HYR1-mediated detoxification of reactive oxygen species is required for full virulence in the rice blast fungus

PLoS Pathogens

Volumn 7, Issue 4, 2011, Pages

  Huang, Kun ^a   Czymmek, Kirk J ^a   Caplan, Jeffrey L ^a   Sweigard, James A ^b   Donofrio, Nicole M ^a  

^a UNIVERSITY OF DELAWARE   (United States)

^b DUPONT COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTATHIONE PEROXIDASE; HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE; FUNGAL PROTEIN; VIRULENCE FACTOR;

ARTICLE; BARLEY; CELL WALL; CONTROLLED STUDY; DELETION MUTANT; DETOXIFICATION; FUNGAL GENE; FUNGAL VIRULENCE; FUNGUS MUTANT; GENE EXPRESSION; GENE INTERACTION; GROWTH INHIBITION; MAGNAPORTHE GRISEA; MAGNAPORTHE ORYZAE; MOHYR1 GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; RICE; WILD TYPE; YEAST; ENZYMOLOGY; GENETICS; MAGNAPORTHE; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PLANT DISEASE;

FUNGI; HORDEUM; MAGNAPORTHE GRISEA; MAGNAPORTHE ORYZAE;

FUNGAL PROTEINS; GLUTATHIONE PEROXIDASE; HYDROGEN PEROXIDE; MAGNAPORTHE; ORYZA SATIVA; PLANT DISEASES; VIRULENCE FACTORS;

EID: 79955769322     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001335     Document Type: Article

References (45)

1. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F, (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9: 490-498.
2. Rogers SA, (2002) Detoxify or Die. Sarasota, FL Sand Key Company, Inc.
3. Thannickal VJ, Fanburg BL, (2000) Reactive oxygen species in cell signaling. Am J Physiol Lung Cell Mol Physiol 279: L1005-L1028.
4. Jones JDG, Dangl JL, (2006) The plant immune system. Nature 444: 323-329.
5. Egan MJ, Wang ZY, Jones MA, Smirnoff N, Talbot NJ, (2007) Generation of reactive oxygen species by fungal NADPH oxidases is required for rice blast disease. Proc Natl Acad Sci U S A 104: 11772-11777.
6. Skamnioti P, Henderson C, Zhang ZG, Robinson Z, Gurr SJ, (2007) A novel role for catalase B in the maintenance of fungal cell-wall integrity during host invasion in the rice blast fungus Magnaporthe grisea. Mol Plant-Microbe Interact 20: 568-580.
7. Neill S, Desikan R, Hancock J, (2002) Hydrogen peroxide signalling. Curr Opin Plant Biol 5: 388-395.
8. Sagi M, Davydov O, Orazova S, Yesbergenova Z, Ophir R, et al. (2004) Plant respiratory burst oxidase homologs impinge on wound responsiveness and development in Lycopersicon esculentum. Plant Cell 16: 616-628.
9. Parker D, Beckmann M, Zubair H, Enot DP, Caracuel-Rios Z, et al. (2009) Metabolomic analysis reveals a common pattern of metabolic re-programming during invasion of three host plant species by Magnaporthe grisea. Plant J 59: 723-737.
10. Shetty NP, Mehrabi R, Lutken H, Haldrup A, Kema GHJ, et al. (2007) Role of hydrogen peroxide during the interaction between the hemibiotrophic fungal pathogen Septoria tritici and wheat. New Phytol 174: 637-647.
11. Able AJ, (2003) Role of reactive oxygen species in the response of barley to necrotrophic pathogens. Protoplasma 221: 137-143.
12. Galletti R, Denoux C, Gambetta S, Dewdney J, Ausubel FM, et al. (2008) The AtrbohD-Mediated Oxidative Burst Elicited by Oligogalacturonides in Arabidopsis Is Dispensable for the Activation of Defense Responses Effective against Botrytis cinerea. Plant Physiol 148: 1695-1706.
13. Kato T, Tanabe S, Nishimura M, Ohtake Y, Nishizawa Y, et al. (2009) Differential responses of rice to inoculation with wild-type and non-pathogenic mutants of Magnaporthe oryzae. Plant Mol Biol 70: 617-625.
14. Chi MH, Park SY, Kim S, Lee YH, (2009) A Novel Pathogenicity Gene Is Required in the Rice Blast Fungus to Suppress the Basal Defenses of the Host. PLoS Path 5: e1000401.
15. Tanabe S, Nishizawa Y, Minami E, (2009) Effects of catalase on the accumulation of H2O2 in rice cells inoculated with rice blast fungus, Magnaporthe oryzae. Physiol Plant 137: 148-154.
16. Kim KH, Willger SD, Park SW, Puttikamonkul S, Grahl N, et al. (2009) TmpL, a Transmembrane Protein Required for Intracellular Redox Homeostasis and Virulence in a Plant and an Animal Fungal Pathogen. PLoS Path 5: e1000653.
17. Inoue Y, Matsuda T, Sugiyama K, Izawa S, Kimura A, (1999) Genetic analysis of glutathione peroxidase in oxidative stress response of Saccharomyces cerevisiae. J Biol Chem 274: 27002-27009.
18. Zhang WJ, He YX, Yang Z, Yu J, Chen Y, et al. (2008) Crystal structure of glutathione-dependent phospholipid peroxidase Hyr1 from the yeast Saccharomyces cerevisiae. Proteins 73: 1058-1062.
19. Delaunay A, Pflieger D, Barrault MB, Vinh J, Toledano MB, (2002) A thiol peroxidase is an H2O2 receptor and redox-transducer in gene activation. Cell 111: 471-481.
20. Molina L, Kahmann R, (2007) An Ustilago maydis gene involved in H2O2 detoxification is required for virulence. Plant Cell 19: 2293-2309.
21. Delaunay A, Isnard AD, Toledano MB, (2000) H2O2 sensing through oxidation of the Yap1 transcription factor. EMBO J 19: 5157-5166.
22. Lee J, Godon C, Lagniel G, Spector D, Garin J, et al. (1999) Yap1 and Skn7 control two specialized oxidative stress response regulons in yeast. J Biol Chem 274: 16040-16046.
23. Lev S, Hadar R, Amedeo P, Baker SE, Yoder OC, et al. (2005) Activation of an AP1-like transcription factor of the maize pathogen Cochliobolus heterostrophus in response to oxidative stress and plant signals. Eukaryot Cell 4: 443-454.
24. Levine A, Tenhaken R, Dixon R, Lamb C, (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79: 583-593.
25. Lin CH, Yang SL, Chung KR, (2009) The YAP1 Homolog-Mediated Oxidative Stress Tolerance Is Crucial for Pathogenicity of the Necrotrophic Fungus Alternaria alternata in Citrus. Mol Plant-Microbe Interact 22: 942-952.
26. Temme N, Tudzynski P, (2009) Does Botrytis cinerea Ignore H2O2-Induced Oxidative Stress During Infection? Characterization of Botrytis Activator Protein 1. Mol Plant-Microbe Interact 22: 987-998.
27. McGuffin LJ, Bryson K, Jones DT, (2000) The PSIPRED protein structure prediction server. Bioinformatics 16: 404.
28. Martin JL, (1995) Thioredoxin- a Fold for All Reasons. Structure 3: 245-250.
29. Valent B, Farrall L, Chumley FG, (1991) Magnaporthe-grisea Genes for Pathogenicity and Virulence Identified through a Series of Backcrosses. Genetics 127: 87-101.
30. Howard RJ, Valent B, (1996) Breaking and entering: Host penetration by the fungal rice blast pathogen Magnaporthe grisea. Annu Rev Microbiol 50: 491-512.
31. Myhre O, Andersen JM, Aarnes H, Fonnum F, (2003) Evaluation of the probes 2 ′,7 ′-dichlorofluorescin diacetate, luminol, and lucigenin as indicators of reactive species formation. Biochem Pharmacol 65: 1575-1582.
32. Kang SH, Khang CH, Lee YH, (1999) Regulation of cAMP-dependent protein kinase during appressorium formation in Magnaporthe grisea. FEMS Microbiol Lett 170: 419-423.
33. Smirnoff N, (2000) Ascorbic acid: metabolism and functions of a multi-facetted molecule. Curr Opin Plant Biol 3: 229-235.
34. Huckelhoven R, (2007) Cell wall- Associated mechanisms of disease resistance and susceptibility. Annu Rev Phytopathol 45: 101-127.
35. Dai SH, Wei XP, Alfonso AA, Pei LP, Duque UG, et al. (2008) Transgenic rice plants that overexpress transcription factors RF2a and RF2b are tolerant to rice tungro virus replication and disease. Proc Natl Acad Sci U S A 105: 21012-21016.
36. Bolwell GP, Bindschedler LV, Blee KA, Butt VS, Davies DR, et al. (2002) The apoplastic oxidative burst in response to biotic stress in plants: a three-component system. J Exp Bot 53: 1367-1376.
37. Trujillo M, Altschmied L, Schweizer P, Kogel KH, Huckelhoven R, (2006) Respiratory Burst Oxidase Homologue A of barley contributes to penetration by the powdery mildew fungus Blumeria graminis f. sp hordei. J Exp Bot 57: 3781-3791.
38. Davies DR, Bindschedler LV, Strickland TS, Bolwell GP, (2006) Production of reactive oxygen species in Arabidopsis thaliana cell suspension cultures in response to an elicitor from Fusarium oxysporum: implications for basal resistance. J Exp Bot 57: 1817-1827.
39. Lessing F, Kniemeyer O, Wozniok W, Loeffler J, Kurzai O, et al. (2007) The Aspergillus fumigatus transcriptional regulator AfYap1 represents the major regulator for defense against reactive oxygen intermediates but is dispensable for pathogenicity in an intranasal mouse infection model. Eukaryot Cell 6: 2290-2302.
40. Khang CH, Berruyer R, Giraldo MC, Kankanala P, Park SY, et al. (2010) Translocation of Magnaporthe oryzae Effectors into Rice Cells and Their Subsequent Cell-to-Cell Movement. Plant Cell 22: 1388-1403.
41. Sweigard JA, Chumley FG, Valent B, (1992) Disruption of a Magnaporthe-Grisea Cutinase Gene. Mol Gen Genet 232: 183-190.
42. Mosquera G, Giraldo MC, Khang CH, Coughlan S, Valent B, (2009) Interaction Transcriptome Analysis Identifies Magnaporthe oryzae BAS1-4 as Biotrophy-Associated Secreted Proteins in Rice Blast Disease. Plant Cell 21: 1273-1290.
43. Patterson GH, Piston DW, Barisas BG, (2000) Forster distances between green fluorescent protein pairs. Anal Biochem 284: 438-440.
44. ThordalChristensen H, Zhang ZG, Wei YD, Collinge DB, (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11: 1187-1194.
45. Fink JL, Hamilton N, (2007) DomainDraw: A macromolecular feature drawing program. In Silico Biol 7: 145-150.