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


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.

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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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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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Authors and Affiliations



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 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).

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