The GPI-anchored protein Ecm33 is vital for conidiation, cell wall integrity, and multi-stress tolerance of two filamentous entomopathogens but not for virulence
详细信息    查看全文
  • 作者:Ying Chen (1)
    Jing Zhu (1)
    Sheng-Hua Ying (1)
    Ming-Guang Feng (1)
  • 关键词:Beauveria bassiana ; Metarhizium robertsii ; GPI ; anchored cell wall proteins ; Functional comparison ; Asexual development ; Multi ; stress responses
  • 刊名:Applied Microbiology and Biotechnology
  • 出版年:2014
  • 出版时间:June 2014
  • 年:2014
  • 卷:98
  • 期:12
  • 页码:5517-5529
  • 全文大小:
  • 参考文献:1. Bischoff JF, Rehner SA, Humber RA (2009) A multilocus phylogeny of the / Metarhizium anisopliae lineage. Mycologia 101:512-30 CrossRef
    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 22:2812-823 CrossRef
    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 13:1477-489 CrossRef
    4. Castro Nda S, Maia ZA, Pereira M, Soares CM (2005) Screening for glycosylphosphatidylinositol-anchored proteins in the / Paracoccidioides brasiliensis transcriptome. Genet Mol Res 4:326-45
    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 72:3259-267 CrossRef
    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 59:345-86
    8. Doehlemann G, Berndt P, Hahn M (2006) Trehalose metabolism is important for heat stress tolerance and spore germination of / Botrytis cinerea. Microbiology UK 152:2625-634 CrossRef
    9. Elbein AD, Pan YT, Pastuszak I, Carroll D (2003) New insights on trehalose: a multifunctional molecule. Glycobiology 13:17R-7R CrossRef
    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 85:18-4 CrossRef
    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 50:883-96 CrossRef
    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 CrossRef
    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 273:26946-6953 CrossRef
    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 181:3886-889
    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 168:145-52 CrossRef
    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 CrossRef
    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 1426:373-83 CrossRef
    18. Lesage G, Bussey H (2006) Cell wall assembly in / Saccharomyces cerevisiae. Microbiol Mol Biol Rev 70:317-43 CrossRef
    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 9:1403-415 CrossRef
    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 113:93-9 CrossRef
    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 85:975-84 CrossRef
    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 95:65-5 CrossRef
    23. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2?Δοem class="a-plus-plus">C T method. Methods 25:402-08 CrossRef
    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 49:544-55 CrossRef
    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 150:3341-354 CrossRef
    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 5:140-47 CrossRef
    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 8:2651-664 CrossRef
    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 275:14882-4889 CrossRef
    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 150:4157-170 CrossRef
    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 7:2484-490
    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 112:1362-372 CrossRef
    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 46:287-98 CrossRef
    33. Roberts DW, St Leger RJ (2004) / Metarhizium spp., cosmopolitan insect pathogenic fungi: mycological aspects. Adv Appl Microbiol 54:1-0 CrossRef
    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 152:1919-928 CrossRef
    35. Takada H, Nishida A, Domae M, Kita A, Yamano Y, Uchida A, Ishiwata S, Fang Y, Zhou X, Masuko T, Kinoshita M, Kakehi K, Sugiura R (2010) The cell surface protein gene / ecm33 / + 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 21:674-85 CrossRef
    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 10:2731-739 CrossRef
    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 218:175-80 CrossRef
    38. Tohe A, Oguchi T (1999) Las21 participates in extracellular/cell surface phenomena in / Saccharomyces cerevisiae. Genes Genet Syst 74:241-56 CrossRef
    39. Tougan T, Chiba Y, Kakihara Y, Hirata A, Nohima H (2002) Meu10 is required for spore wall maturation in / Schizosaccharomyces pombe. Genes Cells 7:217-31 CrossRef
    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 171-20 CrossRef
    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 9:1329-342 CrossRef
    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 155:3123-133 CrossRef
    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 68:129-35 CrossRef
    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 14:2139-150 CrossRef
    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 anti-oxidation, UV tolerance and virulence of / Beauveria bassiana. PLoS ONE 7:e30298 CrossRef
    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 55:413-22 CrossRef
    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 280:20894-0901 CrossRef
    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 75:3787-795
    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 CrossRef
    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 14:817-29 CrossRef
  • 作者单位:Ying Chen (1)
    Jing Zhu (1)
    Sheng-Hua Ying (1)
    Ming-Guang Feng (1)

    1. Institute of Microbiology, College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, 310058, People’s Republic of China
  • ISSN:1432-0614
文摘
Ecm33 is one of several glycosylphosphatidylinositol (GPI)-anchored proteins. This protein is known to be involved in fungal cell wall integrity, but its contribution to multi-stress tolerance is largely unknown. Here we characterized the functions of two Ecm33 orthologues, i.e., Bbecm33 in Beauveria bassiana and Mrecm33 in Metarhizium robertsii. Bbecm33 and Mrecm33 were both confirmed as GPI-anchored cell wall proteins in immunogold localization. Single-gene disruptions of Bbecm33 and Mrecm33 caused slight growth defects, but conidial yield decreased much more in ΔBbecm33 (76?%) than in ΔMrecm33 (42?%), accompanied with significant reductions of intracellular mannitol and trehalose contents in both mutants and weakened cell walls in ΔBbecm33 only. Consequently, ΔBbecm33 was far more sensitive to the cell wall-perturbating agents Congo red and sodium dodecyl sulfate (SDS) than ΔMrecm33, which showed null response to SDS. Both deletion mutants became significantly more sensitive to two oxidants (menadione and H2O2), two fungicides (carbendazim and ethirimol), osmotic salt NaCl, and Ca2+ during growth despite some degrees of differences in their sensitivities to the chemical stressors. Strikingly, conidial UV-B resistance decreased by 55?% in ΔBbecm33 but was unaffected in ΔMrecm33, unlike a similar decrease (25-8?%) of conidial thermotolerance in both. All the changes were restored to wild-type levels by gene complementation through ectopic gene integration in each fungus. However, neither ΔBbecm33 nor ΔMrecm33 showed a significant change in virulence to a susceptible insect host. Our results indicate that Bbecm33 and Mrecm33 contribute differentially to the conidiation and multi-stress tolerance of B. bassiana and M. robertsii.

© 2004-2018 中国地质图书馆版权所有 京ICP备05064691号 京公网安备11010802017129号

地址:北京市海淀区学院路29号 邮编:100083

电话:办公室:(+86 10)66554848;文献借阅、咨询服务、科技查新:66554700