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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.

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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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References

  1. Tian, D., Araki, H., Stahl, E., Bergelson, J. & Kreitman, M. Signature of balancing selection in Arabidopsis. Proc. Natl Acad. Sci. USA 99, 11525–11530 (2002).

    Article  CAS  Google Scholar 

  2. Bakker, E., Toomajian, C., Kreitman, M. & Bergelson, J. A genome-wide survey of R gene polymorphisms in Arabidopsis. Plant Cell Online 18, 1803–1818 (2006).

    Article  CAS  Google Scholar 

  3. Thrall, P. et al. Rapid genetic change underpins antagonistic coevolution in a natural host-pathogen metapopulation. Ecol. Lett. 15, 425–435 (2012).

    Article  Google Scholar 

  4. Brown, J. & Tellier, A. Plant-parasite coevolution: Bridging the gap between genetics and ecology. Annu. Rev. Phytopathol. 49, 345–367 (2011).

    Article  CAS  Google Scholar 

  5. Brown, J. K. Durable resistance of crops to disease: a Darwinian perspective. Annu. Rev. Phytopathol. 53, 513–539 (2015).

    Article  CAS  Google Scholar 

  6. Moreno-Gámez, S., Stephan, W. & Tellier, A. Effect of disease prevalence and spatial heterogeneity on polymorphism maintenance in host–parasite interactions. Plant Pathol. 62, 133–141 (2013).

    Article  Google Scholar 

  7. Korves, T. & Bergelson, J. A novel cost of R gene resistance in the presence of disease. Am. Nat. 163, 489–504 (2004).

    Google Scholar 

  8. Tian, D., Traw, M. B., Chen, J. Q., Kreitman, M. & Bergelson, J. Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423, 74–77 (2003).

    Article  CAS  Google Scholar 

  9. Karasov, T. et al. The long-term maintenance of a resistance polymorphism through diffuse interactions. Nature 512, 436–440 (2014).

    Article  CAS  Google Scholar 

  10. Grant, M., et al. Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269, 843–846 (1995).

    Article  CAS  Google Scholar 

  11. Stahl, E. A., Dwyer, G., Mauricio, R., Kreitman, M. & Bergelson, J. Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature 400, 667–671 (1999).

    Article  CAS  Google Scholar 

  12. Rose, L., Atwell, S., Grant, M. & Holub, E. Parallel loss-of-function at the RPM1 bacterial resistance locus in Arabidopsis thaliana. Front. Plant Sci. 3, 287 (2012).

    PubMed  PubMed Central  Google Scholar 

  13. Meyers, B. C., Kozik, A., Griego, A., Kuang, H. & Michelmore, R. W. Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15, 809–834 (2003).

    CAS  Google Scholar 

  14. Kunkel, B., Bent, A., Dahlbeck, D., Innes, R. & Staskawicz, B. RPS2, an Arabidopsis disease resistance locus specifying recognition of Pseudomonas syringae strains expressing the avirulence gene avrRpt2. Plant Cell Online 5, 865–875 (1993).

    CAS  Google Scholar 

  15. Yu, G. L., Katagiri, F. & Ausubel, F. Arabidopsis mutations at the RPS2 locus result in loss of resistance to Pseudomonas syringae strains expressing the avirulence gene avrRpt2. Mol. Plant Microbe Interact. 6, 434–443 (1993).

    Article  CAS  Google Scholar 

  16. Mauricio, R. et al. Natural selection for polymorphism in the disease resistance gene Rps2 of Arabidopsis thaliana. Genetics 163, 735–746 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Bergelson, J. & Purrington, C. B. Surveying patterns in the cost of resistance in plants. Am. Nat. 148, 536–558 (1996).

    Article  Google Scholar 

  18. Raj, A. & Rifkin, S. Variability in gene expression underlies incomplete penetrance. Nature 463 913–918 (2010).

    Article  CAS  Google Scholar 

  19. Mindrinos, M., Katagiri, F., Yu, G. L. & Ausubel, F. M. The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell 78, 1089–1099 (1994).

    Article  CAS  Google Scholar 

  20. Tao, Y., Yuan, F., Leister, R. T., Ausubel, F. M. & Katagiri, F. Mutational analysis of the Arabidopsis nucleotide binding site-leucine-rich repeat resistance gene RPS2. Plant Cell 12, 2541–2554 (2000).

    CAS  Google Scholar 

  21. McNellis, T. W., Mudgett, M. B., Li, K. & Aoyama, T. Glucocorticoid-inducible expression of a bacterial avirulence gene in transgenic Arabidopsis induces hypersensitive cell death. Plant J. 14, 247–257 (1998).

    Article  CAS  Google Scholar 

  22. Leister, R. T. & Katagiri, F. A resistance gene product of the nucleotide binding site – leucine rich repeats class can form a complex with bacterial avirulence proteins in vivo. Plant J. 22, 345–354 (2000).

    Article  CAS  Google Scholar 

  23. Banerjee, D., Zhang, X. & Bent, A. The leucine-rich repeat domain can determine effective interaction between RPS2 and other host factors in Arabidopsis RPS2-mediated disease resistance. Genetics 158, 439–450 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Axtell, M. J., McNellis, T. W., Mudgett, M. B., Hsu, C. S. & Staskawicz, B. J. Mutational analysis of the Arabidopsis RPS2 disease resistance gene and the corresponding pseudomonas syringae avrRpt2 avirulence gene. Mol. Plant Microbe Interact. 14, 181–188 (2001).

    Article  CAS  Google Scholar 

  25. Day, B. et al. Molecular basis for the RIN4 negative regulation of RPS2 disease resistance. Plant Cell Online 17, 1292–1305 (2005).

    Article  CAS  Google Scholar 

  26. Day, B., Dahlbeck, D. & Staskawicz, B. NDR1 interaction with RIN4 mediates the differential activation of multiple disease resistance pathways in Arabidopsis. Plant Cell Online 18, 2782–2791 (2006).

    Article  CAS  Google Scholar 

  27. Qi, D., DeYoung, B. & Innes, R. Structure-function analysis of the coiled-coil and leucine-rich repeat domains of the RPS5 disease resistance protein. Plant Physiol. 158, 1819–1832 (2012).

    Article  CAS  Google Scholar 

  28. Bergelson, J., Kreitman, M., Stahl, E. A. & Tian, D. Evolutionary dynamics of plant R-genes. Science 292, 2281–2285 (2001).

    Article  CAS  Google Scholar 

  29. Gan, X. et al. Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 477, 419–423 (2011).

    Article  CAS  Google Scholar 

  30. Laine, A. L. & Tellier, A. Heterogeneous selection promotes maintenance of polymorphism in host–parasite interactions. Oikos 117, 1281–1288 (2008).

    Article  Google Scholar 

  31. Guo, Y.-L. L. et al. Genome-wide comparison of nucleotide-binding site-leucine-rich repeat-encoding genes in Arabidopsis. Plant Physiol. 157, 757–769 (2011).

    Article  CAS  Google Scholar 

  32. Vergunst, A. C., Jansen, L. E. & Hooykaas, P. J. Site-specific integration of Agrobacterium T-DNA in Arabidopsis thaliana mediated by Cre recombinase. Nucleic Acids Res. 26, 2729–2734 (1998).

    Article  CAS  Google Scholar 

  33. Caicedo, A. L., Schaal, B. A. & Kunkel, B. N. Diversity and molecular evolution of the RPS2 resistance gene in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 96, 302–306 (1999).

    Article  CAS  Google Scholar 

  34. Guttman, D. S. & Greenberg, J. T. Functional analysis of the type III effectors AvrRpt2 and AvrRpm1 of Pseudomonas syringae with the use of a single-copy genomic integration system. Mol. Plant Microbe Interact. 14, 145–155 (2001).

    Article  CAS  Google Scholar 

  35. Czechowski, T., Stitt, M., Altmann, T., Udvardi, M. K. & Scheible, W.-R. R. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 139, 5–17 (2005).

    Article  CAS  Google Scholar 

  36. Cao, J. et al. Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nature Genet. 43, 956–963 (2011).

    CAS  Google Scholar 

Download references

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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  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 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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