The GPI-anchored protein Ecm33 is vital for conidiation, cell wall integrity, and multi-stress tolerance of two filamentous entomopathogens but not for virulence

Applied Microbiology and Biotechnology

Volumn 98, Issue 12, 2014, Pages 5517-5529

  Chen, Ying ^a   Zhu, Jing ^a   Ying, Sheng Hua ^a   Feng, Ming Guang ^a  

^a ZHEJIANG UNIVERSITY   (China)

Author keywords

Asexual development; Beauveria bassiana; Functional comparison; GPI anchored cell wall proteins; Metarhizium robertsii; Multi stress responses

Indexed keywords

AZO DYES; CELLS; ENZYME ACTIVITY; GENES; PROTEINS; SODIUM DODECYL SULFATE;

ASEXUAL DEVELOPMENT; BEAUVERIA BASSIANA; CELL WALL PROTEINS; FUNCTIONAL COMPARISON; METARHIZIUM ROBERTSII; MULTI-STRESS RESPONSES;

CYTOLOGY;

CARBENDAZIM; CONGO RED; DODECYL SULFATE SODIUM; ECM33 PROTEIN; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; HYDROGEN PEROXIDE; MANNITOL; MENADIONE; SODIUM CHLORIDE; TREHALOSE; UNCLASSIFIED DRUG; FUNGAL PROTEIN; GLYCOSYLPHOSPHATIDYLINOSITOL;

ALCOHOL; ASEXUAL REPRODUCTION; CELL ORGANELLE; ENTOMOPATHOGENIC ORGANISM; MUTATION; PROTEIN; TEMPERATURE TOLERANCE; VIRULENCE;

ARTICLE; BEAUVERIA BASSIANA; CONTROLLED STUDY; ENTOMOPATHOGENIC FUNGUS; FUNGAL CELL WALL; FUNGAL VIRULENCE; FUNGUS GROWTH; GENE DELETION; GENE DISRUPTION; HEAT TOLERANCE; HOST; METARHIZIUM; METARHIZIUM ROBERTSII; MULTI STRESS TOLERANCE; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; OSMOSIS; PROTEIN FUNCTION; STRESS; WILD TYPE; ANIMAL; BEAUVERIA; BIOASSAY; CELL WALL; FUNGUS SPORE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; OXIDATIVE STRESS; PATHOGENICITY; SPODOPTERA; VIRULENCE;

CORDYCEPS BASSIANA; FUNGI; HEXAPODA; METARHIZIUM;

ANIMALS; BEAUVERIA; BIOLOGICAL ASSAY; CELL WALL; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GLYCOSYLPHOSPHATIDYLINOSITOLS; METARHIZIUM; OXIDATIVE STRESS; SPODOPTERA; SPORES, FUNGAL; VIRULENCE;

EID: 84903819252     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-014-5577-y     Document Type: Article

References (51)

1. Bischoff JF, Rehner SA, Humber RA (2009) A multilocus phylogeny of the Metarhizium anisopliae lineage. Mycologia 101:512-530
2. Bruneau JM, Magnin T, Tagat E, Legrand R, Bernard M, Diaquin M, Fudali C, Latgé JP (2001) Proteome analysis of Aspergillus fumigatus identifies glycosylphosphatidylinositol-anchored proteins associated to the cell wall biosynthesis. Electrophoresis 22:2812-2823 (Pubitemid 32798952)
3. Caro LH, Tettelin H, Vossen JH, Ram AF, van den Ende H, Klis FM (1997) In silicio identification of glycosyl-phosphatidylinositol-anchored plasma-membrane and cell wall proteins of Saccharomyces cerevisiae. Yeast 13:1477-1489 (Pubitemid 27515734)
4. Castro Nda S, Maia ZA, Pereira M, Soares CM (2005) Screening for glycosylphosphatidylinositol-anchored proteins in the Paracoccidioides brasiliensis transcriptome. Genet Mol Res 4:326-345
5. Chabane S, Sarfati J, Ibrahim-Granet O, Du C, Schmidt C, Mouyna I, Prevost MC, Calderone R, Latgé JP (2006) Glycosylphosphatidylinositol- anchored Ecm33p influences conidial cell wall biosynthesis in Aspergillus fumigatus. Appl Environ Microbiol 72:3259-3267 (Pubitemid 43727974)
6. Chen Y, Zhu J, Ying SH, Feng MG (2014) Three mitogen-activated protein kinases required for cell wall integrity contribute greatly to biocontrol potential of a fungal entomopathogen. PLos ONE 9:e87948. doi:10.1371/journal. pone.0087948
7. Cid VJ, Durán A, del Rey F, Snyder MP, Nombela C, Sánchez M (1995) Molecular basis of cell integrity and morphogenesis in Saccharomyces cerevisiae. Microbiol Rev 59:345-386
8. Doehlemann G, Berndt P, Hahn M (2006) Trehalose metabolism is important for heat stress tolerance and spore germination of Botrytis cinerea. Microbiology UK 152:2625-2634 (Pubitemid 44405088)
9. Elbein AD, Pan YT, Pastuszak I, Carroll D (2003) New insights on trehalose: a multifunctional molecule. Glycobiology 13:17R-27R (Pubitemid 36592310)
10. Fang WG, Zhang YJ, Yang XY, Zheng X, Duan H, Li Y, Pei Y (2004) Agrobacterium tumefaciens-mediated transformation of Beauveria bassiana using an herbicide resistance gene as a selection marks. J Invertebr Pathol 85:18-24 (Pubitemid 38335236)
11. Frieman MB, Cormack BP (2003) The ω-site sequence of glycosylphosphatidylinositol-anchored proteins in Saccharomyces cerevisiae can determine distribution between the membrane and the cell wall. Mol Microbiol 50:883-896 (Pubitemid 37372251)
12. Gao Q, Jin K, Ying SH, Zhang Y, Xiao G, Shang Y, Duan Z, Hu X, Xie XQ, Zhou G, Peng G, Luo Z, Huang W, Wang B, Fang WG, Wang SB, Zhong Y, Ma LJ, St Leger RJ, Zhao GP, Pei Y, Feng MG, Xia YX, Wang CS (2011) Genome sequencing and comparative transcriptomics of the model entomopathogenic fungi Metarhizium anisopliae and M. acridum. PLoS Genet 7:e1001264
13. Hamada K, Terashima H, Arisawa M, Kitada K (1998) Amino acid sequence requirement for efficient incorporation of glycosylphosphatidylinositol- associated proteins into the cell wall of Saccharomyces cerevisiae. J Biol Chem 273:26946-26953 (Pubitemid 28471716)
14. Hamada K, Terashima H, Arisawa M, Yabuki N, Kitada K (1999) Amino acid residues in the ω-minus region participate in cellular localization of yeast glycosylphosphatidylinositol-attached proteins. J Bacteriol 181:3886-3889 (Pubitemid 29295903)
15. Huang BF, Feng MG (2009) Comparative tolerance of various Beauveria bassiana isolates to UV-B irradiation with a description of a modeling method to assess lethal dose. Mycopathologia 168:145-152
16. Jaiseng W, Fang Y, Ma Y, Sugiura R, Kuno T (2012) Studies on the roles of clathrin-mediated membrane trafficking and zinc transporter Cis4 in the transport of GPI-anchored proteins in fission yeast. PLoS ONE 7:e41946
17. Kapteyn JC, Van Den Ende H, Klis FM (1999) The contribution of cell wall proteins to the organization of the yeast cell wall. Biochim Biophys Acta 1426:373-383 (Pubitemid 29027952)
18. Lesage G, Bussey H (2006) Cell wall assembly in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 70:317-343 (Pubitemid 43895030)
19. Levdansky E, Kashi O, Sharon H, Shadkchan Y, Osherov N (2010) The Aspergillus fumigatus cspA gene encoding a repeat-rich cell wall protein is important for normal conidial cell wall architecture and interaction with host cells. Eukaryot Cell 9:1403-1415
20. Li J, Feng MG (2009) Intraspecific tolerance of Metarhizium anisopliae conidia to the upper thermal limits of summer with a description of a quantitative assay system. Mycol Res 113:93-99
21. Li J, Ying SH, Shan LT, Feng MG (2010) A new non-hydrophobic cell wall protein (CWP10) of Metarhizium anisopliae enhances conidial hydrophobicity when expressed in Beauveria bassiana. Appl Microbiol Biotechnol 85:975-984
22. Liu Q, Ying SH, Feng MG, Jiang XH (2009) Physiological implication of intracellular trehalose and mannitol changes in response of entomopathogenic fungus Beauveria bassiana to thermal stress. Antonie Van Leeuwenhoek 95:65-75
23. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔT method. Methods 25:402-408 (Pubitemid 34164012)
24. Luo XD, Keyhani NO, Yu XD, He ZJ, Luo ZB, Pei Y, Zhang YJ (2012) The MAP kinase Bbslt2 controls growth, conidiation, cell wall integrity, and virulence in the insect pathogenic fungus Beauveria bassiana. Fungal Genet Biol 49:544-555
25. Martínez-López R, Monteoliva L, Diez-Orejas R, Nombela C, Gil C (2004) The GPI-anchored protein CaEcm33 is required for cell wall integrity, morphogenesis and virulence in Candida albicans. Microbiology SGM 150:3341-3354 (Pubitemid 39406204)
26. Martínez-López R, Park H, Myers CL, Gil C, Filler SG (2006) Candida albicans Ecm33p is important for normal cell wall architecture and interactions with host cells. Eukaryot Cell 5:140-147 (Pubitemid 43113459)
27. Martínez-López R, Nombela C, Diez-Orejas R, Monteoliva L, Gil C (2008) Immunoproteomic analysis of the protective response obtained from vaccination with Candida albicans ecm33 cell wall mutant in mice. Proteomics 8:2651-2664 (Pubitemid 351988570)
28. Mouyna I, Fontaine T, Vai M, Monod M, Fonzi WA, Diaquin M, Popolo L, Hartland RP, Latgé JP (2000) Glycosylphosphatidylinositol-anchored glucanosyltransferases play an active role in the biosynthesis of the fungal cell wall. J Biol Chem 275:14882-14889 (Pubitemid 30337202)
29. Pardo M, Monteoliva L, Vázquez P, Martínez R, Molero G, Nombela C, Gil C (2004) PST1 and ECM33 encode two yeast cell surface GPI proteins important for cell wall integrity. Microbiology SGM 150:4157-4170 (Pubitemid 40045344)
30. Percival-Smith A, Segall J (1987) Increased copy number of the 5′ end of the SPS2 gene inhibits sporulation of Saccharomyces cerevisiae. Mol Cell Biol 7:2484-2490
31. Rangel DE, Anderson AJ, Roberts DW (2008) Evaluating physical and nutritional stress during mycelia growth as inducers of tolerance to heat and UV-B radiation in Metarhizium anisopliae conidia. Mycol Res 112:1362-1372
32. Rispail N, Soanes DM, Ant C, Czajkowski R, Grünler A, Huguet R, Perez-Nadales E, Poli A, Sartorel E, Valiante V, Yang M, Beffa R, Brakhage AA, Gow NAR, Kahmann R, Lebrun MH, Lenasi H, Perez-Martin J, Talbot NJ, Wendland J, Di Pietro A (2009) Comparative genomics of MAP kinase and calcium-calcineurin signaling components in plant and human pathogenic fungi. Fungal Genet Biol 46:287-298
33. Roberts DW, St Leger RJ (2004) Metarhizium spp., cosmopolitan insect pathogenic fungi: mycological aspects. Adv Appl Microbiol 54:1-70 (Pubitemid 38898744)
34. Romano J, Nimrod G, Ben-Tal N, Shadkchan Y, Baruch K, Sharon H, Osherov N (2006) Disruption of the Aspergillus fumigatus ECM33 homologue results in rapid conidial germination, antifungal resistance and hypervirulence. Microbiology SGM 152:1919-1928 (Pubitemid 44070450)
35. + is a target of the two transcription factors Atf1 and Mbx1 and negatively regulates Pmk1 MAPK cell integrity signaling in fission yeast. Mol Biol Cell 21:674-685
36. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 10:2731-2739
37. Terashima H, Hamada K, Kitada K (2003) The localization change of Ybr078w/Ecm33, a yeast GPI-associated protein, from the plasma membrane to the cell wall, affecting the cellular function. FEMS Microbiol Lett 218:175-180 (Pubitemid 36173545)
38. Tohe A, Oguchi T (1999) Las21 participates in extracellular/cell surface phenomena in Saccharomyces cerevisiae. Genes Genet Syst 74:241-256
39. Tougan T, Chiba Y, Kakihara Y, Hirata A, Nohima H (2002) Meu10 is required for spore wall maturation in Schizosaccharomyces pombe. Genes Cells 7:217-231 (Pubitemid 34213365)
40. Vega FE, Meyling NV, Luangsa-Ard JJ, Blackwell M (2012) Fungal entomopathogens. In: Vega F, Kaya HK (eds) Insect pathology, 2nd edn. Academic, San Diego, pp 171-220
41. Walker CA, Gómez BL, Mora-Montes HM, Mackenzie KS, Munro CA, Brown AJ, Gow NA, Kibbler CC, Odds FC (2010) Melanin externalization in Candida albicans depends on cell wall chitin structures. Eukaryot Cell 9:1329-1342
42. Wanchoo A, Lewis MW, Keyhani NO (2009) Lectin mapping reveals stage-specific display of surface carbohydrates in in vitro and haemolymph-derived cells of the entomopathogenic fungus Beauveria bassiana. Microbiology SGM 155:3123-3133
43. Wang CS, Feng MG (2014) Advances in fundamental and applied studies in China of fungal biocontrol agents for use against arthropod pests. Biol Control 68:129-135
44. Wang ZL, Lu JD, Feng MG (2012) Primary roles of two dehydrogenases in the mannitol metabolism and multi-stress tolerance of entomopathogenic fungus Beauveria bassiana. Environ Microbiol 14:2139-2150
45. Xiao GH, Ying SH, Zheng P, Wang ZL, Zhang SW, Xie XQ, Shang YF, Zheng HJ, Zhou Y, St Leger RJ, Zhao GP, Wang CS, Feng MG (2012) Genomic perspectives on the evolution of fungal entomopathogenicity in Beauveria bassiana. Sci Rep 2:483. doi:10.1038.srep00483
46. Xie XQ, Li F, Ying SH, Feng MG (2012) Additive contributions of two manganese-cored superoxide dismutases (MnSODs) to antioxidation, UV tolerance and virulence of Beauveria bassiana. PLoS ONE 7:e30298
47. Yao SL, Ying SH, Feng MG, Hatting JL (2010) In vitro and in vivo responses of fungal biocontrol agents to the gradient doses of UV-B and UV-A irradiations. BioControl 55:413-422
48. Yin QY, de Groot PW, Dekker HL, de Jong L, Klis FM, de Koster CG (2005) Comprehensive proteomic analysis of Saccharomyces cerevisiae cell walls: identification of proteins covalently attached via glycosylphosphatidylinositol remnants or mild alkali-sensitive linkages. J Biol Chem 280:20894-20901 (Pubitemid 40776795)
49. Zhang YJ, Zhao JH, Fang WG, Zhang JQ, Luo ZB, Zhang M, Fan YH, Pei Y (2009) Mitogen-activated protien kinase hog1 in the entomopathogenic fungus Beauveria bassiana regulates environmental stress responses and virulence to insects. Appl Environ Microbiol 75:3787-3795
50. Zheng P, Xia YL, Xiao GH, Xiong CH, Zhang SW, Zheng HJ, Huang Y, Zhou Y, Wang SY, Zhao GP, Liu XZ, St Leger RJ, Wang CS (2011) Genome sequence of the insect pathogenic fungus Cordyceps militaris, a valued traditional Chinese medicine. Genome Biol 12:R116
51. Zhou G, Wang J, Qiu L, Feng MG (2012) 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. Environ Microbiol 14:817- 829