Proteome analysis of the Albugo candida-Brassica juncea pathosystem reveals that the timing of the expression of defence-related genes is a crucial determinant of pathogenesis

Journal of Experimental Botany

Volumn 62, Issue 3, 2011, Pages 1285-1298

  Kaur, Parwinder ^a   Jost, Ricarda ^a   Sivasithamparam, Krishnapillai ^a   Barbetti, Martin John ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Albugo candida; biotic stress; Brassica juncea; host resistance; proteome analysis; real time PCR

Indexed keywords

PROTEOME; VEGETABLE PROTEIN;

ARTICLE; BRASSICA; GENE EXPRESSION REGULATION; GENETICS; HOST PARASITE INTERACTION; IMMUNOLOGY; INNATE IMMUNITY; PARASITOLOGY; PLANT DISEASE;

BRASSICA; GENE EXPRESSION REGULATION, PLANT; HOST-PARASITE INTERACTIONS; IMMUNITY, INNATE; PLANT DISEASES; PLANT PROTEINS; PROTEOME;

ALBUGINACEAE; ALBUGO CANDIDA; BRASSICA; BRASSICA JUNCEA; BRASSICA NAPUS; BRASSICA NAPUS VAR. NAPUS; CANDIDA; OOMYCETES;

EID: 79251520279     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erq365     Document Type: Article

References (75)

1. Alvarez ME, Pennel RI, Meijer P-J, Ishikawa A, Dixon RA, Lamb C. 1998. Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92, 773-784.
2. Antoniw JF, Pierpoint WS. 1978. Purification of tobacco leaf protein associated with resistance to virus infection. Biochemical Society Transactions 6, 248-250.
3. Barbetti MJ. 1981. Effects of sowing date and oospore seed contamination upon subsequent crop incidence of white rust (Albugo candida) in rapeseed. Australasian Plant Pathology 10, 44-46.
4. Bari R, Pant BD, Stitt M, Scheible WR. 2006. PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiology 141, 988-999.
5. Bartling D, Radzio R, Steiner U, Weiler EW. 1993. A glutathione S-transferase with glutathione peroxidase activity from Arabidopsis thaliana: molecular cloning and functional characterization. European Journal of Biochemistry 216, 579-586.
6. Belhaj K, Lin BQ, Mauch F. 2009. The chloroplast protein RPH1 plays a role in the immune response of Arabidopsis to Phytophthora brassicae. The Plant Journal 58, 287-298.
7. Berhane K, Widersten M, Engstrom A, Kozarich J, Mannervik B. 1994. Detoxication of base propenals and other a, b-unsaturated aldehyde products of radical reactions and lipid peroxidation by human glutathione S-transferases. Proceedings of the National Academy of Sciences, USA 91, 1480-1484.
8. Bernier CC. 1972. Diseases of rapeseed in Manitoba in 1971. Canadian Plant Disease Survey 52, 108.
9. Bringans S, Eriksen S, Kendrick T, Gopalakrishnakone P, Livk A, Lock R, Lipscombe R. 2008. Proteomic analyses of the venom of Heterometrus longimanus (Asian black scorpion) Proteomics 8, 1081-1096.
10. Coaker G, Falick A, Staskawicz B. 2005. Activation of a phytopathogenic bacterial effector protein by a eukaryotic cyclophilin. Science 308, 548-550.
11. Coca MA, Damsz B, Yun DJ, Hasegawa PM, Bressan RA, Narasimhan ML. 2000. Heterotrimeric G-proteins of a filamentous fungus regulate cell wall composition and susceptibility to a plant PR-5 protein. The Plant Journal 22, 61-69.
12. De Gara L, de Pinto MC, Tommasi F. 2003. The antioxidant systems vis-a-vis reactive oxygen species during plant-pathogen interaction. Plant Physiology and Biochemistry 41, 863-870.
13. Dietz KJ, Jacob S, Oelze ML, Laxa M, Tognetti V, de Miranda SMN, Baier M, Finkemeier I. 2006. The function of peroxiredoxins in plant organelle redox metabolism. Journal of Experimantal Botany 57, 1697-1709.
14. Dixon DP, Skipsey M, Edwards R. 2010. Roles for glutathione transferases in plant secondary metabolism. Phytochemistry 71, 338-350.
15. Dominguez-Solis JR, Zengyong H, Amparo L, Julie T, Buchanan BB, Sheng L. 2008. A cyclophilin links redox and light signals to cysteine biosynthesis and stress responses in chloroplasts. Proceedings of the National Academy of Sciences, USA 105, 16386-16391.
16. Dudler R, Hertig C, Rebman G, Bull J, Mauch F. 1991. A pathogen-induced wheat gene encodes a protein homologous to glutathione S-transferases. Molecular Plant-Microbe Interactions 4, 4-18.
17. El-Zahaby HM, Gullner G, Király Z. 1995. Effects of powdery mildew infection of barley on the ascorbate-glutathione cycle and other antioxidants in different host-pathogen interactions. Phytopathology 85, 1225-1230.
18. Epple P, Vignutelli A, Apel K, Bohlmann H. 1998. Differential induction of the Arabidopsis thaliana Thi21 gene by Fusarium oxysporum F.sp. matthiolae. Molecular Plant-Microbe Interactions 11, 523-529.
19. Fodor J, Gullner G, Adam AL, Barna B, Komives T, Kiraly Z. 1997. Local and systemic responses of antioxidant to tobacco mosaic virus infection and to salicylic acid in tobacco. Plant Physiology 114, 1443-1451.
20. Fernandez AP, Strand A. 2008. Retrograde signaling and plant stress: plastid signals initiate cellular stress responses. Current Opinion in Plant Biology 11, 509-513.
21. Foyer CH, Noctor G. 2000. Oxygen processing in photosynthesis: regulation and signalling. New Phytologist 146, 359-388.
22. Fridovich I. 1986. Superoxide dismutases. Advances in Enzymology and Related Areas of Molecular Biology 58, 61-97.
23. Glazebrook J. 2005. Contrasting mechanisms of defence against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology 43, 205-227.
24. Grenier JC, Potvin Asselin A. 1993. Barley pathogenesis-related proteins with fungal cell wall lytic activity inhibit the growth of yeasts. Plant Physiology 103, 1277-1283.
25. Halliwell B, Gutteridge JMC. 1989. Free radicals in biology and medicine, 2nd edn. Oxford, UK: Oxford University Press.
26. Heeg C, Kruse C, Jost R, Gutensohn M, Ruppert T, Wirtz M, Hell R. 2008. Analysis of the Arabidopsis O-acetylserine (thiol) lyase gene family demonstrates compartment-specific differences in the regulation of cysteine synthesis. The Plant Cell 20, 168-185.
27. Holub EB, Brose E, Tör M, Clay C, Crute IR, Beynon JL. 1995. Phenotypic and genotypic variation in the interaction between Arabidopsis thaliana and Albugo candida. Molecular Plant-Microbe Interactions 8, 916-928.
28. Ibeas JI, Lee H, Damsz B, Prasad DT, Pardo JM, Hasegawa PM, Bressan RA, Narasimhan ML. 2000. Fungal cell wall phosphomannans facilitate the toxic activity of a plant PR-5 protein. The Plant Journal 23, 375-383.
29. Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444, 323-329.
30. Jost R, Altschmied L, Bloem E, Bogs J, Gershenzon J, Hä hnel U, Hänsch R, Hartmann T, Kopriva S, Kruse C. 2005. Expression profiling of metabolic genes in response to methyl jasmonate reveals regulation of genes of primary and secondary sulfur-related pathways in Arabidopsis thaliana. Photosynthesis Research 86, 491-508.
31. Kaur P, Sivasithamparam K, Barbetti MJ. 2008. Pathogenic behaviour of strains of Albugo candida from Brassica juncea and Raphanus raphanistrum (wild radish) in Western Australia. Australasian Plant Pathology 37, 353-356.
32. Kliebenstein DJ, Monde R-A, Last RL. 1998. Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. Plant Physiology 118, 637-650.
33. Kromina KA, Ignatov AN, Abdeeva IA, Adhikari TB. 2008. Role of peptidyl-prolyl cis/trans isomerases in pathological processes. Memory Cell Biology 2, 195-202.
34. Kruse C, Jost R, Lipschis M, Kopp B, Hartmann M, Hell R. 2007. Sulfur-enhanced defence: effects of sulfur metabolism, nitrogen supply, and pathogen lifestyle. Plant Biology 9, 608-619.
35. Lakra BS, Saharan GS. 1989. Correlation of leaf and staghead infection intensities of white rust with yield and yield components of mustard. Indian Journal of Mycology and Plant Pathology 19, 279-281.
36. Laloi C, Stachowiak M, Pers-Kamczyc E, Warzych E, Murgia I, Apel K. 2007. Cross-talk between singlet oxygen- and hydrogen peroxide-dependent signaling of stress responses in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 104, 672-677.
37. Lamb C, Dixon R. 1997. The oxidative burst in plant disease resistance. Annual Review of Plant Physiology and Plant Molecular Biology 48, 251-275.
38. Li CX, Sivasithamparam K, Walton G, et al. 2007a. Expression and relationships of resistance to white rust (Albugo candida) at cotyledonary, seedling and flowering stages in Brassica juncea germplasm from Australia, China, and India. Australian Journal of Agricultural Research 58, 259-264.
39. Li CX, Sivasithamparam K, Walton G, et al. 2007b. Identification of resistance to Albugo candida in Indian, Australian and Chinese Brassica juncea genotypes. In: Proceedings of the 10th International Rapeseed Congress, Wuhan, China. March 1, 408-410.
40. Li CX, Sivasithamparam K, Walton G, Fels P, Barbetti MJ. 2008. Both incidence and severity of white rust disease reflect host resistance in Brassica juncea germplasm from Australia, China and India, screened using artificial or natural inoculum in field trials as well as in glasshouse trials. Field Crops Research 106, 1-8.
41. Mach JM, Castillo AR, Hoogstraten R, Greenberg JT. 2001. The Arabidopsis-accelerated cell death gene ACD2 encodes red chlorophyll catabolite reductase and suppresses the spread of disease symptoms. Proceedings of the National Academy of Sciences, USA 98, 771-776.
42. Marrs KA. 1996. The functions and regulation of glutathione S-transferases in plants. Annual Review of Plant Biology 47, 127-158.
43. Miller G, Suzuki N, Rizhsky L, Hegie A, Koussevitzky S, Mittler R. 2007. Double mutants deficient in cytosolic and thylakoid ascorbate peroxidase reveal a complex mode of interaction between reactive oxygen species, plant development, and response to abiotic stresses. Plant Physiology 144, 1777-1785.
44. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F. 2004. Reactive oxygen gene network of plants. Trends in Plant Science 9, 490-498.
45. Motohashi K, Koyama F, Nakanishi Y, Ueoka-Nakanishi H, Hisabori T. 2003. Chloroplast cyclophilin is a target protein of thioredoxin. Journal of Biological Chemistry 278, 31848-31852.
46. Noctor G, Foyer CH. 1998. Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Physiology and Plant Molecular Biology 49, 249-279.
47. Noji M, Saito M, Nakamura M, Aono M, Saji H, Saito K. 2001. Cysteine synthase overexpression in tobacco confers tolerance to sulfur-containing environment pollutants. Plant Physiology 126, 973-980.
48. Peterson GL. 1983. Determination of total protein. Methods in Enzymology 91, 95-119.
49. Pickett CB, Lu AYH. 1989. Glutathione S-transferases: gene structure, regulation, and biological function. Annual Review of Biochemistry 58, 743-764.
50. Pruzinska A, Anders I, Aubry S, Schenk N, Tapernoux-Luthi E, Muller T, Krautler B, Hortensteiner S. 2007. In vivo participation of red chlorophyll catabolite reductase in chlorophyll breakdown. The Plant Cell 19, 369-387.
51. Ramakers C, Ruijter JM, Deprez RH, Moorman AF. 2003. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neuroscience Letters 339, 62-66.
52. Richardson M, Valdes-Rodriquez S, Blanco-Labra A. 1987. A possible function for thaumatin and a TMV-induced protein suggested by homology to a maize inhibitor. Nature 327, 432-434.
53. Roberts W, Selitrennikoff CP. 1990. Zeamatin, an antifungal protein from maize with membrane-permeabilizing activity. Journal of General Microbiology 136, 1771-1778.
54. Rodoni S, Vicentini F, Schellenberg M, Matile P, Hortensteiner S. 1997. Partial purification and characterization of red chlorophyll catabolite reductase, a stroma protein involved in chIorophyll breakdown. Plant Physiology 115, 677-682.
55. Sappl PG, Carroll AJ, Clifton R, Lister R, Whelan J, Millar AH, Singh KB. 2009. The Arabidopsis glutathione transferase gene family displays complex stress regulation and co-silencing multiple genes results in altered metabolic sensitivity to oxidative stress. The Plant Journal 58, 53-68.
56. Selitrennikoff CP. 2001. Antifungal proteins. Applied and Environmental Microbiology 67, 2883-2894.
57. Sharma N, Rahman MH, Strelkov S, Thiagarajah M, Bansal VK, Kav NNV. 2007. Proteome-level changes in two Brassica napus varieties exhibiting differential responses to the fungal pathogen Alternaria brassicae. Plant Science 172, 95-110.
58. Sogin ML, Silberman JD. 1998. Evolution of the protists and protistan parasites from the perspective of molecular systematics. International Journal of Parasitology 28, 11-20.
59. Sokhi SS, Khangura RK. 1992. White rust of rapeseed and mustard. Punjab Agricultural University, Ludhiana, DR/Publ. 92/23.
60. Strohm M, Jouanin L, Kunert KJ, Pruvost C, Polle A, Foyer CH, Rennenberg H. 1995. Regulation of glutathione synthesis in leaves of transgenic poplar (Populus tremula3P. alba) overexpressing glutathione synthetase. The Plant Journal 7, 141-145.
61. Trudel J, Grenier J, Potvin C, Asselin A. 1998. Several thaumatin like proteins bind to b-1,3-glucans. Plant Physiology 118, 1431-1438.
62. Van Breusegem F, Dat JF. 2006. Reactive oxygen species in plant cell death. Plant Physiology 141, 384-390.
63. Vanacker H, Carver TLW, Foyer CH. 1998. Pathogen-induced changes in the antioxidant status of the apoplast in barley leaves. Plant Physiology 117, 1103-1114.
64. Vanacker H, Foyer CH, Carver TLW. 1999. Changes in apoplastic antioxidants induced by powdery mildew attack in oat genotypes with race non-specific resistance. Planta 208, 444-452.
65. Van Loon LC. 1997. Induced resistance in plants and the role of pathogenesis-related proteins. European Journal of Plant Pathology 102, 753-765.
66. Van Loon LC, Pierpoint WS, Boller T, Conejero V. 1994. Recommendations for naming plant pathogenesis-related proteins. Plant Molecular Biology Reporter 12, 245-264.
67. Verma PR, Petrie GA. 1980. Effect of seed infestation and flower bud inoculation on systemic infection of turnip rape by Albugo candida. Canadian Journal of Plant Science 60, 267-271.
68. Wang X, Zafian P, Choudhary M, Lawton M. 1996. The PR5K receptor protein kinase from Arabidopsis thaliana is structurally related to a family of plant defence proteins. Proceedings of the National Academy of Sciences, USA 93, 2598-2602.
69. Wachter A, Wolf S, Steininger H, Bogs J, Rausch T. 2005. Differential targeting of GSH1 and GSH2 is achieved by multiple transcription initiation: implications for the compartmentation of glutathione biosynthesis in the Brassicaceae. The Plant Journal 41, 15-30.
70. Williamson G, Beverley MC. 1987. The purification of acidic glutathione S-transferases from pea seeds and their activity with lipid peroxidation products. Biochemical Society Transactions 15, 1103-1104.
71. Williams PH. 1985. Crucifer genetics cooperative (CRGC) resource book. University Wisconsin, USA: Department of Plant Pathology.
72. Wirtz M, Hell R. 2007. Dominant-negative modification reveals the regulatory function of the multimeric cysteine synthase protein complex in transgenic tobacco. The Plant Cell 19, 625-639.
73. Wuthrich KL, Bovet L, Hunziker PE, Donnison IS, Hortensteiner S. 2000. Molecular cloning, functional expression and characterisation of RCC reductase involved in chlorophyll catabolism. The Plant Journal 21, 189-198.
74. Yajima W, Hall JC, Kav NNV. 2004. Proteome-level differences between auxinic herbicide-susceptible and -resistant wild mustard (Sinapis arvensis L.). Journal of Agricultural and Food Chemistry 52, 5063-5070.
75. Yang B, Srivastava S, Deyholos MK, Kav NNV. 2007. Transcriptional profiling of canola (Brassica napus L.) responses to the fungal pathogen Sclerotinia sclerotiorum. Plant Science 173, 156-171.