A Group III histidine kinase (mhk1) upstream of high-osmolarity glycerol pathway regulates sporulation, multi-stress tolerance and virulence of Metarhizium robertsii, a fungal entomopathogen

Environmental Microbiology

Volumn 14, Issue 3, 2012, Pages 817-829

  Zhou, Gang ^a   Wang, Jie ^a   Qiu, Lei ^a   Feng, Ming Guang ^a  

^a ZHEJIANG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGICIDE; GLYCEROL; PROTEIN HISTIDINE KINASE; PROTEIN KINASE; PROTEIN-HISTIDINE KINASE;

ANIMAL; ARTICLE; METABOLISM; METARHIZIUM; MICROBIOLOGY; OSMOLARITY; PATHOGENICITY; PHOSPHORYLATION; PHYSIOLOGICAL STRESS; PHYSIOLOGY; TENEBRIO; VIRULENCE;

ANIMALS; FUNGICIDES, INDUSTRIAL; GLYCEROL; METARHIZIUM; OSMOLAR CONCENTRATION; PHOSPHORYLATION; PROTEIN KINASES; STRESS, PHYSIOLOGICAL; TENEBRIO; VIRULENCE;

METARHIZIUM; TENEBRIO; TENEBRIO MOLITOR;

EID: 84857914482     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2011.02643.x     Document Type: Article

References (44)

1. Angelova, M.B., Pashova, S.B., Spasova, B.K., Vassilev, S.V., and Slokoska, L.S. (2005) Oxidative stress response of filamentous fungi induced by hydrogen peroxide and paraquat. Mycol Res 109: 150-158.
2. Bischoff, J.F., Rehner, S.A., and Humber, R.A. (2009) A multilocus phylogeny of the Metarhizium anisopliae lineage. Mycologia 101: 512-530.
3. Braga, G.U., Rangel, D.E., Flint, S.D., Anderson, A.J., and Roberts, D.W. (2006) Conidial pigmentation is important to tolerance against solar-simulated radiation in the entomopathogenic fungus Metarhizium anisopliae. Photochem Photobiol 82: 418-422.
4. Catlett, N.L., Yoder, O.C., and Turgeon, B.G. (2003) Whole-genome analysis of two-component signal transduction genes in fungal pathogens. Eukaryot Cell 2: 1151-1161.
5. Chang, L., and Karin, M. (2001) Mammalian MAP kinase signalling cascades. Nature 410: 37-40.
6. Dixon, K.P., Xu, J.R., Smirnoff, N., and Talbot, N.J. (1999) Independent signaling pathways regulate cellular turgor during hyperosmotic stress and appressorium-mediated plant Infection by Magnaporthe grisea. Plant Cell 11: 2045-2058.
7. Dongo, A., Bataille-Simoneau, N., Campion, C., Guillemette, T., Hamon, B., Iacomi-Vasilescu, B., etal. (2009) The Group III two-component histidine kinase of filamentous fungi is involved in the fungicidal activity of the bacterial polyketide ambruticin. Appl Environ Microbiol 75: 127-134.
8. Duarte, R.T.D., Staats, C.C., Fungaro, M.H.P., Schrank, A., Vainsten, M.H., Furlaneto-Maia, L., etal. (2007) Development of a simple and rapid Agrobacterium tumefaciens-mediated transformation system for the entomopathogenic fungus Metarhizium anisopliae var. acridum. Lett Appl Microbiol 44: 248-254.
9. Fang, W.G., Pei, Y., and Bidochka, M.J. (2006) Transformation of Metarhizium anisopliae mediated by Agrobacterium tumefaciens. Can J Microbiol 52: 623-626.
10. Fang, W., Pei, Y., and Bidochka, M.J. (2007) A regulator of a G protein signalling (RGS) gene, cag8, from the insect-pathogenic fungus Metarhizium anisopliae is involved in conidiation, virulence and hydrophobin synthesis. Microbiology 153: 1017-1025.
11. de Faria, M.R., and Wraight, S.P. (2007) Mycoinsecticides and mycoacaricides: a comprehensive list with worldwide coverage and international classification of formulation types. Biol Control 43: 237-256.
12. Furukawa, K., Katsuno, Y., Urao, T., Yabe, T., Yamada-Okabe, T., Yamada-Okabe, H., etal. (2002) Isolation and functional analysis of a gene, tcsB, encoding a transmembrane hybrid-type histidine kinase from Aspergillus nidulans. Appl Environ Microbiol 68: 5304-5310.
13. Gao, Q., Jin, K., Ying, S.H., Zhang, Y., Xiao, G., Shang, Y., etal. (2011) Genome sequencing and comparative transcriptomics of the model entomopathogenic fungi Metarhizium anisopliae and M.acridum. PLoS Genet 7: e1001264.
14. 2 and the acquisition of oxidative tolerance in Candida albicans. Yeast 20: 1161-1169.
15. Izumitsu, K., Yoshimi, A., Kubo, D., Morita, A., Saitoh, Y., and Tanaka, C. (2009) The MAPKK kinase ChSte11 regulates sexual/asexual development, melanization, pathogenicity, and adaptation to oxidative stress in Cochliobolus heterostrophus. Curr Genet 55: 439-448.
16. Jeong, J.H., Kwon, E.S., and Roe, J.H. (2001) Characterization of the manganese-containing superoxide dismutase and its gene regulation in stress response of Schizosaccharomyces pombe. Biochem Biophys Res Commun 283: 908-914.
17. Jones, C.A., Greer-Phillips, S.E., and Borkovich, K.A. (2007) 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: 2123-2136.
18. Kashyap, R.S., Rajan, A.N., Ramteke, S.S., Agrawal, V.S., Kelkar, S.S., Purohit, H.J., etal. (2007) Diagnosis of tuberculosis in an Indian population by an indirect ELISA protocol based on detection of Antigen 85 complex: a prospective cohort study. BMC Infect Dis 7: 74.
19. Khang, C.H., Park, S.Y., Lee, Y.H., and Kang, S. (2005) A dual selection based, targeted gene replacement tool for Magnaporthe grisea and Fusarium oxysporum. Fungal Genet Biol 42: 483-492.
20. Lin, C.H., and Chung, K.R. (2010) Specialized and shared functions of the histidine kinase- and HOG1 MAP kinase-mediated signaling pathways in Alternaria alternata, a filamentous fungal pathogen of citrus. Fungal Genet Biol 47: 818-827.
21. Liu, W.W., Leroux, P., and Fillinger, S. (2008) The HOG1-like MAP kinase Sak1 of Botrytis cinerea is negatively regulated by the upstream histidine kinase Bos1 and is not involved in dicarboximide- and phenylpyrrole-resistance. Fungal Genet Biol 45: 1062-1074.
22. Livak, K.J., and Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408.
23. Marina, A., Waldburger, C.D., and Hendrickson, W.A. (2005) Structure of the entire cytoplasmic portion of a sensor histidine-kinase protein. EMBO J 24: 4247-4259.
24. Motoyama, T., Ochiai, N., Morita, M., Iida, Y., Usami, R., and Kudo, T. (2008) Involvement of putative response regulator genes of the rice blast fungus Magnaporthe oryzae in osmotic stress response, fungicide action, and pathogenicity. Curr Genet 54: 185-195.
25. Nathues, E., Jorgens, C., Lorenz, N., and Tudzynski, P. (2007) The histidine kinase CpHK2 has impact on spore germination, oxidative stress and fungicide resistance, and virulence of the ergot fungus Claviceps purpurea. Mol Plant Pathol 8: 653-665.
26. Rispail, N., and Di Pietro, A. (2010) The two-component histidine kinase Fhk1 controls stress adaptation and virulence of Fusarium oxysporum. Mol Plant Pathol 11: 395-407.
27. Roberts, D., and St Leger, R. (2004) Metarhizium spp., cosmopolitan insect-pathogenic fungi: mycological aspects. Adv Appl Microbiol 54: 1-70.
28. Saito, H., and Tatebayashi, K. (2004) Regulation of the osmoregulatory HOG MAPK cascade in yeast. J Biol Chem 136: 267-272.
29. Santos, J.L., and Shiozaki, K. (2001) Fungal histidine kinases. Sci STKE 2001: re1.
30. Tang, Q.Y., and Feng, M.G. (2007) DPS Data Processing System: Experimental Design, Statistical Analysis and Data Mining. Beijing: Science Press.
31. Thomason, P., and Kay, R. (2000) Eukaryotic signal transduction via histidine-aspartate phosphorelay. J Cell Sci 113: 3141-3150.
32. Viaud, M., Fillinger, S., Liu, W., Polepalli, J.S., Le Pecheur, P., Kunduru, A.R., etal. (2006) A class III histidine kinase acts as a novel virulence factor in Botrytis cinerea. Mol Plant Microbe Interact 19: 1042-1050.
33. Wang, F., Tao, J.H., Qian, Z., You, S., Dong, H., Shen, H., etal. (2009) A histidine kinase PmHHK1 regulates polar growth, sporulation and cell wall composition in the dimorphic fungus Penicillium marneffei. Mycol Res 113: 915-923.
34. West, A.H., and Stock, A.M. (2001) Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem Sci 26: 369-376.
35. Wolanin, P.M., Thomason, P.A., and Stock, J.B. (2002) Histidine protein kinases: key signal transducers outside the animal kingdom. Genome Biol 3: reviews3013.1-reviews3013.8.
36. Xie, X.Q., Wang, J., Huang, B.F., Ying, S.H., and Feng, M.G. (2010) A new manganese superoxide dismutase identified from Beauveria bassiana enhances virulence and stress tolerance when overexpressed in the fungal pathogen. Appl Microbiol Biotechnol 86: 1543-1553.
37. Yan, L., Yang, Q., Sundin, G.W., Li, H., and Ma, Z. (2010) The mitogen-activated protein kinase kinase BOS5 is involved in regulating vegetative differentiation and virulence in Botrytis cinerea. Fungal Genet Biol 47: 753-760.
38. Ying, S.H., and Feng, M.G. (2004) Relationship between thermotolerance and hydrophobin-like proteins in aerial conidia of Beauveria bassiana and Paecilomyces fumosoroseus as fungal biocontrol agents. J Appl Microbiol 97: 323-331.
39. Ying, S.H., and Feng, M.G. (2006) Novel blastospore-based transformation system for integration of phosphinothricin resistance and green fluorescence protein genes into Beauveria bassiana. Appl Microbiol Biotechnol 72: 206-210.
40. Ying, S.H., and Feng, M.G. (2011) A conidial protein (CP15) of Beauveria bassiana contributes to the conidial tolerance of the entomopathogenic fungus to thermal and oxidative stresses. Appl Microbiol Biotechnol 90: 1711-1720.
41. Yoshimi, A., Kojima, K., Takano, Y., and Tanaka, C. (2005) Group III histidine kinase is a positive regulator of Hog1-type mitogen-activated protein kinase in filamentous fungi. Eukaryot Cell 4: 1820-1828.
42. Zhang, H., Liu, K., Zhang, X., Song, W., Zhao, Q., Dong, Y., etal. (2010) A two-component histidine kinase, MoSLN1, is required for cell wall integrity and pathogenicity of the rice blast fungus, Magnaporthe oryzae. Curr Genet 56: 517-528.
43. Zhang, S., Fan, Y., Xia, Y.X., and Keyhani, N.O. (2010) Sulfonylurea resistance as a new selectable marker for the entomopathogenic fungus Beauveria bassiana. Appl Microbiol Biotechnol 87: 1151-1156.
44. Zhang, Y.J., Zhao, J.H., Fang, W.G., Zhang, J.Q., Luo, Z.B., Zhang, M., etal. (2009) Mitogen-activated protein kinase hog1 in the entomopathogenic fungus Beauveria bassiana regulates environmental stress responses and virulence to insects. Appl Environ Microbiol 75: 3787-3795.