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Genetic architecture and pleiotropy shape costs of Rps2-mediated resistance in Arabidopsis thaliana

Nature Plants volume 2, Article number: 16110 (2016) Cite this article

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Abstract

The mounting evidence that R genes incur large fitness costs raises a question: how can there be a 5–10% fitness reduction for all 149 R genes in the Arabidopsis thaliana genome? The R genes tested to date segregate for insertion–deletion (indel) polymorphisms where susceptible alleles are complete deletions. Since costs of resistance are measured as the differential fitness of isolines carrying resistant and susceptible alleles, indels reveal costs that may be masked when susceptible alleles are expressed. Rps2 segregates for two expressed clades of alleles, one resistant and one susceptible. Plants with resistant Rps2 are not less fit than those with a susceptible Rps2 allele in the absence of disease. Instead, all alleles provide a fitness benefit relative to an artificial deletion because of the role of RPS2 as a negative regulator of defence. Our results highlight the interplay between genomic architecture and the magnitude of costs of resistance.

Understanding how plants maximize fitness in response to intermittent pathogen presence is of central importance in plant pathology. Natural plant pathosystems frequently involve long-maintained polymorphisms for host resistance1–3, and current theory on the maintenance of stable resistance polymorphisms requires costs of resistance and/or virulence acting in combination with frequency-dependent selection4. In contrast, in agricultural contexts, resistance genes often have useful lifespans of only a few years and high costs of resistance are undesirable because of their negative effects on plant performance5. Pathogen resistance may involve two distinct fitness costs. The first, which we term a cost of surveillance, accrues from harbouring R genes that allow a resistance response on attack6, and the second, a cost of defence, accrues from activation of the resistance response during attack6,7.

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Figure 1: Natural variation in Rps2 captured by the transgenic allelic series.
Figure 2: Significant fitness variation among lines in the allelic series in the absence of pathogen.
Figure 3: Rps2 knockout lines differentially express stress response, defence response and growth-related genes relative to all lines with an allele of Rps2.
Figure 4: Rps2 expression level affects both stress response and defence response genes.

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Acknowledgements

We thank H. King, L. Merwin, C. Meyer, W. Muliyati, A. Olsen, N. Shakoor and T. Stewart for their assistance in the field; J. Greenberg for donation of strains for infection; P. Hooykaas for pSDM3110, M. Vetter for her high-throughput infection protocol; and B. Brachi, T. Karasov, M. Kreitman and L. Merwin for helpful discussions. This research was supported by NSF and NIH grants to J.B. and a grant from the National Natural Science Foundation of China to X.Q.S. (Grant no. 31470448).

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Author notes

  1. Alice MacQueen & Xiaoqin Sun

    Present address: †Present addresses: Department of Integrative Biology, University of Texas at Austin, 1 University Station #C0930, Austin, Texas 78712, USA (A.M.); Institute of Botany, Jiangsu Province and Chinese Academy of Sciences, Nanjing 210014, China (X.S.).,

Authors and Affiliations

  1. Department of Ecology and Evolution, University of Chicago, 1101 East 57th Street, Chicago, 60637, Illinois, USA

    Alice MacQueen, Xiaoqin Sun & Joy Bergelson

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  1. Alice MacQueen
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Contributions

X.Q.S. created the allelic series; A.M., X.Q.S. and J.B. designed the experiments; A.M. conducted the experiments; J.B. conceived of the experiments; A.M. and J.B. wrote the paper.

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Correspondence to Joy Bergelson.

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The authors declare no competing financial interests.

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Supplementary Information

Supplementary Methods, Supplementary References, Supplementary Figs 1–8 and Supplementary Tables 1–22. (PDF 1428 kb)

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MacQueen, A., Sun, X. & Bergelson, J. Genetic architecture and pleiotropy shape costs of Rps2-mediated resistance in Arabidopsis thaliana. Nature Plants 2, 16110 (2016). https://doi.org/10.1038/nplants.2016.110

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