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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.

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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.

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.).

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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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