Multiple plant surface signals are sensed by different mechanisms in the rice blast fungus for appressorium formation

PLoS Pathogens

Volumn 7, Issue 1, 2011, Pages

  Liu, Wende ^a,b   Zhou, Xiaoying ^b   Li, Guotian ^a,b   Li, Lei ^b   Kong, Lingan ^b   Wang, Chenfang ^a   Zhang, Haifeng ^b   Xu, Jin Rong ^a,b  

^a NORTHWEST A F UNIVERSITY   (China)

^b PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; FUNGAL PROTEIN;

ARTICLE; ENZYME PHOSPHORYLATION; FUNGAL VIRULENCE; NONHUMAN; PLANT; PLANT DISEASE; PLANT FUNGUS INTERACTION; PLANT LEAF; RICE; FUNGAL GENE; FUNGAL MORPHOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MAGNAPORTHE; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; SIGNAL TRANSDUCTION; VIRULENCE;

FUNGI; MAGNAPORTHE GRISEA; MAGNAPORTHE ORYZAE; POACEAE;

FUNGAL PROTEINS; FUNGAL STRUCTURES; GENE EXPRESSION REGULATION, FUNGAL; GENES, FUNGAL; MAGNAPORTHE; ORYZA SATIVA; PLANT DISEASES; SIGNAL TRANSDUCTION; VIRULENCE;

EID: 79551545344     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001261     Document Type: Article

References (56)

1. Valent B, Chumley FG (1991) Molecular genetic analysis of the rice blast fungus Magnaporthe grisea. Annu Rev Phytopathol 29: 443-467.
2. Xu JR, Peng YL, Dickman MB, Sharon A (2006) The dawn of fungal pathogen genomics. Annu Rev Phytopathol 44: 337-366.
3. Wilson RA, Talbot NJ (2009) Under pressure: investigating the biology of plant infection by Magnaporthe oryzae. Nature Rev Micriobiol 7: 185-195.
4. Kankanala P, Czymmek K, Valent B (2007) Roles for rice membrane dynamics and plasmodesmata during biotrophic invasion by the blast fungus. Plant Cell 19: 706-724.
5. Choi WB, 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.
6. 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.
7. Uchiyama T, Okuyama K (1990) Participation of Oryza-Sativa leaf wax in appressorium formation by Pyricularia oryzae. Phytochemistry 29: 91-92.
8. Xiao JZ, Watanabe T, Sekido S, Choi WB, Kamakura T, et al. (1997) An anti-hydrotactic response and solid surface recognition of germ tubes of the rice blast fungus, Magnaporthe grisea. Biosci Biotechnol Biochem 61: 1225-1229.
9. Ohtake M, Yamamoto H, Uchiyama T (1999) Influences of metabolic inhibitors and hydrolytic enzymes on the adhesion of appressoria of Pyricularia oryzae to wax-coated cover-glasses. Biosci Biotechnol Biochem 63: 978-982.
10. Jelitto TC, Page HA, Read ND (1994) Role of external signals in regulating the pre-penetration phase of infection by the rice blast fungus Magnaporthe grisea. Planta 194: 471-477.
11. Liu H, Suresh A, Willard FS, Siderovski DP, Lu S, et al. (2007) Rgs1 regulates multiple G alpha subunits in Magnaporthe pathogenesis, asexual growth and thigmotropism. Embo Journal 26: 690-700.
12. Zhao X, Mehrabi R, Xu J-R (2007) Mitogen-activated protein kinase pathways and fungal pathogenesis. Eukaryot Cell 6: 1701-1714.
13. Chen RE, Thorner J (2007) Function and regulation in MAPK signaling pathways: Lessons learned from the yeast Saccharomyces cerevisiae. Bioch Biophys Acta 1773: 1311-1340.
14. Zhao XH, Kim Y, Park G, Xu JR (2005) A mitogen-activated protein kinase cascade regulating infection-related morphogenesis in Magnaporthe grisea. Plant Cell 17: 1317-1329.
15. Park G, Xue C, Zhao X, Kim Y, Orbach M, et al. (2006) Multiple upstream signals converge on an adaptor protein Mst50 to activate the PMK1 pathway in Magnaporthe grisea. Plant Cell 18: 2822-2835.
16. Park G, Xue GY, Zheng L, Lam S, Xu JR (2002) MST12 regulates infectious growth but not appressorium formation in the rice blast fungus Magnaporthe grisea. Mol Plant-Microbe Interact 15: 183-192.
17. Kramer B, Thines E, Foster AJ (2009) MAP kinase signalling pathway components and targets conserved between the distantly related plant pathogenic fungi Mycosphaerella graminicola and Magnaporthe grisea. Fungal Genet Biol 46: 667-681.
18. Rispail N, Soanes DM, Ant C, Czajkowski R, Grunler A, et al. (2009) Comparative genomics of MAP kinase and calcium-calcineurin signalling components in plant and human pathogenic fungi. Fung Genet Biol 46: 287-298.
19. DeZwaan TM, Carroll AM, Valent B, Sweigard JA (1999) Magnaporthe grisea Pth11p is a novel plasma membrane protein that mediates appressorium differentiation in response to inductive substrate cues. Plant Cell 11: 2013-2030.
20. Bardwell L (2006) Mechanisms of MAPK signalling specificity. Biochem Soc Transact 34: 837-841.
21. Cullen PJ, Schultz J, Horecka J, Stevenson BJ, Jigami Y, et al. (2000) Defects in protein glycosylation cause SHO1-dependent activation of a STE12 signaling pathway in yeast. Genetics 155: 1005-1018.
22. Pitoniak A, Birkaya B, Dionne HM, Vadaie N, Cullen PJ (2009) The signaling mucins Msb2 and Hkr1 differentially regulate the filamentation mitogen-activated protein kinase pathway and contribute to a multimodal response. Mol Biol Cell 20: 3101-3114.
23. Raitt DC, Posas F, Saito H (2000) Yeast Cdc42 GTPase and Ste20 PAK-like kinase regulate Sho1-dependent activation of the Hog1 MAPK pathway. EMBO J 19: 4623-4631.
24. Lanver D, Mendoza-Mendoza A, Brachmann A, Kahmann R (2010) Sho1 and Msb2-related proteins regulate appressorium development in the smut fungus Ustilago maydis. Plant Cell 22: 2085-2101.
25. Madhani HD, Fink GR (1997) Combinatorial control required for the specificity of yeast MAPK signaling. Science 275: 1314-1317.
26. Villalba F, Collemare J, Landraud P, Lambou K, Brozek V, et al. (2008) Improved gene targeting in Magnaporthe grisea by inactivation of MgKU80 required for non-homologous end joining. Fungal Genet Biol 45: 68-75.
27. Gilbert RD, Johnson AM, Dean RA (1996) Chemical signals responsible for appressorium formation in the rice blast fungus Magnaporthe grisea. Physiol Mol Plant Pathol 48: 335-346.
28. Kunst L, Samuels AL (2003) Biosynthesis and secretion of plant cuticular wax. Prog Lipid Res 42: 51-80.
29. Yu D, Ranathunge K, Huang H, Pei Z, Franke R, et al. (2008) Wax Crystal-Sparse Leaf1 encodes a beta-ketoacyl CoA synthase involved in biosynthesis of cuticular waxes on rice leaf. Planta 228: 675-685.
30. Dixon KP, Xu JR, Smirnoff N, Talbot NJ (1999) Independent signaling pathways regulate cellular turgor during hyperosmotic stress and appressorium-mediated plant infection by Magnaporthe grisea. Plant Cell 11: 2045-2058.
31. Hattrup CL, Gendler SJ (2008) Structure and function of the cell surface (tethered) mucins. Annu Rev Physiol 70: 431-457.
32. Cullen PJ, Sabbagh W, Jr., Graham E, Irick MM, van Olden EK, et al. (2004) A signaling mucin at the head of the Cdc42- and MAPK-dependent filamentous growth pathway in yeast. Genes Dev 18: 1695-1708.
33. Tatebayashi K, Tanaka K, Yang HY, Yamamoto K, Matsushita Y, et al. (2007) Transmembrane mucins Hkr1 and Msb2 are putative osmosensors in the SHO1 branch of yeast HOG pathway. EMBO J 26: 3521-3533.
34. Kamakura T, Yamaguchi S, Saitoh K, Teraoka T, Yamaguchi I (2002) A novel gene, CBP1, encoding a putative extracellular chitin- binding protein, may play an important role in the hydrophobic surface sensing of Magnaporthe grisea during appressorium differentiation. Mol Plant-Microbe Interact 15: 437-444.
35. Zabka V, Stangl M, Bringmann G, Vogg G, Riederer M, et al. (2008) Host surface properties affect prepenetration processes in the barley powdery mildew fungus. New Phytol 177: 251-263.
36. Xu JR, Hamer JE (1996) MAP kinase and cAMP signaling regulate infection structure formation and pathogenic growth in the rice blast fungus Magnaporthe grisea. Genes Dev 10: 2696-2706.
37. Vadaie N, Dionne H, Akajagbor DS, Nickerson SR, Krysan DJ, et al. (2008) Cleavage of the signaling mucin Msb2 by the aspartyl protease Yps1 is required for MAPK activation in yeast. J Cell Biol 181: 1073-1081.
38. Talbot NJ, Ebbole DJ, Hamer JE (1993) Identification and characterization of MPG1, a gene involved in pathogenicity from the rice blast fungus Magnaporthe grisea. Plant Cell 5: 1575-1590.
39. Sweigard JA, Carroll AM, Farrall L, Chumley FG, Valent B (1998) Magnaporthe grisea pathogenicity genes obtained through insertional mutagenesis. Mol Plant-Microbe Interact 11: 404-412.
40. Xue CY, Park G, Choi WB, Zheng L, Dean RA, et al. (2002) Two novel fungal virulence genes specifically expressed in appressoria of the rice blast fungus. Plant Cell 14: 2107-2119.
41. Sweigard JA, Chumley FG, Valent B (1992) Disruption of a Magnaporthe grisea cutinase gene. Mol Gen Genet 232: 183-190.
42. Bruno KS, Tenjo F, Li L, Hamer JE, Xu JR (2004) Cellular localization and role of kinase activity of PMK1 in Magnaporthe grisea. Eukaryot Cell 3: 1525-1532.
43. Liu WD, Xie SY, Zhao XH, Chen X, Zheng WH, et al. (2010) A homeobox gene is essential for conidiogenesis of the rice blast fungus Magnaporthe oryzae. Mol Plant-Microbe Interact 23: 366-375.
44. Bourett TM, Sweigard JA, Czymmek KJ, Carroll A, Howard RJ (2002) Reef coral fluorescent proteins for visualizing fungal pathogens. Fungal Genet Biol 37: 211-220.
45. Cullen PJ, Sabbagh W, Graham E, Irick MM, van Olden EK, et al. (2004) A signaling mucin at the head of the Cdc42- and MAPK-dependent filamentous growth pathway in yeast. Genes Dev 18: 1695-1708.
46. Zarrinpar A, Bhattacharyya RP, Nittler MP, Lim WA (2004) Sho1 and Pbs2 act as coscaffolds linking components in the yeast high osmolarity MAP kinase pathway. Mol Cell 14: 825-832.
47. Tucker SL, Thornton CR, Tasker K, Jacob C, Giles G, et al. (2004) A fungal metallothionein is required for pathogenicity of Magnaporthe grisea. Plant Cell 16: 1575-1588.
48. Koga H (1994) Hypersensitive death, autofluorescence, and ultrastructural-changes in cells of leaf sheaths of susceptible and resistant near-isogenic lines of rice (PI-Z(T)) in relation to penetration and growth of Pycularia oryza. Can J Bot 72: 1463-1477.
49. Park G, Bruno KS, Staiger CJ, Talbot NJ, Xu JR (2004) Independent genetic mechanisms mediate turgor generation and penetration peg formation during plant infection in the rice blast fungus. Mol Microbiol 53: 1695-1707.
50. Li L, Xue CY, Bruno K, Nishimura M, Xu JR (2004) Two PAK kinase genes, CHM1 and MST20, have distinct functions in Magnaporthe grisea. Mol Plant-Microbe Interact 17: 547-556.
51. Talbot NJ, Kershaw MJ, Wakley GE, deVries OMH, Wessels JGH, et al. (1996) MPG1 encodes a fungal hydrophobin involved in surface interactions during infection-related development of Magnaporthe grisea. Plant Cell 8: 985-999.
52. Chen XB, Goodwin SM, Boroff VL, Liu XL, Jenks MA (2003) Cloning and characterization of the WAX2 gene of Arabidopsis involved in cuticle membrane and wax production. Plant Cell 15: 1170-1185.
53. Li L, Ding SL, Sharon A, Orbach M, Xu JR (2007) Mir1 is highly upregulated and localized to nuclei during infectious hyphal growth in the rice blast fungus. Mol Plant-Microbe Interact 20: 448-458.
54. 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.
55. Ding S, Liu W, LLiuk A, Ribot C, Vallet J, et al. (2010) The Tig1 HDAC complex regulates infectious growth in the rice blast fungus Magnaporthe oryzae. Plant Cell 22: 2495-2508.
56. Sambrook J, Russell D (2001) Molecular Cloning - A Laboratory Manual. Cold Spring Harbor NY: Cold Spring Harbor Laboratory Press.