Genome-wide survey of Arabidopsis natural variation in downy mildew resistance using combined association and linkage mapping

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 22, 2010, Pages 10302-10307

  Nemri, Adnane ^a,c   Atwell, Susanna ^b,d   Tarone, Aaron M ^b   Huang, Yu S ^b   Zhao, Keyan ^b,e   Studholme, David J ^a   Nordborg, Magnus ^b   Jones, Jonathan D G ^a  

^a SAINSBURY LABORATORY   (United Kingdom)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c CSIRO   (Australia)

^d TEXAS A AND M UNIVERSITY   (United States)

^e Plant Breeding and Genetics Section in the School of Integrative Plant Science   (United States)

Author keywords

Gene discovery; Plant; Quantitative trait loci

Indexed keywords

ARABIDOPSIS; ARTICLE; DISEASE RESISTANCE; DOWNY MILDEW; GENE MAPPING; GENETIC ASSOCIATION; GENETIC LINKAGE; GENETIC VARIABILITY; GENOTYPE; HYALOPERONOSPORA ARABIDOPSIDIS; NONHUMAN; OOMYCETES; PLANT GENETICS; PLANT GENOME; PRIORITY JOURNAL; QUANTITATIVE TRAIT LOCUS;

ARABIDOPSIS; CHROMOSOME MAPPING; GENETIC VARIATION; GENOME, PLANT; GENOME-WIDE ASSOCIATION STUDY; OOMYCETES; PLANT DISEASES; QUANTITATIVE TRAIT LOCI;

ARABIDOPSIS; ARABIDOPSIS THALIANA; HYALOPERONOSPORA; PERONOSPORACEAE; TEREBRANTIA;

EID: 77953414585     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0913160107     Document Type: Article

References (38)

1. Crute IR, Pink DAC (1996) Genetics and utilization of pathogen resistance in plants. Plant Cell 8:1747-1755.
2. Holub E, Beynon J (1997) Symbiology of mouse-ear cress (Arabidopsis thaliana) and oomycetes. Advances in Botanical Research: Incorporating Advances in Plant Pathology, eds Andrews JH, Tommerup IC, Vol 24, pp 227-273.
3. McHale L, Tan X, Koehl P, Michelmore RW (2006) Plant NBS-LRR proteins: Adaptable guards. Genome Biol 7:212.
4. Speulman E, Bouchez D, Holub EB, Beynon JL (1998) Disease resistance gene homologs correlate with disease resistance loci of Arabidopsis thaliana. Plant J 14:467-474.
5. Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW (2003) Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15:809-834.
6. Botella MA, et al. (1998) Three genes of the Arabidopsis RPP1 complex resistance locus recognize distinct Peronospora parasitica avirulence determinants. Plant Cell 10:1847-1860.
7. Sinapidou E, et al. (2004) Two TIR:NB:LRR genes are required to specify resistance to Peronospora parasitica isolate Cala2 in Arabidopsis. Plant J 38:898-909.
8. Parker JE, et al. (1997) The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the toll and interleukin-1 receptors with N and L6. Plant Cell 9:879-894.
9. McDowell JM, et al. (1998) Intragenic recombination and diversifying selection contribute to the evolution of downy mildew resistance at the RPP8 locus of Arabidopsis. Plant Cell 10:1861-1874.
10. Bittner-Eddy PD, Crute IR, Holub EB, Beynon JL (2000) RPP13 is a simple locus in Arabidopsis thaliana for alleles that specify downy mildew resistance to different avirulence determinants in Peronospora parasitica. Plant J 21:177-188.
11. Slusarenko AJ, Schlaich NL (2003) Downy mildew of Arabidopsis thaliana caused by Hyaloperonospora parasitica (formerly Peronospora parasitica). Mol Plant Pathol 4:159-170.
12. Borhan MH, et al. (2008) WRR4 encodes a TIR-NB-LRR protein that confers broadspectrum white rust resistance in Arabidopsis thaliana to four physiological races of Albugo candida. Mol Plant Microbe Interact 21:757-768.
13. Staal J, Kaliff M, Bohman S, Dixelius C (2006) Transgressive segregation reveals two Arabidopsis TIR-NB-LRR resistance genes effective against Leptosphaeria maculans, causal agent of blackleg disease. Plant J 46:218-230.
14. Staal J, Kaliff M, Dewaele E, Persson M, Dixelius C (2008) RLM3, a TIR domain encoding gene involved in broad-range immunity of Arabidopsis to necrotrophic fungal pathogens. Plant J 55:188-200.
15. Cooley MB, Pathirana S, Wu HJ, Kachroo P, Klessig DF (2000) Members of the Arabidopsis HRT/RPP8 family of resistance genes confer resistance to both viral and oomycete pathogens. Plant Cell 12:663-676.
16. Takahashi H, et al. (2002) RCY1, an Arabidopsis thaliana RPP8/HRT family resistance gene, conferring resistance to cucumber mosaic virus requires salicylic acid, ethylene and a novel signal transduction mechanism. Plant J 32:655-667.
17. Koch E, Slusarenko A (1990) Arabidopsis is susceptible to infection by a downy mildew fungus. Plant Cell 2:437-445. (Pubitemid 120029602)
18. Holub EB, Williams PH, Crute IR (1991) Natural infection of Arabidopsis thaliana by Albugo candida and Peronospora parasitica. Phytopathology 81:1226.
19. Salvaudon L, Héraudet V, Shykoff JA (2007) Genotype-specific interactions and the trade-off between host and parasite fitness. BMC Evol Biol 7:189. (Pubitemid 350293829)
20. Holub EB, Beynon JL, Crute IR (1994) Phenotypic and genotypic characterization of interactions between isolates of peronospora parasitica and accessions of Arabidopsis thaliana. Mol Plant Microbe Interact 7:223-239.
21. van der Biezen EA, Freddie CT, Kahn K, Parker JE, Jones JD (2002) Arabidopsis RPP4 is a member of the RPP5 multigene family of TIR-NB-LRR genes and confers downy mildew resistance through multiple signalling components. Plant J 29:439-451. (Pubitemid 34196956)
22. Holub EB (2007) Natural variation in innate immunity of a pioneer species. Curr Opin Plant Biol 10:415-424. (Pubitemid 47126949)
23. Shindo C, Bernasconi G, Hardtke CS (2007) Natural genetic variation in Arabidopsis: Tools, traits and prospects for evolutionary ecology. Ann Bot 99:1043-1054. (Pubitemid 47355817)
24. Atwell S, et al. (2010) Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature, in press.
25. Nordborg M, Weigel D (2008) Next-generation genetics in plants. Nature 456:720-723.
26. Eulgem T, et al. (2007) EDM2 is required for RPP7-dependent disease resistance in Arabidopsis and affects RPP7 transcript levels. Plant J 49:829-839. (Pubitemid 46279266)
27. Parker JE, et al. (1996) Characterization of eds1, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes. Plant Cell 8:2033-2046.
28. Vorwerk S, et al. (2007) EDR2 negatively regulates salicylic acid-based defenses and cell death during powdery mildew infections of Arabidopsis thaliana. BMC Plant Biol 7:35.
29. Nordborg M, et al. (2002) The extent of linkage disequilibrium in Arabidopsis thaliana. Nat Genet 30:190-193. (Pubitemid 47340659)
30. Song JT, Lu H, McDowell JM, Greenberg JT (2004) A key role for ALD1 in activation of local and systemic defenses in Arabidopsis. Plant J 40:200-212. (Pubitemid 39404070)
31. Caldwell KS, Michelmore RW (2009) Arabidopsis thaliana genes encoding defense signaling and recognition proteins exhibit contrasting evolutionary dynamics. Genetics 181:671-684.
32. Todesco M, et al. (2010) A fitness trade off between growth and disease resistance in Arabidopsis thaliana. Nature, in press.
33. Sohn KH, Lei R, Nemri A, Jones JDG (2007) The downy mildew effector proteins ATR1 and ATR13 promote disease susceptibility in Arabidopsis thaliana. Plant Cell 19:4077-4090. (Pubitemid 351253120)
34. Van Ooijen JW (2004) MAPQTL 5, Software for the Mapping of Quantitative Trait Loci in Experimental Populations (Kyazma B.V., Wageningen, The Netherlands).
35. Nordborg M, et al. (2005) The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol 3:e196.
36. Bakker EG, Toomajian C, Kreitman M, Bergelson J (2006) A genome-wide survey of R gene polymorphisms in Arabidopsis. Plant Cell 18:1803-1818. (Pubitemid 44260179)
37. Zhao K, et al. (2007) An Arabidopsis example of association mapping in structured samples. PLoS Genet 3:e4. (Pubitemid 46168834)
38. Bureau A, et al. (2005) Identifying SNPs predictive of phenotype using random forests. Genet Epidemiol 28:171-182.