The HOG signal transduction pathway in the halophilic fungus Wallemia ichthyophaga: Identification and characterisation of MAP kinases WiHog1A and WiHog1B

Extremophiles

Volumn 17, Issue 4, 2013, Pages 623-636

  Konte, Tilen ^a   Plemenitas, Ana ^a  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

Basidiomycetous fungus; HOG pathway; Hog1; MAPK; Obligatory halophile; Wallemia ichthyophaga

Indexed keywords

FUNGI; SACCHAROMYCES CEREVISIAE; WALLEMIA ICHTHYOPHAGA;

EID: 84879507441     PISSN: 14310651     EISSN: 14334909     Source Type: Journal    
DOI: 10.1007/s00792-013-0546-4     Document Type: Article

References (55)

1. Anisimova M, Gascuel O (2006) Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst Biol 55: 539-552.
2. Bahn YS, Kojima K, Cox GM, Heitman J (2005) Specialization of the HOG pathway and its impact on differentiation and virulence of Cryptococcus neoformans. Mol Biol Cell 16: 2285-2300.
3. Bahn YS, Geunes-Boyer S, Heitman J (2007) Ssk2 mitogen-activated protein kinase kinase kinase governs divergent patterns of the stress-activated Hog1 signaling pathway in Cryptococcus neoformans. Eukaryot Cell 6: 2278-2289.
4. Bell M, Engelberg D (2003) Phosphorylation of Tyr-176 of the yeast MAPK Hog1/p38 is not vital for Hog1 biological activity. J Biol Chem 278: 14603-14606.
5. Bell M, Capone R, Pashtan I, Levitzki A, Engelberg D (2001) Isolation of hyperactive mutants of the MAPK p38/Hog1 that are independent of MAPK kinase activation. J Biol Chem 276: 25351-25358.
6. Brewster JL, de Valoir T, Dwyer ND, Winter E, Gustin MC (1993) An osmosensing signal transduction pathway in yeast. Science 259: 1760-1763.
7. Chen RE, Thorner J (2007) Function and regulation in MAPK signaling pathways: lessons learned from the yeast Saccharomyces cerevisiae. Biochim Biophys Acta 1773: 1311-1340.
8. de Nadal E, Alepuz PM, Posas F (2002) Dealing with osmostress through MAP kinase activation. EMBO Rep 3: 735-740.
9. Fettich M, Lenassi M, Veranic P, Gunde-Cimerman N, Plemenitas A (2011) Identification and characterization of putative osmosensors, HwSho1A and HwSho1B, from the extremely halotolerant black yeast Hortaea werneckii. Fungal Genet Biol 48: 475-484.
10. Furukawa K, Hoshi Y, Maeda T, Nakajima T, Abe K (2005) Aspergillus nidulans HOG pathway is activated only by two-component signalling pathway in response to osmotic stress. Mol Microbiol 56: 1246-1261.
11. Gietz RD, Schiestl RH (2007) Quick and easy yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc 2: 35-37.
12. Gostincar C, Lenassi M, Gunde-Cimerman N, Plemenitas A (2011) Fungal adaptation to extremely high salt concentrations. Adv Appl Microbiol 77(77): 71-96.
13. Gottlich E, deHoog GS, Yoshida S, Takeo K, Nishimura K, Miyaji M (1995) Cell-surface hydrophobicity and lipolysis as essential factors in human Tinea nigra. Mycoses 38: 489-494.
14. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3. 0. Syst Biol 59: 307-321.
15. Gunde-Cimerman N, Zalar P, de Hoog S, Plemenitas A (2000) Hypersaline waters in salterns-natural ecological niches for halophilic black yeasts. FEMS Microbiol Ecol 32: 235-240.
16. Gunde-Cimerman N, Ramos J, Plemenitas A (2009) Halotolerant and halophilic fungi. Mycol Res 113: 1231-1241.
17. Gustin MC, Albertyn J, Alexander M, Davenport K (1998) MAP kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol Mol Biol Rev 62: 1264-1300.
18. Han KH, Prade RA (2002) Osmotic stress-coupled maintenance of polar growth in Aspergillus nidulans. Mol Microbiol 43: 1065-1078.
19. Heermann R, Jung K (2004) Structural features and mechanisms for sensing high osmolarity in microorganisms. Curr Opin Microbiol 7: 168-174.
20. Hohmann S, Krantz M, Nordlander B (2007) Yeast osmoregulation. Methods Enzymol 428: 29-45.
21. Kondrashov FA, Rogozin IB, Wolf YI, Koonin EV (2002) Selection in the evolution of gene duplications. Genome Biol 3: 1-9.
22. Kralj Kuncic M, Kogej T, Drobne D, Gunde-Cimerman N (2010) Morphological response of the halophilic fungal genus Wallemia to high salinity. Appl Environ Microbiol 76: 329-337.
23. Krantz M, Becit E, Hohmann S (2006a) Comparative analysis of HOG pathway proteins to generate hypotheses for functional analysis. Curr Genet 49: 152-165.
24. Krantz M, Becit E, Hohmann S (2006b) Comparative genomics of the HOG-signalling system in fungi. Curr Genet 49: 137-151.
25. Lenassi M, Plemenitas A (2007) Novel group VII histidine kinase HwHhk7B from the halophilic fungi Hortaea werneckii has a putative role in osmosensing. Curr Genet 51: 393-405.
26. Lenassi M, Vaupotic T, Gunde-Cimerman N, Plemenitas A (2007) The MAP kinase HwHog1 from the halophilic black yeast Hortaea werneckii: coping with stresses in solar salterns. Saline Systems 3: 3.
27. Lenassi M, Zajc J, Gostincar C, Gorjan A, Gunde-Cimerman N, Plemenitas A (2011) Adaptation of the glycerol-3-phosphate dehydrogenase Gpd1 to high salinities in the extremely halotolerant Hortaea werneckii and halophilic Wallemia ichthyophaga. Fungal Biol 115: 959-970.
28. Maayan I, Beenstock J, Marbach I, Tabachnick S, Livnah O, Engelberg D (2012) Osmostress induces autophosphorylation of Hog1 via a C-terminal regulatory region that is conserved in p38alpha. PLoS ONE 7: e44749.
29. Maeda T, Wurglermurphy SM, Saito H (1994) A 2-component system that regulates an osmosensing map kinase cascade in yeast. Nature 369: 242-245.
30. Mas G, de Nadal E, Dechant R, Rodriguez de la Concepcion ML, Logie C, Jimeno-Gonzalez S, Chavez S, Ammerer G, Posas F (2009) Recruitment of a chromatin remodelling complex by the Hog1 MAP kinase to stress genes. EMBO J 28: 326-336.
31. Miller JH (1972) Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
32. Murakami Y, Tatebayashi K, Saito H (2008) Two adjacent docking sites in the yeast Hog1 mitogen-activated protein (MAP) kinase differentially interact with the Pbs2 MAP kinase kinase and the Ptp2 protein tyrosine phosphatase. Mol Cell Biol 28: 2481-2494.
33. Notredame C, Higgins DG, Heringa J (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302: 205-217.
34. O'Rourke SM, Herskowitz I (1998) The Hog1 MAPK prevents cross talk between the HOG and pheromone response MAPK pathways in Saccharomyces cerevisiae. Genes Dev 12: 2874-2886.
35. Padamsee M, Kumar TK, Riley R, Binder M, Boyd A, Calvo AM, Furukawa K, Hesse C, Hohmann S, James TY, LaButti K, Lapidus A, Lindquist E, Lucas S, Miller K, Shantappa S, Grigoriev IV, Hibbett DS, McLaughlin DJ, Spatafora JW, Aime MC (2012) The genome of the xerotolerant mold Wallemia sebi reveals adaptations to osmotic stress and suggests cryptic sexual reproduction. Fungal Genet Biol 49: 217-226.
36. Petelenz-Kurdziel E, Eriksson E, Smedh M, Beck C, Hohmann S, Goksor M (2011) Quantification of cell volume changes upon hyperosmotic stress in Saccharomyces cerevisiae. Integr Biol (Camb) 3: 1120-1126.
37. Plemenitas A, Vaupotic T, Lenassi M, Kogej T, Gunde-Cimerman N (2008) Adaptation of extremely halotolerant black yeast Hortaea werneckii to increased osmolarity: a molecular perspective at a glance. Stud Mycol 61: 67-75.
38. Reiser V, Ruis H, Ammerer G (1999) Kinase activity-dependent nuclear export opposes stress-induced nuclear accumulation and retention of Hog1 mitogen-activated protein kinase in the budding yeast Saccharomyces cerevisiae. Mol Biol Cell 10: 1147-1161.
39. Reyes G, Romans A, Nguyen CM, May GS (2006) Novel mitogen-activated protein kinase MpkC of Aspergillus fumigatus is required for utilization of polyalcohol sugars. Eukaryot Cell 5: 1934-1940.
40. Rizner TL, Moeller G, Thole HH, Zakelj-Mavric M, Adamski J (1999) A novel 17 beta-hydroxysteroid dehydrogenase in the fungus Cochliobolus lunatus: new insights into the evolution of steroid-hormone signalling. Biochem J 337: 425-431.
41. Rozman D, Komel R (1994) Isolation of genomic DNA from filamentous fungi with high glucan level. Biotechniques 16: 382-384.
42. Saito H (2010) Regulation of cross-talk in yeast MAPK signaling pathways. Curr Opin Microbiol 13: 677-683.
43. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671-675.
44. Sole C, Nadal-Ribelles M, Kraft C, Peter M, Posas F, de Nadal E (2011) Control of Ubp3 ubiquitin protease activity by the Hog1 SAPK modulates transcription upon osmostress. EMBO J 30: 3274-3284.
45. Tanoue T, Nishida E (2003) Molecular recognitions in the MAP kinase cascades. Cell Signal 15: 455-462.
46. Turk M, Plemenitas A (2002) The HOG pathway in the halophilic black yeast Hortaea werneckii: isolation of the HOG1 homolog gene and activation of HwHog1p. FEMS Microbiol Lett 216: 193-199.
47. Vaupotic T, Plemenitas A (2007) Differential gene expression and Hog1 interaction with osmoresponsive genes in the extremely halotolerant black yeast Hortaea werneckii. BMC Genomics 8: 280.
48. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ (2009) Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189-1191.
49. Westfall PJ, Thorner J (2006) Analysis of mitogen-activated protein kinase signaling specificity in response to hyperosmotic stress: use of an analog-sensitive HOG1 allele. Eukaryot Cell 5: 1215-1228.
50. Westfall PJ, Ballon DR, Thorner J (2004) When the stress of your environment makes you go HOG wild. Science 306: 1511-1512.
51. Westfall PJ, Patterson JC, Chen RE, Thorner J (2008) Stress resistance and signal fidelity independent of nuclear MAPK function. Proc Natl Acad Sci USA 105: 12212-12217.
52. Wilkins MR, Gasteiger E, Bairoch A, Sanchez JC, Williams KL, Appel RD, Hochstrasser DF (1999) Protein identification and analysis tools in the ExPASy server. Methods Mol Biol 112: 531-552.
53. Wu XC, Chi XQ, Wang PM, Zheng DQ, Ding R, Li YD (2010) The evolutionary rate variation among genes of HOG-signaling pathway in yeast genomes. Biol Direct 5: 46.
54. Xue T, Nguyen CK, Romans A, May GS (2004) A mitogen-activated protein kinase that senses nitrogen regulates conidial germination and growth in Aspergillus fumigatus. Eukaryot Cell 3: 557-560.
55. Zalar P, Sybren de Hoog G, Schroers HJ, Frank JM, Gunde-Cimerman N (2005) Taxonomy and phylogeny of the xerophilic genus Wallemia (Wallemiomycetes and Wallemiales, cl. et ord. nov.). Antonie van Leeuwenhoek 87: 311-328.