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

Nature Plants

Volumn 2, Issue 8, 2016, Pages

  Macqueen, Alice ^a,b,c   Sun, Xiaoqin ^a,b,c   Bergelson, Joy ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^c INSTITUTE OF BOTANY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; RPS2 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; GENETIC POLYMORPHISM; GENETICS; IMMUNOLOGY; METABOLISM; PLANT DISEASE; PLANT IMMUNITY; PLEIOTROPY; REPRODUCTIVE FITNESS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENETIC FITNESS; GENETIC PLEIOTROPY; PLANT DISEASES; PLANT IMMUNITY; POLYMORPHISM, GENETIC;

EID: 84985916112     PISSN: None     EISSN: 20550278     Source Type: Journal    
DOI: 10.1038/NPLANTS.2016.110     Document Type: Article

References (36)

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).
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).
3. Thrall, P. et al. Rapid genetic change underpins antagonistic coevolution in a natural host-pathogen metapopulation. Ecol. Lett. 15, 425-435 (2012).
4. Brown, J. & Tellier, A. Plant-parasite coevolution: Bridging the gap between genetics and ecology. Annu. Rev. Phytopathol. 49, 345-367 (2011).
5. Brown, J. K. Durable resistance of crops to disease: A Darwinian perspective. Annu. Rev. Phytopathol. 53, 513-539 (2015).
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).
7. Korves, T. & Bergelson, J. A novel cost of R gene resistance in the presence of disease. Am. Nat. 163, 489-504 (2004).
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).
9. Karasov, T. et al. The long-term maintenance of a resistance polymorphism through diffuse interactions. Nature 512, 436-440 (2014).
10. Grant, M., et al. Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269, 843-846 (1995).
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).
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).
13. Meyers, B. C., Kozik, A., Griego, A., Kuang, H. & Michelmore, R. W. Genomewide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15, 809-834 (2003).
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).
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).
16. Mauricio, R. et al. Natural selection for polymorphism in the disease resistance gene Rps2 of Arabidopsis thaliana. Genetics 163, 735-746 (2003).
17. Bergelson, J. & Purrington, C. B. Surveying patterns in the cost of resistance in plants. Am. Nat. 148, 536-558 (1996).
18. Raj, A. & Rifkin, S. Variability in gene expression underlies incomplete penetrance. Nature 463 913-918 (2010).
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).
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).
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).
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).
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).
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).
25. Day, B. et al. Molecular basis for the RIN4 negative regulation of RPS2 disease resistance. Plant Cell Online 17, 1292-1305 (2005).
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).
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).
28. Bergelson, J., Kreitman, M., Stahl, E. A. & Tian, D. Evolutionary dynamics of plant R-genes. Science 292, 2281-2285 (2001).
29. Gan, X. et al. Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 477, 419-423 (2011).
30. Laine, A. L. & Tellier, A. Heterogeneous selection promotes maintenance of polymorphism in host-parasite interactions. Oikos 117, 1281-1288 (2008).
31. Guo, Y.L. L. et al. Genome-wide comparison of nucleotide-binding site-leucinerich repeat-encoding genes in Arabidopsis. Plant Physiol. 157, 757-769 (2011).
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).
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).
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).
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).
36. Cao, J. et al. Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nature Genet. 43, 956-963 (2011).