NATURAL VARIATION AT _FLM_ SPLICING HAS PLEIOTROPIC EFFECTS MODULATING

ECOLOGICAL STRATEGIES IN _ARABIDOPSIS THALIANA_ Article Open access 18 August 2020 MOLECULAR VARIATION IN A FUNCTIONALLY DIVERGENT HOMOLOG OF FCA REGULATES FLOWERING TIME IN _ARABIDOPSIS

THALIANA_ Article Open access 17 November 2020 MAPPING THE ADAPTIVE LANDSCAPE OF A MAJOR AGRICULTURAL PATHOGEN REVEALS EVOLUTIONARY CONSTRAINTS ACROSS HETEROGENEOUS ENVIRONMENTS Article Open

access 15 January 2021 ACCESSION CODES PRIMARY ACCESSIONS GENBANK/EMBL/DDBJ * HM053468 * HM053469 * HM214805 * HM214897 DATA DEPOSITS DNA sequences have been deposited in GenBank under

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Article  CAS  Google Scholar  Download references 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 * 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.)., * Marco Todesco and Sureshkumar Balasubramanian: These authors contributed equally to this

work. AUTHORS AND AFFILIATIONS * 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 * Molecular and Computational Biology, University of Southern California, Los Angeles, California 90089, USA , Tina T. Hu,

 Yu Huang & Magnus Nordborg * Department of Biological Sciences, University of Pittsburgh, Pittsburgh, Pennsylvania 15238, USA, M. Brian Traw * Department of Ecology and Evolution,

University of Chicago, Chicago, Illinois 60637, USA, Matthew Horton, Justin O. Borevitz & Joy Bergelson * Department of Biology, University of North Carolina, Chapel Hill, North Carolina

27599, USA, Petra Epple & Jeffery L. Dangl * The Sainsbury Laboratory, John Innes Centre, Colney, Norwich NR4 7UH, UK , Christine Kuhns & Volker Lipka * Albrecht von Haller

Institute for Plant Sciences, Georg August University Göttingen, 37073 Göttingen, Germany Christine Kuhns & Volker Lipka * Plant Biology Laboratory, The Salk Institute for Biological

Studies, La Jolla, California 92037, USA , Christopher Schwartz & Joanne Chory * Department of Biochemistry, University of Wisconsin, Madison, Wisconsin 53706, USA, Christopher Schwartz

* Howard Hughes Medical Institute, The Salk Institute for Biological Studies, La Jolla, California 92037, USA , Joanne Chory * 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 * Gregor Mendel Institute, 1030 Vienna, Austria

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Scholar * Detlef Weigel View author publications You can also search for this author inPubMed Google Scholar 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. CORRESPONDING AUTHOR Correspondence to Detlef Weigel. ETHICS DECLARATIONS COMPETING INTERESTS The authors declare

no competing financial interests. SUPPLEMENTARY INFORMATION SUPPLEMENTARY INFORMATION This file contains Supplementary Methods, References, Supplementary Tables 1-9 and Supplementary

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FOR FIG. 5 RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE 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 Download citation * Received: 10 July 2009 * Accepted: 14 April 2010 * Issue

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