The effect of environmental heterogeneity on RPW8-mediated resistance to powdery mildews in Arabidopsis thaliana

Annals of Botany

Volumn 109, Issue 4, 2012, Pages 833-842

  Jorgensen, Tove H ^a  

^a UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

Arabidopsis thaliana; disease resistance; Genotype environment interaction; Golovinomyces orontii; plant pathogen interaction; powdery mildew; qPCR; RPW8; temperature

Indexed keywords

ARABIDOPSIS PROTEIN;

DISEASE RESISTANCE; FUNGAL DISEASE; GENE EXPRESSION; GENETIC VARIATION; GENOTYPE; HERB; HETEROGENEITY; INFECTIVITY; MAGNITUDE; PATHOGENICITY; POLYMERASE CHAIN REACTION; POPULATION STRUCTURE; SELECTION; SOIL NUTRIENT; SPATIOTEMPORAL ANALYSIS; TEMPERATURE EFFECT;

ARABIDOPSIS; ARTICLE; ASCOMYCETES; BIOSYNTHESIS; CHEMISTRY; DISEASE RESISTANCE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; GENETICS; GENOTYPE ENVIRONMENT INTERACTION; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; PLANT DISEASE; PLANT GENE; SOIL; TEMPERATURE; UNITED KINGDOM;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; ASCOMYCOTA; DISEASE RESISTANCE; GENE EXPRESSION REGULATION, PLANT; GENE-ENVIRONMENT INTERACTION; GENES, PLANT; GENETIC VARIATION; GREAT BRITAIN; PLANT DISEASES; SOIL; TEMPERATURE; TRANSCRIPTION, GENETIC;

ARABIDOPSIS THALIANA; ERYSIPHALES; GOLOVINOMYCES ORONTII;

EID: 84857710137     PISSN: 03057364     EISSN: 10958290     Source Type: Journal    
DOI: 10.1093/aob/mcr320     Document Type: Article

References (70)

1. Agrios GN. 1997. Plant pathology. New York: Academic Press.
2. Boyes DC, Nam J, Dangl JL. 1998. The Arabidopsis thaliana RPM1 disease resistance gene product is a peripheral plasma membrane protein that is degraded coincident with the hypersensitive response. Proceedings of the National Academy of Sciences of the USA 95: 15849-15854. (Pubitemid 29018789)
3. Brown JKM. 2003. A cost of disease resistance: Paradigm or peculiarity? Trends in Genetics 19: 667-671. (Pubitemid 37464839)
4. Burdon JJ. 1987. Diseases and plant population biology. Cambridge: Cambridge University Press.
5. Burdon JJ, Jarosz AM. 1991. Host-pathogen interactions in natural populations of Linum marginale and Melampsora lini. 1. Patterns of resistance and racial variation in a large host population. Evolution 45: 205-217.
6. Bustin SA, Benes V, Garson JA, et al. 2009. The MIQE Guidelines: Minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry 55: 611-622.
7. Carroll LS, Meagher S, Morrison L, Penn DJ, Potts WK. 2004. Fitness effects of a selfish gene (the Mus T complex) are revealed in an ecological context. Evolution 58: 1318-1328. (Pubitemid 38826283)
8. Century KS, Lagman RA, Adkisson M, et al. 1999. Developmental control of Xa21-mediated disease resistance in rice. Plant Journal 20: 231-236. (Pubitemid 129515857)
9. Chongo G, Bernier CC. 2000. Effects of host, inoculum concentration, wetness duration, growth stage, and temperature on anthracnose of lentil. Plant Disease 84: 544-548. (Pubitemid 30218255)
10. Collins N, Drake J, Ayliffe M, et al. 1999. Molecular characterization of the maize Rp1-D rust resistance haplotype and its mutants. Plant Cell 11: 1365-1376.
11. Dawkins R, Krebs JR. 1979. Arms races between and within species. Proceedings of The Royal Society of London Series B-Biological Sciences 205: 489-511. (Pubitemid 10248037)
12. Dubuffet A, Dupas S, Frey F, Drezen JM, Poirie M, Carton Y. 2007. Genetic interactions between the parasitoid wasp Leptopilina boulardi and its Drosophila hosts. Heredity 98: 21-27. (Pubitemid 44973573)
13. Eitas TK, Dangl JL. 2010. NB-LRR proteins: Pairs, pieces, perception, partners, and pathways. Current Opinion in Plant Biology 13: 472-477.
14. Elmore JM, Lin Z-JD, Coaker G. 2011. Plant NB-LRR signaling: Upstreams and downstreams. Current Opinion in Plant Biology 14: 365-371.
15. Fu DL, Uauy C, Distelfeld A, et al. 2009. A Kinase-START Gene confers temperature-dependent resistance to wheat stripe rust. Science 323: 1357-1360.
16. Gandon S, Mackinnon MJ, Nee S, Read AF. 2001. Imperfect vaccines and the evolution of pathogen virulence. Nature 414: 751-756. (Pubitemid 34000772)
17. Gijzen M, MacGregor T, Bhattacharyya M, Buzzell R. 1996. Temperature induced susceptibility to Phytophthora sojae in soybean isolines carrying different Rps genes. Physiological and Molecular Plant Pathology 48: 209-215. (Pubitemid 26356227)
18. Gillespie JH, Turelli M. 1989. Genotype-environment interactions and the maintenance of polygenic variation. Genetics 121: 129-138. (Pubitemid 19026326)
19. Jarosz AM, Burdon JJ. 1992. Host-pathogen interactions in natural populations of Linum marginale and Melampsora lini. 3. Influence of pathogen epidemics on host survivorship and flower production. Oecologia 89: 53-61.
20. Jeffery KJM, Bangham CRM. 2000. Do infectious diseases drive MHC diversity? Microbes and Infection 2: 1335-1341.
21. Jensen B, Munk L. 1997. Nitrogen-induced changes in colony density and spore production of Erysiphe graminis f sp hordei on seedlings of six spring barley cultivars. Plant Pathology 46: 191-202. (Pubitemid 27185426)
22. Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444: 323-329. (Pubitemid 44764102)
23. de Jong CF, Takken FLW, Cai XH, de Wit P, Joosten M. 2002. Attenuation of Cf-mediated defense responses at elevated temperatures correlates with a decrease in elicitor-binding sites. Molecular Plant-Microbe Interactions 15: 1040-1049. (Pubitemid 35211758)
24. Jorgensen TH, Emerson BC. 2008. Functional variation in a disease resistance gene in populations of Arabidopsis thaliana. Molecular Ecology 17: 4912-4923.
25. Koch E, Slusarenko A. 1990. Arabidopsis is susceptible to infection by a downy mildew fungus. Plant Cell 2: 437-445. (Pubitemid 120029602)
26. Laine AL. 2007. Pathogen fitness components and genotypes differ in their sensitivity to nutrient and temperature variation in a wild plant-pathogen association. Journal of Evolutionary Biology 20: 2371-2378.
27. Laine AL, Tellier A. 2008. Heterogenous selection promotes maintenance of polymorphism in host-parasite interactions. Oikos 117: 1281-1288.
28. Lazzaro BP, Little TJ. 2009. Immunity in a variable world. Philosophical Transactions of the Royal Society B-Biological Sciences 364: 15-26.
29. Levene H. 1953. Genetic equilibrium when more than one ecological niche is available. American Naturalist 87: 331-333.
30. Lynch M, Walsh B. 1998. Genetics and analysis of quantitative traits. Sunderland, MA: Sinauer Associates.
31. Millett BP, Mollov DS, Iorizzo M, Carputo D, Bradeen JM. 2009. Changes in disease resistance phenotypes associated with plant physiological age are not caused by variation in R gene transcript abundance. Molecular Plant-Microbe Interactions 22: 362-368.
32. Mohr TJ, Mammarella ND, Hoff T, Woffenden BJ, Jelesko JG, McDowell JM. 2010. The Arabidopsis downy mildew resistance gene RPP8 is induced by pathogens and salicylic acid and is regulated by W box cis elements. Molecular Plant-Microbe Interactions 23: 1303-1315.
33. Noutoshi Y, Ito T, Seki M, et al. 2005. A single amino acid insertion in the WRKY domain of the Arabidopsis TIR-NBS-LRR-WRKY-type disease resistance protein SLH1 (sensitive to low humidity 1) causes activation of defense responses and hypersensitive cell death. Plant Journal 43: 873-888. (Pubitemid 43922154)
34. Oliva R, Win J, Raffaele S, et al. 2010. Recent developments in effector biology of filamentous plant pathogens. Cellular Microbiology 12: 705-715.
35. Orgil U, Arakit H, Tangchaiburana S, Berkey R, Xiao S. 2007. Intraspecific genetic variations, fitness cost and benefit of RPW8, a disease resistance locus in Arabidopsis thaliana. Genetics 176: 2317-2333. (Pubitemid 47360662)
36. Pedley KF, Martin GB. 2005. Role of mitogen-activated protein kinases in plant immunity. Current Opinion in Plant Biology 8: 541-547. (Pubitemid 41188190)
37. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29: E45. http://dx.doi.org/10 1093/nar/29.9.e45.
38. Plotnikova JM, Reuber TL, Ausubel FM. 1998. Powdery mildew pathogenesis of Arabidopsis thaliana. Mycologia 90: 1009-1016. (Pubitemid 29022665)
39. Price JS, Bever JD, Clay K. 2004. Genotype, environment and genotype by environment interactions determine quantitative resistance to leaf rust (Coleosporium asterum) in Euthamia graminifolia (Asteraceae). New Phytologist 162: 729-743. (Pubitemid 38700185)
40. Ramage RA, Sutherland MW. 1995. High and low pre-inoculation temperatures decrease the effectiveness of the Lr20 and Sr15 rust resistance genes in wheat. Plant Pathology 44: 772-778. (Pubitemid 3006509)
41. Ramakers C, Ruijter JM, Deprez RHL, Moorman AFM. 2003. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neuroscience Letters 339: 62-66. (Pubitemid 36263221)
42. Salvaudon L, Heraudet V, Shykoff JA. 2005. Parasite-host fitness trade-offs change with parasite identity: Genotype-specific interactions in a plantpathogen system. Evolution 59: 2518-2524. (Pubitemid 43069934)
43. Sander JF, Heitefuss R. 1998. Susceptibility to Erysiphe graminis f. sp. tritici and phenolic acid content of wheat as influenced by different levels of nitrogen fertilization. Journal of Phytopathology 146: 495-507. (Pubitemid 129536276)
44. Sasaki A. 2000. Host-parasite coevolution in a multilocus gene-for-gene system. Proceedings of the Royal Society of London Series B-Biological Sciences 267: 2183-2188.
45. Shi J, Zhang L, An H, et al. 2011. GhMPK16, a novel stress-responsive group D MAPK gene from cotton, is involved in disease resistance and drought sensitivity. BMC Molecular Biology 12: 22. http://dx.doi.org/10.1186/1471-2199- 12-22.
46. Shirasu K. 2009. The HSP90-SGT1 chaperone complex for NLR immune sensors. Annual Review of Plant Biology 60: 139-164.
47. Simms EL, Rausher MD. 1987. Costs and benefits of plant resistance to herbivory. American Naturalist 130: 570-581.
48. Tan XP, Meyers BC, Kozik A, et al. 2007. Global expression analysis of nucleotide binding site-leucine rich repeat-encoding and related genes in Arabidopsis. BMC Plant Biology 7: 56. http://dx.doi.org/10.1186/1471- 2229-7-56.
49. Tellier A. 2009. The influence of perenniality and seed banks on polymorphism in plant-parasite interactions. American Naturalist 174: 769-779.
50. Thompson JN. 2005. The geographic mosaic of co-evolution. Chicago: University of Chicago Press.
51. Thrall PH, Burdon JJ. 2002. Evolution of gene-for-gene systems in metapopulations: The effect of spatial scale of host and pathogen dispersal. Plant Pathology 51: 169-184. (Pubitemid 34432051)
52. Vale PF, Stjernman M, Little TJ. 2008. Temperature-dependent costs of parasitism and maintenance of polymorphism under genotype-by-environment interactions. Journal of Evolutionary Biology 21: 1418-1427.
53. Vandesompele J, De Preter K, Pattyn F, et al. 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3: Research0034-research0034.11. http://dx.doi.org/10.1186/gb-2002-3-7-research0034.
54. Wang WM, Devoto A, Turner JG, Xiao SY. 2007. Expression of the membrane-associated resistance protein RPW8 enhances basal defense against biotrophic pathogens. Molecular Plant-Microbe Interactions 20: 966-976. (Pubitemid 47105729)
55. Wang WM, Wen YQ, Berkey R, Xiao SY. 2009. Specific targeting of the Arabidopsis resistance protein RPW8.2 to the interfacial membrane encasing the fungal haustorium renders broad-spectrum resistance to powdery mildew. Plant Cell 21: 2898-2913.
56. Wang Y, Bao ZL, Zhu Y, Hua J. 2009. Analysis of temperature modulation of plant defense against biotrophic microbes. Molecular Plant-Microbe Interactions 22: 498-506.
57. Wang ZX, Yano M, Yamanouchi U, et al. 1999. The Pib gene for rice blast resistance belongs to the nucleotide binding and leucine-rich repeat class of plant disease resistance genes. Plant Journal 19: 55-64.
58. Wang ZX, Yamanouchi U, Katayose Y, Sasaki T, Yano M. 2001. Expression of the Pib rice-blast-resistance gene family is up-regulated by environmental conditions favouring infection and by chemical signals that trigger secondary plant defences. Plant Molecular Biology 47: 653-661. (Pubitemid 33066324)
59. Webb KM, Ona I, Bai J, et al. 2010. A benefit of high temperature: Increased effectiveness of a rice bacterial blight disease resistance gene. New Phytologist 185: 568-576.
60. Weinig C, Ungerer MC, Dorn LA, et al. 2002. Novel loci control variation in reproductive timing in Arabidopsis thaliana in natural environments. Genetics 162: 1875-1884. (Pubitemid 36114670)
61. Wolinska J, King KC. 2009. Environment can alter selection in host-parasite interactions. Trends in Parasitology 25: 236-244.
62. Xiao SY, Ellwood S, Calis O, et al. 2001. Broad-spectrum mildew resistance in Arabidopsis thaliana mediated by RPW8. Science 291: 118-120. (Pubitemid 32056678)
63. Xiao SY, Brown S, Patrick E, Brearley C, Turner JG. 2003. Enhanced transcription of the Arabidopsis disease resistance genes RPW8.1 and RPW8.2 via a salicylic acid-dependent amplification circuit is required for hypersensitive cell death. Plant Cell 15: 33-45. (Pubitemid 36137660)
64. Xiao SY, Emerson B, Ratanasut K, et al. 2004. Origin and maintenance of a broad-spectrum disease resistance locus in Arabidopsis. Molecular Biology and Evolution 21: 1661-1672. (Pubitemid 39096882)
65. Xiao SY, Calis O, Patrick E, et al. 2005. The atypical resistance gene, RPW8, recruits components of basal defence for powdery mildew resistance in Arabidopsis. Plant Journal 42: 95-110.
66. Yan GP, Chen XM. 2008. Identification of a quantitative trait locus for hightemperature adult-plant resistance against Puccinia striiformis f. sp hordei in 'Bancroft' barley. Phytopathology 98: 120-127.
67. Yang SH, Hua J. 2004. A haplotype-specific resistance gene regulated by BONZAI1 mediates temperature-dependent growth control in Arabidopsis. Plant Cell 16: 1060-1071. (Pubitemid 38459223)
68. Yang X, Wang W, Coleman M, et al. 2009. Arabidopsis 14-3-3 lambda is a positive regulator of RPW8-mediated disease resistance. The Plant Journal 60: 539-550.
69. Yoshimura S, Yamanouchi U, Katayose Y, et al. 1998. Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation. Proceedings of the National Academy of Sciences of the USA 95: 1663-1668.
70. Zhu Y, Yang HJ, Mang HG, Hua JA. 2011. Induction of BAP1 by a moderate decrease in temperature is mediated by ICE1 in Arabidopsis. Plant Physiology 155: 580-588.