PdeH, a high-affinity camp phosphodiesterase, is a key regulator of asexual and pathogenic differentiation in magnaporthe oryzae

PLoS Pathogens

Volumn 6, Issue 5, 2010, Pages 1-23

  Ramanujam, Ravikrishna ^a,b   Naqvi, Naweed I ^a,b,c  

^a TEMASEK LIFE SCIENCES LABORATORY   (Singapore)

^b NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIC AMP PHOSPHODIESTERASE; PROTEIN PDEH; PROTEIN PDEL; UNCLASSIFIED DRUG; 8 BROMO CYCLIC AMP; EXONUCLEASE; FUNGAL PROTEIN; PHOSPHODIESTERASE I; SPLEEN EXONUCLEASE;

ARTICLE; CONIDIUM; CONTROLLED STUDY; DELETION MUTANT; DEVELOPMENTAL STAGE; ENZYME ACTIVITY; ENZYME LOCALIZATION; FUNGAL COLONIZATION; FUNGAL PLANT DISEASE; FUNGAL VIRULENCE; FUNGUS GROWTH; MAGNAPORTHE; MAGNAPORTHE ORYZAE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN FUNCTION; RICE; SIGNAL TRANSDUCTION; VEGETATIVE GROWTH; WILD TYPE; AMINO ACID SEQUENCE; CELL MEMBRANE; CELL NUCLEUS; CYTOPLASM; DRUG EFFECT; ENZYMOLOGY; FUNGUS HYPHAE; FUNGUS SPORE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MUTAGENESIS; PHYSIOLOGY; PLANT DISEASE;

MAGNAPORTHE GRISEA; MAGNAPORTHE ORYZAE;

8-BROMO CYCLIC ADENOSINE MONOPHOSPHATE; AMINO ACID SEQUENCE; CELL MEMBRANE; CELL NUCLEUS; CYCLIC AMP; CYTOPLASM; EXONUCLEASES; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, FUNGAL; HYPHAE; MAGNAPORTHE; MOLECULAR SEQUENCE DATA; MUTAGENESIS; ORYZA SATIVA; PHOSPHODIESTERASE I; PLANT DISEASES; SIGNAL TRANSDUCTION; SPORES, FUNGAL;

EID: 77954156711     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000897     Document Type: Article

References (110)

1. Pierce K, Premont R, Lefkowitz R (2002) Seven-transmembrane receptors. Nature Reviews Molecular Cell Biology: 639-650.
2. Houslay MD, Baillie GS, Maurice DH (2007) cAMP-Specific phosphodiesterase-4 enzymes in the cardiovascular system: a molecular toolbox for generating compartmentalized cAMP signaling. Circ Res 100: 950-966.
3. Beavo J, Francis SH, Houslay M, eds. (2006) Cyclic nucleotide Phosphodiesterases in Health and Disease. CRC Press,Boca Raton,Florida.
4. Houslay MD, Milligan G (1997) Tailoring cAMP-signalling responses through isoform multiplicity. Trends Biochem Sci 22: 217-224.
5. Houslay MD (2001) PDE4 cAMP-specific phosphodiesterases. Prog Nucleic Acid Res Mol Biol 69: 249-315.
6. Houslay MD, Sullivan M, Bolger GB (1998) The multienzyme PDE4 cyclic adenosine monophosphate-specific phosphodiesterase family: intracellular targeting, regulation, and selective inhibition by compounds exerting anti-inflammatory and antidepressant actions. Adv Pharmacol 44: 225-342.
7. Hu Y, Liu E, Bai X, Zhang A (2009) The localization and concentration of the PDE2-encoded high-affinity cAMP phosphodiesterase is regulated by cAMPdependent protein kinase A in the yeast Saccharomyces cerevisiae. FEMS Yeast Res.
8. Namy O, Duchateau-Nguyen G, Rousset JP (2002) Translational readthrough of the PDE2 stop codon modulates cAMP levels in Saccharomyces cerevisiae. Mol Microbiol 43: 641-652.
9. Bender AT, Beavo JA (2006) Cyclic nucleotide phosphodiesterases: molecular regulation to clinical use. Pharmacol Rev 58: 488-520.
10. Cooper DM (2003) Regulation and organization of adenylyl cyclases and cAMP. Biochem J 375: 517-529.
11. Omori K, Kotera J (2007) Overview of PDEs and their Regulation. Circulation research 100: 309-327.
12. Conti M, Beavo J (2007) Biochemistry and physiology of cyclic nucleotide phosphodiesterases: essential components in cyclic nucleotide signaling. Annu Rev Biochem 76: 481-511.
13. Lemaire K, Van de Velde S, Van Dijck P, Thevelein JM (2004) Glucose and sucrose act as agonist and mannose as antagonist ligands of the G proteincoupled receptor Gpr1 in the yeast Saccharomyces cerevisiae. Mol Cell 16: 293-299.
14. Jones DL, Petty J, Hoyle DC, Hayes A, Oliver SG, et al. (2004) Genome-Wide Analysis of the Effects of Heat Shock on a Saccharomyces cerevisiae Mutant With a Constitutively Activated cAMP-Dependent Pathway. Comp Funct Genomics 5: 419-431.
15. Jones DL, Petty J, Hoyle DC, Hayes A, Ragni E, et al. (2003) Transcriptome profiling of a Saccharomyces cerevisiae mutant with a constitutively activated Ras/ cAMP pathway. Physiol Genomics 16: 107-118.
16. Pan X, Heitman J (1999) Cyclic AMP-dependent protein kinase regulates pseudohyphal differentiation in Saccharomyces cerevisiae. Mol Cell Biol 19: 4874-4887.
17. Park JI, Grant CM, Dawes IW (2005) The high-affinity cAMP phosphodiesterase of Saccharomyces cerevisiae is the major determinant of cAMP levels in stationary phase: involvement of different branches of the Ras-cyclic AMP pathway in stress responses. Biochem Biophys Res Commun 327: 311-319.
18. Schneper L, Krauss A, Miyamoto R, Fang S, Broach JR (2004) The Ras/ protein kinase A pathway acts in parallel with the Mob2/Cbk1 pathway to effect cell cycle progression and proper bud site selection. Eukaryot Cell 3: 108-120.
19. Davey J (1998) Fusion of a fission Yeast. Yeast: 1529-1566.
20. Yamamoto M (1996) The molecular control mechanisms of meiosis in fission yeast. Trends Biochemical Sciences: 18-22.
21. DeVoti JSG, Beach D, McLeod M (1991) Interaction between ran1+ protein kinase and cAMP dependent protein kinase as negative regulators of fission yeast meiosis. EMBO J: 3759-3768.
22. Higuchi T, Watanabe Y, Yamamoto M (2002) Protein kinase A regulates sexual development and gluconeogenesis through phosphorylation of the Zn finger transcriptional activator Rst2p in fission yeast. Mol Cell Biol 22: 1-11.
23. Bahn YS, Staab J, Sundstrom P (2003) Increased high-affinity phosphodiesterase PDE2 gene expression in germ tubes counteracts CAP1-dependent synthesis of cyclic AMP, limits hypha production and promotes virulence of Candida albicans. Mol Microbiol 50: 391-409.
24. Jung WH, Stateva LI (2003) The cAMP phosphodiesterase encoded by CaPDE2 is required for hyphal development in Candida albicans. Microbiology 149: 2961-2976.
25. Jung WH, Warn P, Ragni E, Popolo L, Nunn CD, et al. (2005) Deletion of PDE2, the gene encoding the high-affinity cAMP phosphodiesterase, results in changes of the cell wall and membrane in Candida albicans. Yeast 22: 285-294.
26. Harcus D, Nantel A, Marcil A, Rigby T, Whiteway M (2004) Transcription profiling of cyclic AMP signaling in Candida albicans. Mol Biol Cell 15: 4490-4499.
27. Bahn YS, Molenda M, Staab JF, Lyman CA, Gordon LJ, et al. (2007) Genomewide transcriptional profiling of the cyclic AMP-dependent signaling pathway during morphogenic transitions of Candida albicans. Eukaryot Cell 6: 2376-2390.
28. Hu G, Steen BR, Lian T, Sham AP, Tam N, et al. (2007) Transcriptional regulation by protein kinase A in Cryptococcus neoformans. PLoS Pathog 3: e42. doi:10.1371/journal.ppat.0030042.
29. D'Souza CA, Heitman J (2001) Conserved cAMP signaling cascades regulate fungal development and virulence. FEMS Microbiol Rev 25: 349-364.
30. Hicks JK, Bahn YS, Heitman J (2005) Pde1 phosphodiesterase modulates cyclic AMP levels through a protein kinase A-mediated negative feedback loop in Cryptococcus neoformans. Eukaryot Cell 4: 1971-1981.
31. Alspaugh JA, Perfect JR, Heitman J (1997) Cryptococcus neoformans mating and virulence are regulated by the G-protein alpha subunit GPA1 and cAMP. Genes Dev 11: 3206-3217.
32. Kozubowski L, Lee SC, Heitman J (2009) Signalling pathways in the pathogenesis of Cryptococcus. Cell Microbiol 11: 370-380.
33. Pukkila-Worley R, Alspaugh JA (2004) Cyclic AMP signaling in Cryptococcus neoformans. FEMS Yeast Res 4: 361-367.
34. Larraya LM, Boyce KJ, So A, Steen BR, Jones S, et al. (2005) Serial analysis of gene expression reveals conserved links between protein kinase A, ribosome biogenesis, and phosphate metabolism in Ustilago maydis. Eukaryot Cell 4: 2029-2043.
35. Regenfelder E, Spellig T, Hartmann A, Lauenstein S, Bolker M, et al. (1997) G proteins in Ustilago maydis: transmission of multiple signals? EMBO J 16: 1934-1942.
36. Durrenberger F, Wong K, Kronstad JW (1998) Identification of a cAMPdependent protein kinase catalytic subunit required for virulence and morphogenesis in Ustilago maydis. Proc Natl Acad Sci U S A 95: 5684-5689.
37. Gold SE, Brogdon SM, Mayorga ME, Kronstad JW (1997) The Ustilago maydis regulatory subunit of a cAMP-dependent protein kinase is required for gall formation in maize. Plant Cell 9: 1585-1594.
38. Lee N, Kronstad JW (2002) ras2 Controls morphogenesis, pheromone response, and pathogenicity in the fungal pathogen Ustilago maydis. Eukaryot Cell 1: 954-966.
39. Banno S, Ochiai N, Noguchi R, Kimura M, Yamaguchi I, et al. (2005) A catalytic subunit of cyclic AMP-dependent protein kinase, PKAC-1, regulates asexual differentiation in Neurospora crassa. Genes Genet Syst 80: 25-34.
40. Bencina M, Panneman H, Ruijter GJ, Legisa M, Visser J (1997) Characterization and overexpression of the Aspergillus niger gene encoding the cAMPdependent protein kinase catalytic subunit. Microbiology 143 (Pt 4): 1211-1220.
41. Brakhage AA, Liebmann B (2005) Aspergillus fumigatus conidial pigment and cAMP signal transduction: significance for virulence. Med Mycol 43 Suppl 1: S75-82.
42. Grosse C, Heinekamp T, Kniemeyer O, Gehrke A, Brakhage AA (2008) Protein kinase A regulates growth, sporulation, and pigment formation in Aspergillus fumigatus. Appl Environ Microbiol 74: 4923-4933.
43. Ivey FD, Kays AM, Borkovich KA (2002) Shared and independent roles for a Galpha(i) protein and adenylyl cyclase in regulating development and stress responses in Neurospora crassa. Eukaryot Cell 1: 634-642.
44. Kays AM, Rowley PS, Baasiri RA, Borkovich KA (2000) Regulation of conidiation and adenylyl cyclase levels by the Galpha protein GNA-3 in Neurospora crassa. Mol Cell Biol 20: 7693-7705.
45. Kays AM, Borkovich KA (2004) Severe impairment of growth and differentiation in a Neurospora crassa mutant lacking all heterotrimeric G alpha proteins. Genetics 166: 1229-1240.
46. Liebmann B, Muller M, Braun A, Brakhage AA (2004) The cyclic AMPdependent protein kinase a network regulates development and virulence in Aspergillus fumigatus. Infect Immun 72: 5193-5203.
47. Saudohar M, Bencina M, van de Vondervoort PJ, Panneman H, Legisa M, et al. (2002) Cyclic AMP-dependent protein kinase is involved in morphogenesis of Aspergillus niger. Microbiology 148: 2635-2645.
48. Liebmann B, Gattung S, Jahn B, Brakhage AA (2003) cAMP signaling in Aspergillus fumigatus is involved in the regulation of the virulence gene pksP and in defense against killing by macrophages. Mol Genet Genomics 269: 420-435.
49. Lafon A, Han KH, Seo JA, Yu JH, d'Enfert C (2006) G-protein and cAMPmediated signaling in Aspergilli: a genomic perspective. Fungal Genet Biol 43: 490-502.
50. Uno I, Matsumoto K, Ishikawa T (1983) Characterization of a cyclic nucleotide phosphodiesterase-deficient mutant in yeast. J Biol Chem 258: 3539-3542.
51. Londesborough J (1978) The high-Km cyclic AMP phosphodiesterase of baker's yeast is a zinc metalloenzyme [proceedings]. Biochem Soc Trans 6: 1218-1220.
52. Londesborough JC (1975) Soluble and membrane-bound cyclic AMP diesterase activity with a low Michaelis constant in baker's yeast. FEBS Lett 50: 283-287.
53. Londesborough J, Suoranta K (1983) The zinc-containing high Km cyclic nucleotide phosphodiesterase of bakers' yeast. J Biol Chem 258: 2966-2972.
54. Ma P, Wera S, Van Dijck P, Thevelein JM (1999) The PDE1-encoded lowaffinity phosphodiesterase in the yeast Saccharomyces cerevisiae has a specific function in controlling agonist-induced cAMP signaling. Mol Biol Cell 10: 91-104.
55. Hoffman CS (2005) Glucose sensing via the protein kinase A pathway in Schizosaccharomyces pombe. Biochem Soc Trans 33: 261-264.
56. Wera S, Ma P, Thevelein JM (1997) Glucose exerts opposite effects on mRNA versus protein and activity levels of Pde1, the low-affinity cAMP phosphodiesterase from budding yeast, Saccharomyces cerevisiae. FEBS Lett 420: 147-150.
57. Wilson RB, Renault G, Jacquet M, Tatchell K (1993) The pde2 gene of Saccharomyces cerevisiae is allelic to rca1 and encodes a phosphodiesterase which protects the cell from extracellular cAMP. FEBS Lett 325: 191-195.
58. Wentzinger L, Seebeck T (2006) Protozoalphosphodiesterases. In: Phosphodiesterases in Health and Disease; Beavo JA, Francis S, Houslay M, eds. CRC Press. 277-300.
59. Sass P, Field J, Nikawa J, Toda T, Wigler M (1986) Cloning and characterization of the high-affinity cAMP phosphodiesterase of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 83: 9303-9307.
60. Matviw H, Li J, Young D (1993) The Schizosaccharomyces pombe pde1/cgs2 gene encodes a cyclic AMP phosphodiesterase. Biochem Biophys Res Commun 194: 79-82.
61. Hoyer LL, Cieslinski LB, McLaughlin MM, Torphy TJ, Shatzman AR, et al. (1994) A Candida albicans cyclic nucleotide phosphodiesterase: cloning and expression in Saccharomyces cerevisiae and biochemical characterization of the recombinant enzyme. Microbiology 140 (Pt 7): 1533-1542.
62. Masciarelli S, Horner K, Liu C, Park SH, Hinckley M, et al. (2004) Cyclic nucleotide phosphodiesterase 3A-deficient mice as a model of female infertility. J Clin Invest 114: 196-205.
63. Fevre EM, Picozzi K, Jannin J, Welburn SC, Maudlin I (2006) Human African trypanosomiasis: Epidemiology and control. Adv Parasitol 61: 167-221.
64. Ou SH (1985) Rice Diseases: Commonwealth Mycological Institute, Kew, Surrey, England.
65. Lee K, Singh P, Chung WC, Ash J, Kim TS, et al. (2006) Light regulation of asexual development in the rice blast fungus, Magnaporthe oryzae. Fungal Genet Biol 43: 694-706.
66. Leung H, Shi Z (1994) Genetic regulation of sporulation in the rice blast fungus. In:Zeigler, RS, Leong,SA, Teng, PS (Eds), Rice Blast Disease CAB international, Oxon. pp 35-50.
67. Lau GW, Hamer JE (1998) Acropetal: a genetic locus required for conidiophore architecture and pathogenicity in the rice blast fungus. Fungal Genet Biol 24: 228-239.
68. Beckerman JL, Ebbole DJ (1996) MPG1, a gene encoding a fungal hydrophobin of Magnaporthe grisea, is involved in surface recognition. Mol Plant Microbe Interact 9: 450-456.
69. Lee YH, Dean RA (1993) cAMP Regusates Infection Structure Formation in the Plant Pathogenic Fungus Magnaporthe grisea. Plant Cell 5: 693-700.
70. Liu H, Ramanujam R, Naqvi N (2009) Surface sensing and signaling during initiation of rice blast disease. In Advances in Genetics, Genomics and Control of Rice Blast Disease. pp 23-32.
71. Liu H, Suresh A, Willard FS, Siderovski DP, Lu S, et al. (2007) Rgs1 regulates multiple Galpha subunits in Magnaporthe pathogenesis, asexual growth and thigmotropism. Embo J 26: 690-700.
72. Choi W, Dean RA (1997) The adenylate cyclase gene MAC1 of Magnaporthe grisea controls appressorium formation and other aspects of growth and development. Plant Cell 9: 1973-1983.
73. Charbonneau H, Beier N, Walsh KA, Beavo JA (1986) Identification of a conserved domain among cyclic nucleotide phosphodiesterases from diverse species. Proc Natl Acad Sci U S A 83: 9308-9312.
74. Balhadere PV, Talbot NJ (2001) PDE1 encodes a P-type ATPase involved in appressorium-mediated plant infection by the rice blast fungus Magnaporthe grisea. Plant Cell 13: 1987-2004.
75. Talbot NJ (1995) Having a blast: exploring the pathogenicity of Magnaporthe grisea. Trends Microbiol 3: 9-16.
76. Veneault-Fourrey C, Barooah M, Egan M, Wakley G, Talbot NJ (2006) Autophagic fungal cell death is necessary for infection by the rice blast fungus. Science 312: 580-583.
77. McCahill A, Campbell L, McSorley T, Sood A, Lynch MJ, et al. (2008) In cardiac myocytes, cAMP elevation triggers the down-regulation of transcripts and promoter activity for cyclic AMP phosphodiesterase-4A10 (PDE4A10). Cell Signal 20: 2071-2083.
78. Riley BB, Barclay SL (1990) Conditions that alter intracellular cAMP levels affect expression of the cAMP phosphodiesterase gene in Dictyostelium. Proc Natl Acad Sci U S A 87: 4746-4750.
79. 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.
80. Skamnioti P, Gurr SJ (2007) Magnaporthe grisea cutinase2 mediates appressorium differentiation and host penetration and is required for full virulence. Plant Cell 19: 2674-2689.
81. Mitchell TK, Dean RA (1995) The cAMP-dependent protein kinase catalytic subunit is required for appressorium formation and pathogenesis by the rice blast pathogen Magnaporthe grisea. Plant Cell 7: 1869-1878.
82. Soanes DM, Kershaw MJ, Cooley RN, Talbot NJ (2002) Regulation of the MPG1 hydrophobin gene in the rice blast fungus Magnaporthe grisea. Mol Plant Microbe Interact 15: 1253-1267.
83. Nishimura M, Hayashi N, Jwa NS, Lau GW, Hamer JE, et al. (2000) Insertion of the LINE retrotransposon MGL causes a conidiophore pattern mutation in Magnaporthe grisea. Mol Plant Microbe Interact 13: 892-894.
84. Odenbach D, Breth B, Thines E, Weber RW, Anke H, et al. (2007) The transcription factor Con7p is a central regulator of infection-related morphogenesis in the rice blast fungus Magnaporthe grisea. Mol Microbiol 64: 293-307.
85. Liu S, Dean RA (1997) G protein alpha subunit genes control growth, development, and pathogenicity of Magnaporthe grisea. Mol Plant Microbe Interact 10: 1075-1086.
86. Nishimura M, Park G, Xu JR (2003) The G-beta subunit MGB1 is involved in regulating multiple steps of infection-related morphogenesis in Magnaporthe grisea. Mol Microbiol 50: 231-243.
87. Han KH, Seo JA, JHY (2004) Regulators of G-protein signalling in Aspergillus nidulans: RgsA downregulates stress response and stimulates asexual sporulation through attenuation of GanB (Ga) signalling. Molecular Microbiology 53: 529-540.
88. Choi GH, Chen B, N DL (1995) Virus-mediated or transgenic suppression of a G protein a subunit and attenuation of fungal virulence. Proc Natl Acad Sci U S A 92: 305-309.
89. Segers GC, DLN (2003) Constitutively activated Ga negatively regulates virulence, reproduction and hydrophobin gene expression in the chestnut blight fungus Cryphonectria parasitica. Fungal Genet Biol 38: 198-208.
90. Rosen S, Yu JH, Adams TH (1999) The Aspergillus nidulans sfaD gene encodes a G protein beta subunit that is required for normal growth and repression of sporulation. Embo J 18: 5592-5600.
91. Hicks JK, Yu JH, Keller NP, Adams TH (1997) Aspergillus sporulation and mycotoxin production both require inactivation of the FadA G alpha proteindependent signaling pathway. Embo J 16: 4916-4923.
92. Adachi K, Hamer JE (1998) Divergent cAMP signaling pathways regulate growth and pathogenesis in the rice blast fungus Magnaporthe grisea. Plant Cell 10: 1361-1374.
93. Xu J-R, Urban M, Sweigard JA, Hamer JE (1997) The CPKA Gene of Magnaporthe grisea Is Essential for Appressorial Penetration. Molecular Plant Microbe Interactions 10: 187.
94. Houslay MD (2009) Underpinning compartmentalised cAMP signaling through targeted cAMP breakdown. Trends Biochem Sci.
95. Baillie GS (2009) Compartmentalized signalling: spatial regulation of cAMP by the action of compartmentalized phosphodiesterases. Febs J 276: 1790-1799.
96. Houslay MD, Adams DR (2003) PDE4 cAMP phosphodiesterases: modular enzymes that orchestrate signalling cross-talk, desensitization and compartmentalization. Biochem J 370: 1-18.
97. Shakur Y, Wilson M, Pooley L, Lobban M, Griffiths SL, et al. (1995) Identification and characterization of the type-IVA cyclic AMP-specific phosphodiesterase RD1 as a membrane-bound protein expressed in cerebellum. Biochem J 306 (Pt 3): 801-809.
98. Baillie GS, Scott JD, Houslay MD (2005) Compartmentalisation of phosphodiesterases and protein kinase A: opposites attract. FEBS Lett 579: 3264-3270.
99. Wilson D, Tutulan-Cunita A, Jung W, Hauser NC, Hernandez R, et al. (2007) Deletion of the high-affinity cAMP phosphodiesterase encoded by PDE2 affects stress responses and virulence in Candida albicans. Mol Microbiol 65: 841-856.
100. Londesborough J, Jonkkari L (1982) Low Km cyclic AMP phosphodiesterase of yeast may be bound to ribosomes associated with the nucleus. Mol Cell Biochem 46: 65-71.
101. Huston E, Lynch MJ, Mohamed A, Collins DM, Hill EV, et al. (2008) EPAC and PKA allow cAMP dual control over DNA-PK nuclear translocation. Proc Natl Acad Sci U S A 105: 12791-12796.
102. Soundararajan S, Jedd G, Li X, Ramos-Pamplona M, Chua NH, et al. (2004) Woronin body function in Magnaporthe grisea is essential for efficient pathogenesis and for survival during nitrogen starvation stress. Plant Cell 16: 1564-1574.
103. Naqvi NI, Bonman JM, Mackill DJ, Nelson RJ, Chattoo BB (1995) Identification of RAPD markers linked to a major gene for blast resistance in rice. Molecular Breeding 1: 341-348.
104. Vogel J, Somerville S (2000) Isolation and characterization of powdery mildewresistant Arabidopsis mutants. Proc Natl Acad Sci U S A 97: 1897-1902.
105. Ramos-Pamplona M, Naqvi NI (2006) Host invasion during rice-blast disease requires carnitine-dependent transport of peroxisomal acetyl-CoA. Mol Microbiol 61: 61-75.
106. Harris SD, Morrell JL, Hamer JE (1994) Identification and characterization of Aspergillus nidulans mutants defective in cytokinesis. Genetics 136: 517-532.
107. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning:A laboratory Manual. Cold Spring Harbor, NY: Cold Spring Laboratory Press.
108. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
109. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
110. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.