Comparative genomics of MAP kinase and calcium-calcineurin signalling components in plant and human pathogenic fungi

Fungal Genetics and Biology

Volumn 46, Issue 4, 2009, Pages 287-298

  Rispail, Nicolas ^a   Soanes, Darren M ^b   Ant, Cemile ^c   Czajkowski, Robert ^d   Grünler, Anke ^e   Huguet, Romain ^b   Perez Nadales, Elena ^a   Poli, Anna ^f   Sartorel, Elodie ^g   Valiante, Vito ^h   Yang, Meng ⁱ   Beffa, Roland ^c   Brakhage, Axel A ^h   Gow, Neil A R ⁱ   Kahmann, Regine ^d   Lebrun, Marc Henri ^c   Lenasi, Helena ^f   Perez Martin, José ^g   Talbot, Nicholas J ^b   Wendland, Jürgen ^e   Di Pietro, Antonio ^a   more..

^a UNIVERSITY OF CÓRDOBA   (Spain)

^b UNIVERSITY OF EXETER   (United Kingdom)

^c CNRS   (France)

^d MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^e CARLSBERG LABORATORY   (Denmark)

^f UNIVERSITY OF LJUBLJANA   (Slovenia)

^g CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^h HANS KNÖLL INSTITUTE   (Germany)

ⁱ UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Calcium; MAPK; Signalling; Stress; Virulence

Indexed keywords

CALCINEURIN; CALCIUM; CALCIUM BINDING PROTEIN; FUS3 PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN; UNCLASSIFIED DRUG;

CALCIUM SIGNALING; CELL CYCLE ARREST; FUNGUS GROWTH; GENOMICS; NONHUMAN; PATHOGENESIS; PLANT DISEASE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; REVIEW; RHIZOPUS ORYZAE; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; SPECIES DIVERSITY; UBIQUITINATION; ZYGOMYCETES;

CALCINEURIN; CALCIUM; FUNGAL PROTEINS; FUNGI; GENOMICS; HUMANS; MAP KINASE SIGNALING SYSTEM; MYCOSES; PLANT DISEASES; PLANTS; PROTEIN KINASES; SIGNAL TRANSDUCTION;

FUNGI; MAMMALIA; RHIZOPUS ORYZAE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCOTINA;

EID: 61749104584     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2009.01.002     Document Type: Review

References (126)

1. Alonso-Monge R., Navarro-Garcia F., Molero G., Diez-Orejas R., Gustin M., Pla J., Sanchez M., and Nombela C. Role of the mitogen-activated protein kinase Hog1p in morphogenesis and virulence of Candida albicans. J. Bacteriol. 181 (1999) 3058-3068
2. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., and Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl. Acids Res. 25 (1997) 3389-3402
3. Andrianopoulos A., and Timberlake W.E. The Aspergillus nidulans abaA gene encodes a transcriptional activator that acts as a genetic switch to control development. Mol. Cell Biol. 14 (1994) 2503-2515
4. Bader T., Bodendorfer B., Schroppel K., and Morschhauser J. Calcineurin is essential for virulence in Candida albicans. Infect. Immun. 71 (2003) 5344-5354
5. Ballon D.R., Flanary P.L., Gladue D.P., Konopka J.B., Dohlman H.G., and Thorner J. DEP-domain-mediated regulation of GPCR signaling responses. Cell 126 (2006) 1079-1093
6. Banuett F., and Herskowitz I. Identification of fuz7, a Ustilago maydis MEK/MAPKK homolog required for a-locus-dependent and -independent steps in the fungal life cycle. Genes Dev. 8 (1994) 1367-1378
7. Bermejo C., Rodriguez E., Garcia R., Rodriguez-Pena J.M., Rodriguez de la Concepcion M.L., Rivas C., Arias P., Nombela C., Posas F., and Arroyo J. The sequential activation of the yeast HOG and SLT2 pathways is required for cell survival to cell wall stress. Mol. Biol. Cell 19 (2008) 1113-1124
8. Bilsland E., Molin C., Swaminathan S., Ramne A., and Sunnerhagen P. Rck1 and Rck2 MAPKAP kinases and the HOG pathway are required for oxidative stress resistance. Mol. Microbiol. 53 (2004) 1743-1756
9. Blankenship J.R., Wormley F.L., Boyce M.K., Schell W.A., Filler S.G., Perfect J.R., and Heitman J. Calcineurin is essential for Candida albicans survival in serum and virulence. Eukaryot. Cell 2 (2003) 422-430
10. Bluhm B.H., Zhao X., Flaherty J.E., Xu J.R., and Dunkle L.D. RAS2 regulates growth and pathogenesis in Fusarium graminearum. Mol. Plant Microbe Interact. 20 (2007) 627-636
11. Bolker M., Urban M., and Kahmann R. The a mating type locus of U. Maydis specifies cell signaling components. Cell 68 (1992) 441-450
12. Brachmann A., Schirawski J., Muller P., and Kahmann R. An unusual MAP kinase is required for efficient penetration of the plant surface by Ustilago maydis. EMBO J. 22 (2003) 2199-2210
13. Butty A.C., Pryciak P.M., Huang L.S., Herskowitz I., and Peter M. The role of Far1p in linking the heterotrimeric G protein to polarity establishment proteins during yeast mating. Science 282 (1998) 1511-1516
14. Calera J.A., Zhao X.J., and Calderone R. Defective hyphal development and avirulence caused by a deletion of the SSK1 response regulator gene in Candida albicans. Infect. Immun. 68 (2000) 518-525
15. Catlett N.L., Yoder O.C., and Turgeon B.G. Whole-genome analysis of two-component signal transduction genes in fungal pathogens. Eukaryot. Cell 2 (2003) 1151-1161
16. Cliften P., Sudarsanam P., Desikan A., Fulton L., Fulton B., Majors J., Waterston R., Cohen B.A., and Johnston M. Finding functional features in Saccharomyces genomes by phylogenetic footprinting. Science 301 (2003) 71-76
17. Cook J.G., Bardwell L., Kron S.J., and Thorner J. Two novel targets of the MAP kinase Kss1 are negative regulators of invasive growth in the yeast Saccharomyces cerevisiae. Genes Dev. 10 (1996) 2831-2848
18. Cote P., and Whiteway M. The role of Candida albicans FAR1 in regulation of pheromone-mediated mating, gene expression and cell cycle arrest. Mol. Microbiol. 68 (2008) 392-404
19. Cramer Jr. R.A., Perfect B.Z., Pinchai N., Park S., Perlin D.S., Asfaw Y.G., Heitman J., Perfect J.R., and Steinbach W.J. Calcineurin target CrzA regulates conidial germination, hyphal growth, and pathogenesis of Aspergillus fumigatus. Eukaryot. Cell 7 (2008) 1085-1097
20. Cruz M.C., Goldstein A.L., Blankenship J.R., Del Poeta M., Davis D., Cardenas M.E., Perfect J.R., McCusker J.H., and Heitman J. Calcineurin is essential for survival during membrane stress in Candida albicans. EMBO J. 21 (2002) 546-559
21. Csank C., Schroppel K., Leberer E., Harcus D., Mohamed O., Meloche S., Thomas D.Y., and Whiteway M. Roles of the Candida albicans mitogen-activated protein kinase homolog, Cek1p, in hyphal development and systemic candidiasis. Infect. Immun. 66 (1998) 2713-2721
22. Cullen P.J., Sabbagh Jr. W., Graham E., Irick M.M., van Olden E.K., Neal C., Delrow J., Bardwell L., and Sprague Jr. G.F. A signaling mucin at the head of the Cdc42- and MAPK-dependent filamentous growth pathway in yeast. Genes Dev. 18 (2004) 1695-1708
23. Cyert M.S. Genetic analysis of calmodulin and its targets in Saccharomyces cerevisiae. Annu. Rev. Genet. 35 (2001) 647-672
24. Cyert M.S. Calcineurin signaling in Saccharomyces cerevisiae: how yeast go crazy in response to stress. Biochem. Biophys. Res. Commun. 311 (2003) 1143-1150
25. Chang L., and Karin M. Mammalian MAP kinase signalling cascades. Nature 410 (2001) 37-40
26. Chen J., Chen J., Lane S., and Liu H. A conserved mitogen-activated protein kinase pathway is required for mating in Candida albicans. Mol. Microbiol. 46 (2002) 1335-1344
27. Chin D., and Means A.R. Calmodulin: a prototypical calcium sensor. Trends Cell Biol. 10 (2000) 322-328
28. da Silva Ferreira M.E., Heinekamp T., Hartl A., Brakhage A.A., Semighini C.P., Harris S.D., Savoldi M., de Gouvea P.F., De Souza Goldman M.H., and Goldman G.H. Functional characterization of the Aspergillus fumigatus calcineurin. Fungal Genet. Biol. 44 (2007) 219-230
29. de Nadal E., Casadome L., and Posas F. Targeting the MEF2-like transcription factor Smp1 by the stress-activated Hog1 mitogen-activated protein kinase. Mol. Cell Biol. 23 (2003) 229-237
30. Del Poeta M., Cruz M.C., Cardenas M.E., Perfect J.R., and Heitman J. Synergistic antifungal activities of bafilomycin A(1), fluconazole, and the pneumocandin MK-0991/caspofungin acetate (L-743, 873) with calcineurin inhibitors FK506 and L-685, 818 against Cryptococcus neoformans. Antimicrob. Agents Chemother. 44 (2000) 739-746
31. Dietrich F.S., Voegeli S., Brachat S., Lerch A., Gates K., Steiner S., Mohr C., Pohlmann R., Luedi P., Choi S., Wing R.A., Flavier A., Gaffney T.D., and Philippsen P. The Ashbya gossypii genome as a tool for mapping the ancient Saccharomyces cerevisiae genome. Science 304 (2004) 304-307
32. Diez-Orejas R., Molero G., Navarro-Garcia F., Pla J., Nombela C., and Sanchez-Perez M. Reduced virulence of Candida albicans MKC1 mutants: a role for mitogen-activated protein kinase in pathogenesis. Infect. Immun. 65 (1997) 833-837
33. Dixon K.P., Xu J.R., Smirnoff N., and Talbot N.J. Independent signaling pathways regulate cellular turgor during hyperosmotic stress and appressorium-mediated plant infection by Magnaporthe grisea. Plant Cell 11 (1999) 2045-2058
34. Dohlman H.G., Song J., Ma D., Courchesne W.E., and Thorner J. Sst2, a negative regulator of pheromone signaling in the yeast Saccharomyces cerevisiae: expression, localization, and genetic interaction and physical association with Gpa1 (the G-protein alpha subunit). Mol. Cell Biol. 16 (1996) 5194-5209
35. Du C., Sarfati J., Latge J.P., and Calderone R. The role of the sakA (Hog1) and tcsB (sln1) genes in the oxidant adaptation of Aspergillus fumigatus. Med. Mycol. 44 (2006) 211-218
36. Dujon B., Sherman D., Fischer G., Durrens P., Casaregola S., Lafontaine I., De Montigny J., Marck C., Neuveglise C., Talla E., Goffard N., Frangeul L., Aigle M., Anthouard V., Babour A., Barbe V., Barnay S., Blanchin S., Beckerich J.M., Beyne E., Bleykasten C., Boisrame A., Boyer J., Cattolico L., Confanioleri F., De Daruvar A., Despons L., Fabre E., Fairhead C., Ferry-Dumazet H., Groppi A., Hantraye F., Hennequin C., Jauniaux N., Joyet P., Kachouri R., Kerrest A., Koszul R., Lemaire M., Lesur I., Ma L., Muller H., Nicaud J.M., Nikolski M., Oztas S., Ozier-Kalogeropoulos O., Pellenz S., Potier S., Richard G.F., Straub M.L., Suleau A., Swennen D., Tekaia F., Wesolowski-Louvel M., Westhof E., Wirth B., Zeniou-Meyer M., Zivanovic I., Bolotin-Fukuhara M., Thierry A., Bouchier C., Caudron B., Scarpelli C., Gaillardin C., Weissenbach J., Wincker P., and Souciet J.L. Genome evolution in yeasts. Nature 430 (2004) 35-44
37. Elion E.A. Routing MAP kinase cascades. Science 281 (1998) 1625-1626
38. Elion E.A. Pheromone response, mating and cell biology. Curr. Opin. Microbiol. 3 (2000) 573-581
39. Elion E.A., Satterberg B., and Kranz J.E. FUS3 phosphorylates multiple components of the mating signal transduction cascade: evidence for STE12 and FAR1. Mol. Biol. Cell 4 (1993) 495-510
40. Fox D.S., Cruz M.C., Sia R.A., Ke H., Cox G.M., Cardenas M.E., and Heitman J. Calcineurin regulatory subunit is essential for virulence and mediates interactions with FKBP12-FK506 in Cryptococcus neoformans. Mol. Microbiol. 39 (2001) 835-849
41. Grimshaw S.J., Mott H.R., Stott K.M., Nielsen P.R., Evetts K.A., Hopkins L.J., Nietlispach D., and Owen D. Structure of the sterile alpha motif (SAM) domain of the Saccharomyces cerevisiae mitogen-activated protein kinase pathway-modulating protein STE50 and analysis of its interaction with the STE11 SAM. J. Biol. Chem. 279 (2004) 2192-2201
42. Gustin M.C., Albertyn J., Alexander M., and Davenport K. MAP kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 62 (1998) 1264-1300
43. Hahn J.S., and Thiele D.J. Regulation of the Saccharomyces cerevisiae Slt2 kinase pathway by the stress-inducible Sdp1 dual specificity phosphatase. J. Biol. Chem. 277 (2002) 21278-21284
44. Hallen H.E., and Trail F. The L-type calcium ion channel cch1 affects ascospore discharge and mycelial growth in the filamentous fungus Gibberella zeae (anamorph Fusarium graminearum). Eukaryot. Cell 7 (2008) 415-424
45. Harel A., Bercovich S., and Yarden O. Calcineurin is required for sclerotial development and pathogenicity of Sclerotinia sclerotiorum in an oxalic acid-independent manner. Mol. Plant Microbe Interact. 19 (2006) 682-693
46. Hohmann S., Krantz M., and Nordlander B. Yeast osmoregulation. Methods Enzymol. 428 (2007) 29-45
47. Hou Z., Xue C., Peng Y., Katan T., Kistler H.C., and Xu J.R. A mitogen-activated protein kinase gene (MGV1) in Fusarium graminearum is required for female fertility, heterokaryon formation, and plant infection. Mol. Plant Microbe Interact. 15 (2002) 1119-1127
48. Jenczmionka N.J., Maier F.J., Losch A.P., and Schafer W. Mating, conidiation and pathogenicity of Fusarium graminearum, the main causal agent of the head-blight disease of wheat, are regulated by the MAP kinase gpmk1. Curr. Genet. 43 (2003) 87-95
49. Jones C.A., Greer-Phillips S.E., and Borkovich K.A. The response regulator RRG-1 functions upstream of a mitogen-activated protein kinase pathway impacting asexual development, female fertility, osmotic stress, and fungicide resistance in Neurospora crassa. Mol. Biol. Cell 18 (2007) 2123-2136
50. Jung U.S., and Levin D.E. Genome-wide analysis of gene expression regulated by the yeast cell wall integrity signalling pathway. Mol. Microbiol. 34 (1999) 1049-1057
51. Jung U.S., Sobering A.K., Romeo M.J., and Levin D.E. Regulation of the yeast Rlm1 transcription factor by the Mpk1 cell wall integrity MAP kinase. Mol. Microbiol. 46 (2002) 781-789
52. Kellis M., Birren B.W., and Lander E.S. Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 428 (2004) 617-624
53. Kingsbury T.J., and Cunningham K.W. A conserved family of calcineurin regulators. Genes Dev. 14 (2000) 1595-1604
54. Kobori H., Toda T., Yaguchi H., Toya M., Yanagida M., and Osumi M. Fission yeast protein kinase C gene homologues are required for protoplast regeneration: a functional link between cell wall formation and cell shape control. J. Cell Sci. 107 Pt 5 (1994) 1131-1136
55. Kontoyiannis D.P., Lewis R.E., Osherov N., Albert N.D., and May G.S. Combination of caspofungin with inhibitors of the calcineurin pathway attenuates growth in vitro in Aspergillus species. J. Antimicrob. Chemother. 51 (2003) 313-316
56. Kraus P.R., and Heitman J. Coping with stress: calmodulin and calcineurin in model and pathogenic fungi. Biochem. Biophys. Res. Commun. 311 (2003) 1151-1157
57. Kurjan J. The pheromone response pathway in Saccharomyces cerevisiae. Annu. Rev. Genet. 27 (1993) 147-179
58. Leberer E., Harcus D., Dignard D., Johnson L., Ushinsky S., Thomas D.Y., and Schroppel K. Ras links cellular morphogenesis to virulence by regulation of the MAP kinase and cAMP signalling pathways in the pathogenic fungus Candida albicans. Mol. Microbiol. 42 (2001) 673-687
59. Lee N., D'Souza C.A., and Kronstad J.W. Of smuts, blasts, mildews, and blights: cAMP signaling in phytopathogenic fungi. Annu. Rev. Phytopathol. 41 (2003) 399-427
60. Lee N., and Kronstad J.W. Ras2 Controls morphogenesis, pheromone response, and pathogenicity in the fungal pathogen Ustilago maydis. Eukaryot. Cell 1 (2002) 954-966
61. Lengeler K.B., Davidson R.C., D'Souza C., Harashima T., Shen W.C., Wang P., Pan X., Waugh M., and Heitman J. Signal transduction cascades regulating fungal development and virulence. Microbiol. Mol. Biol. Rev. 64 (2000) 746-785
62. Levin D.E. Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 69 (2005) 262-291
63. Lew R.R., Abbas Z., Anderca M.I., and Free S.J. Phenotype of a mechanosensitive channel mutant, mid-1, in a filamentous fungus, Neurospora crassa. Eukaryot. Cell 7 (2008) 647-655
64. Li L., Wright S.J., Krystofova S., Park G., and Borkovich K.A. Heterotrimeric G protein signaling in filamentous fungi. Annu. Rev. Microbiol. 61 (2007) 423-452
65. Locke E.G., Bonilla M., Liang L., Takita Y., and Cunningham K.W. A homolog of voltage-gated Ca(2+) channels stimulated by depletion of secretory Ca(2+) in yeast. Mol. Cell Biol. 20 (2000) 6686-6694
66. Lyons D.M., Mahanty S.K., Choi K.Y., Manandhar M., and Elion E.A. The SH3-domain protein Bem1 coordinates mitogen-activated protein kinase cascade activation with cell cycle control in Saccharomyces cerevisiae. Mol. Cell Biol. 16 (1996) 4095-4106
67. Ma Y., Qiao J., Liu W., Wan Z., Wang X., Calderone R., and Li R. The sho1 sensor regulates growth, morphology, and oxidant adaptation in Aspergillus fumigatus but is not essential for development of invasive pulmonary aspergillosis. Infect. Immun. 76 (2008) 1695-1701
68. Madhani H.D., and Fink G.R. Combinatorial control required for the specificity of yeast MAPK signaling. Science 275 (1997) 1314-1317
69. Madhani H.D., and Fink G.R. The control of filamentous differentiation and virulence in fungi. Trends Cell Biol. 8 (1998) 348-353
70. Madhani H.D., Styles C.A., and Fink G.R. MAP kinases with distinct inhibitory functions impart signaling specificity during yeast differentiation. Cell 91 (1997) 673-684
71. Martin H., Flandez M., Nombela C., and Molina M. Protein phosphatases in MAPK signalling: we keep learning from yeast. Mol. Microbiol. 58 (2005) 6-16
72. Martinez-Pastor M.T., Marchler G., Schuller C., Marchler-Bauer A., Ruis H., and Estruch F. The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). EMBO J. 15 (1996) 2227-2235
73. Martinez-Rocha A.L., Roncero M.I., Lopez-Ramirez A., Marine M., Guarro J., Martinez-Cadena G., and Di Pietro A. Rho1 has distinct functions in morphogenesis, cell wall biosynthesis and virulence of Fusarium oxysporum. Cell Microbiol. 10 (2008) 1339-1351
74. Mayorga M.E., and Gold S.E. A MAP kinase encoded by the ubc3 gene of Ustilago maydis is required for filamentous growth and full virulence. Mol. Microbiol. 34 (1999) 485-497
75. Mayorga M.E., and Gold S.E. The ubc2 gene of Ustilago maydis encodes a putative novel adaptor protein required for filamentous growth, pheromone response and virulence. Mol. Microbiol. 41 (2001) 1365-1379
76. Miskei, M., Karanyi, Z., Pocsi, I., 2009. Annotation of stress-response proteins in the aspergilli. Fungal Genet. Biol. 46, S105-S120.
77. Mosch H.U., Roberts R.L., and Fink G.R. Ras2 signals via the Cdc42/Ste20/mitogen-activated protein kinase module to induce filamentous growth in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 93 (1996) 5352-5356
78. 2+ influx and cell fusion during mating of Saccharomyces cerevisiae. J. Biol. Chem. 278 (2003) 38461-38469
79. Muller P., Aichinger C., Feldbrugge M., and Kahmann R. The MAP kinase kpp2 regulates mating and pathogenic development in Ustilago maydis. Mol. Microbiol. 34 (1999) 1007-1017
80. Nagahashi S., Mio T., Ono N., Yamada-Okabe T., Arisawa M., Bussey H., and Yamada-Okabe H. Isolation of CaSLN1 and CaNIK1, the genes for osmosensing histidine kinase homologues, from the pathogenic fungus Candida albicans. Microbiology 144 Pt 2 (1998) 425-432
81. Nasmyth K., and Dirick L. The role of SWI4 and SWI6 in the activity of G1 cyclins in yeast. Cell 66 (1991) 995-1013
82. Ochiai N., Tokai T., Nishiuchi T., Takahashi-Ando N., Fujimura M., and Kimura M. Involvement of the osmosensor histidine kinase and osmotic stress-activated protein kinases in the regulation of secondary metabolism in Fusarium graminearum. Biochem. Biophys. Res. Commun. 363 (2007) 639-644
83. Odom A., Muir S., Lim E., Toffaletti D.L., Perfect J., and Heitman J. Calcineurin is required for virulence of Cryptococcus neoformans. EMBO J. 16 (1997) 2576-2589
84. Ozaki K., Tanaka K., Imamura H., Hihara T., Kameyama T., Nonaka H., Hirano H., Matsuura Y., and Takai Y. Rom1p and Rom2p are GDP/GTP exchange proteins (GEPs) for the Rho1p small GTP binding protein in Saccharomyces cerevisiae. EMBO J. 15 (1996) 2196-2207
85. Park G., Bruno K.S., Staiger C.J., Talbot N.J., and Xu J.R. Independent genetic mechanisms mediate turgor generation and penetration peg formation during plant infection in the rice blast fungus. Mol. Microbiol. 53 (2004) 1695-1707
86. Park G., Xue C., Zhao X., Kim Y., Orbach M., and Xu J.R. Multiple upstream signals converge on the adaptor protein Mst50 in Magnaporthe grisea. Plant Cell 18 (2006) 2822-2835
87. Peter M., Gartner A., Horecka J., Ammerer G., and Herskowitz I. FAR1 links the signal transduction pathway to the cell cycle machinery in yeast. Cell 73 (1993) 747-760
88. Philip B., and Levin D.E. Wsc1 and Mid2 are cell surface sensors for cell wall integrity signaling that act through Rom2, a guanine nucleotide exchange factor for Rho1. Mol. Cell Biol. 21 (2001) 271-280
89. Posas F., and Saito H. Osmotic activation of the HOG MAPK pathway via Ste11p MAPKKK: scaffold role of Pbs2p MAPKK. Science 276 (1997) 1702-1705
90. Posas F., Wurgler-Murphy S.M., Maeda T., Witten E.A., Thai T.C., and Saito H. Yeast HOG1 MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1-YPD1-SSK1 "two-component" osmosensor. Cell 86 (1996) 865-875
91. Pryciak P.M., and Huntress F.A. Membrane recruitment of the kinase cascade scaffold protein Ste5 by the Gbetagamma complex underlies activation of the yeast pheromone response pathway. Genes Dev. 12 (1998) 2684-2697
92. Qi M., and Elion E.A. MAP kinase pathways. J. Cell Sci. 118 (2005) 3569-3572
93. Raitt D.C., Posas F., and Saito H. Yeast Cdc42 GTPase and Ste20 PAK-like kinase regulate Sho1-dependent activation of the Hog1 MAPK pathway. EMBO J. 19 (2000) 4623-4631
94. Rep M., Krantz M., Thevelein J.M., and Hohmann S. The transcriptional response of Saccharomyces cerevisiae to osmotic shock. Hot1p and Msn2p/Msn4p are required for the induction of subsets of high osmolarity glycerol pathway-dependent genes. J. Biol. Chem. 275 (2000) 8290-8300
95. Rep M., Proft M., Remize F., Tamas M., Serrano R., Thevelein J.M., and Hohmann S. The Saccharomyces cerevisiae Sko1p transcription factor mediates HOG pathway-dependent osmotic regulation of a set of genes encoding enzymes implicated in protection from oxidative damage. Mol. Microbiol. 40 (2001) 1067-1083
96. Reyes G., Romans A., Nguyen C.K., and May G.S. Novel mitogen-activated protein kinase MpkC of Aspergillus fumigatus is required for utilization of polyalcohol sugars. Eukaryot. Cell 5 (2006) 1934-1940
97. Roman E., Nombela C., and Pla J. The Sho1 adaptor protein links oxidative stress to morphogenesis and cell wall biosynthesis in the fungal pathogen Candida albicans. Mol. Cell Biol. 25 (2005) 10611-10627
98. Sanglard D., Ischer F., Marchetti O., Entenza J., and Bille J. Calcineurin A of Candida albicans: involvement in antifungal tolerance, cell morphogenesis and virulence. Mol. Microbiol. 48 (2003) 959-976
99. Schimek C., and Wöstemeyer J. Pheromone action in the fungal groups Chytridiomycota, and Zygomycota, and in the Oomycota. In: Kües U., and Fischer R. (Eds). The Mycota (2006), Springer Verlag, Berlin, Heidelberg 215-231
100. Schumacher J., de Larrinoa I.F., and Tudzynski B. Calcineurin-responsive zinc finger transcription factor CRZ1 of Botrytis cinerea is required for growth, development, and full virulence on bean plants. Eukaryot. Cell 7 (2008) 584-601
101. Schweizer A., Rupp S., Taylor B.N., Rollinghoff M., and Schroppel K. The TEA/ATTS transcription factor CaTec1p regulates hyphal development and virulence in Candida albicans. Mol. Microbiol. 38 (2000) 435-445
102. Smith D.G., Garcia-Pedrajas M.D., Hong W., Yu Z., Gold S.E., and Perlin M.H. An ste20 homologue in Ustilago maydis plays a role in mating and pathogenicity. Eukaryot. Cell 3 (2004) 180-189
103. Smith S.E., Csank C., Reyes G., Ghannoum M.A., and Berlin V. Candida albicans RHO1 is required for cell viability in vitro and in vivo. FEMS Yeast Res. 2 (2002) 103-111
104. Soriani F.M., Malavazi I., da Silva Ferreira M.E., Savoldi M., Von Zeska Kress M.R., de Souza Goldman M.H., Loss O., Bignell E., and Goldman G.H. Functional characterization of the Aspergillus fumigatus CRZ1 homologue, CrzA. Mol. Microbiol. 67 (2008) 1274-1291
105. Steinbach W.J., Cramer Jr. R.A., Perfect B.Z., Asfaw Y.G., Sauer T.C., Najvar L.K., Kirkpatrick W.R., Patterson T.F., Benjamin Jr. D.K., Heitman J., and Perfect J.R. Calcineurin controls growth, morphology, and pathogenicity in Aspergillus fumigatus. Eukaryot. Cell 5 (2006) 1091-1103
106. Steinbach W.J., Reedy J.L., Cramer Jr. R.A., Perfect J.R., and Heitman J. Harnessing calcineurin as a novel anti-infective agent against invasive fungal infections. Nat. Rev. Microbiol. 5 (2007) 418-430
107. Tatebayashi K., Tanaka K., Yang H.Y., Yamamoto K., Matsushita Y., Tomida T., Imai M., and Saito H. Transmembrane mucins Hkr1 and Msb2 are putative osmosensors in the SHO1 branch of yeast HOG pathway. EMBO J. 26 (2007) 3521-3533
108. Tatebayashi K., Yamamoto K., Tanaka K., Tomida T., Maruoka T., Kasukawa E., and Saito H. Adaptor functions of Cdc42, Ste50, and Sho1 in the yeast osmoregulatory HOG MAPK pathway. EMBO J. 25 (2006) 3033-3044
109. Truckses D.M., Bloomekatz J.E., and Thorner J. The RA domain of Ste50 adaptor protein is required for delivery of Ste11 to the plasma membrane in the filamentous growth signaling pathway of the yeast Saccharomyces cerevisiae. Mol. Cell Biol. 26 (2006) 912-928
110. Valiante V., Heinekamp T., Jain R., Hartl A., and Brakhage A.A. The mitogen-activated protein kinase MpkA of Aspergillus fumigatus regulates cell wall signaling and oxidative stress response. Fungal Genet. Biol. 45 (2008) 618-627
111. Verna J., Lodder A., Lee K., Vagts A., and Ballester R. A family of genes required for maintenance of cell wall integrity and for the stress response in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 94 (1997) 13804-13809
112. Walker L.A., Munro C.A., de Bruijn I., Lenardon M.D., McKinnon A., and Gow N.A. Stimulation of chitin synthesis rescues Candida albicans from echinocandins. PLoS Pathog. 4 (2008) e1000040
113. Wang P., and Heitman J. The cyclophilins. Genome Biol. 6 (2005) 226
114. Wang Y., and Dohlman H.G. Pheromone signaling mechanisms in yeast: a prototypical sex machine. Science 306 (2004) 1508-1509
115. Warmka J., Hanneman J., Lee J., Amin D., and Ota I. Ptc1, a type 2C Ser/Thr phosphatase, inactivates the HOG pathway by dephosphorylating the mitogen-activated protein kinase Hog1. Mol. Cell Biol. 21 (2001) 51-60
116. Wickes B.L., Edman U., and Edman J.C. The Cryptococcus neoformans STE12alpha gene: a putative Saccharomyces cerevisiae STE12 homologue that is mating type specific. Mol. Microbiol. 26 (1997) 951-960
117. Wu C., Leberer E., Thomas D.Y., and Whiteway M. Functional characterization of the interaction of Ste50p with Ste11p MAPKKK in Saccharomyces cerevisiae. Mol. Biol. Cell 10 (1999) 2425-2440
118. Wurgler-Murphy S.M., Maeda T., Witten E.A., and Saito H. Regulation of the Saccharomyces cerevisiae HOG1 mitogen-activated protein kinase by the PTP2 and PTP3 protein tyrosine phosphatases. Mol. Cell Biol. 17 (1997) 1289-1297
119. Xu J.R., and Hamer J.E. MAP kinase and cAMP signaling regulate infection structure formation and pathogenic growth in the rice blast fungus Magnaporthe grisea. Genes Dev. 10 (1996) 2696-2706
120. Xu J.R., Staiger C.J., and Hamer J.E. Inactivation of the mitogen-activated protein kinase Mps1 from the rice blast fungus prevents penetration of host cells but allows activation of plant defense responses. Proc. Natl. Acad. Sci. USA 95 (1998) 12713-12718
121. Xue T., Nguyen C.K., Romans A., and May G.S. A mitogen-activated protein kinase that senses nitrogen regulates conidial germination and growth in Aspergillus fumigatus. Eukaryot. Cell 3 (2004) 557-560
122. + and pH homeostasis: implications for salt tolerance, cell wall integrity and cell cycle progression. EMBO J. 21 (2002) 920-929
123. Yu G., Deschenes R.J., and Fassler J.S. The essential transcription factor, Mcm1, is a downstream target of Sln1, a yeast "two-component" regulator. J. Biol. Chem. 270 (1995) 8739-8743
124. Zhan X.L., Deschenes R.J., and Guan K.L. Differential regulation of FUS3 MAP kinase by tyrosine-specific phosphatases PTP2/PTP3 and dual-specificity phosphatase MSG5 in Saccharomyces cerevisiae. Genes Dev. 11 (1997) 1690-1702
125. Zhao X., Kim Y., Park G., and Xu J.R. A mitogen-activated protein kinase cascade regulating infection-related morphogenesis in Magnaporthe grisea. Plant Cell 17 (2005) 1317-1329
126. Zhao X., Mehrabi R., and Xu J.R. Mitogen-activated protein kinase pathways and fungal pathogenesis. Eukaryot. Cell 6 (2007) 1701-1714