Hydrophobin genes of the entomopathogenic fungus, Metarhizium brunneum, are diVerentially expressed and corresponding mutants are decreased in virulence

Current Genetics

Volumn 58, Issue 2, 2012, Pages 79-92

  Sevim, Ali ^a,b,c   Donzelli, Bruno G G ^a   Wu, Dongliang ^a   Demirbag, Zihni ^c   Gibson, Donna M ^d   Turgeon, B Gillian ^a  

^a Department of Obstetrics Gynecology   (United States)

^b RECEP TAYYIP ERDOGAN UNIVERSITY   (Turkey)

^c KARADENIZ TECHNICAL UNIVERSITY   (Turkey)

^d ROBERT W HOLLEY CENTER FOR AGRICULTURE AND HEALTH   (United States)

Author keywords

Hydrophobicity; Hydrophobin; Metarhizium anisopliae; Metarhizium brunneum; Virulence

Indexed keywords

HYDROPHOBIN;

ARMYWORM; ARTICLE; BIOTRANSFORMATION; CONIDIUM; CONTROLLED STUDY; DEVELOPMENTAL STAGE; FUNGAL GENE; FUNGAL GENOME; FUNGAL STRAIN; FUNGAL VIRULENCE; FUNGUS GROWTH; FUNGUS MUTANT; GENE DELETION; GENE DUPLICATION; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; HYD2 GENE; HYD3 GENE; HYDROPHOBICITY; HYDROPHOBIN GENE; INSECT; LARVA; METARHIZIUM; METARHIZIUM BRUNNEUM; MORTALITY; NONHUMAN; PHENOTYPE; PIGMENTATION; PRIORITY JOURNAL; RHIZOBIUM RADIOBACTER; SPOROGENESIS; SURFACE PROPERTY; WILD TYPE;

AMINO ACID SEQUENCE; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; METARHIZIUM; MOLECULAR SEQUENCE DATA; MUTATION; PHYLOGENY; PIGMENTATION; SEQUENCE ALIGNMENT; VIRULENCE;

AGROBACTERIUM; FUNGI; HEXAPODA; METARHIZIUM; METARHIZIUM ANISOPLIAE; SPODOPTERA EXIGUA;

EID: 84860274573     PISSN: 01728083     EISSN: 14320983     Source Type: Journal    
DOI: 10.1007/s00294-012-0366-6     Document Type: Article

References (70)

1. An G, Ebert PR, Mitra A, Ha SB (1988) Binary vectors. In: Gelvin SB, Schilperoort RA (eds) Plant molecular biology manual. Kluwer Academic Publishers, Great Britain, pp 1-19
2. Ando A, Harada A, Miura K, Tamai Y (2001) A gene encoding a hydrophobin, fvh1, is specially expressed after the induction of fruiting in the edible mushroom Flammulina velutipes. Curr Genet 39:190-197 (Pubitemid 32492647)
3. Askolin S, Penttila M, Wösten HA, Nakari-Setala T (2005) The Trichoderma reesei hydrophobin genes hfb1 and hfb2 have diverse functions in fungal development. FEMS Microbiol Lett 253:281-288 (Pubitemid 41674527)
4. Bailey MJ, Askolin S, Hörhammer N, Tenkanen M, Linder M, Penttila M, Nakari-Setala T (2002) Process technological eVects of deletion and amplification of hydrophobins I and II in transformants of Trichoderma reesei. Appl Microbiol Biotechnol 58:721-727 (Pubitemid 34493933)
5. Bell-Pedersen D, Dunlap JC, Loros JJ (1992) The Neurospora circadian clock-controlled gene, ccg-2, is allelic to eas and encodes a fungal hydrophobin required for formation of tlie conidial rodlet layer. Genes Dev 6:2382-2394 (Pubitemid 23037403)
6. Bidochka MJ, De Koning J, St Leger RJ (2001) Analysis of a genomic clone of hydrophobin (ssgA) from the entomopathogenic fungus Metarhizium brunneum. Mycol Res 105:360-364 (Pubitemid 32258470)
7. BischoV JF, Rehner SA, Humber RA (2009) A multilocus phylogeny of the Metarhizium anisopliae lineage. Mycologia 101:512-530
8. Boucias DG, Pendland JC, Latge JP (1988) Nonspecific factors involved in the attachment of entomopathogenic deuteromycetes to host insect cuticle. Appl Environ Microbiol 54:1795-1805
9. Castrillo LA, Roberts DW, Vandenberg JD (2005) The fungal past, present, and future: Germination, ramification, and reproduction. J Invertebr Pathol 89:46-56
10. Charnley AB, St Leger RJ (1991) The role of cuticle-degrading enzymes in fungal pathogenesis in insects. In: Hoch HC, Cole GT (eds) The fungal spore and disease initiation in plants and animals. Plenum Press, New York, pp 267-286
11. Cho EM, Kirkland BH, Holder DJ, Keyhani NO (2007) Phage display cDNA cloning and expression analysis of hydrophobins from the entomopathogenic fungus Beauveria (Cordyceps) bassiana. Microbiology 153:3438-3447 (Pubitemid 47629548)
12. Clarkson JM, Charnley AK (1996) New insights into the mechanisms of fungal pathogenesis in insects. Trends Microbiol 4:197-203 (Pubitemid 26163468)
13. Covert SF, Kapoor P, Lee M, Briley A, Nairn CJ (2001) Agrobacterium tumefaciens-mediated transformation of Fusarium circinatum. Mycol Res 105:259-264 (Pubitemid 32258457)
14. Donzelli BGG, Krasnoff SB, Churchill ACL, Vandenberg JD, Gibson DM (2010) Identification of a hybrid PKS-NRPS required for the biosynthesis of NG-391 in Metarhizium robertsii. Curr Genet 56:151-162
15. Donzelli BGG, Krasnoff SB, Sun-Moon Y, Churchill ACL, Gibson DM (2012) Genetic basis of destruxin production in Metarhizium robertsii. Curr Genet. doi:10.1007/s00294-012-0368-4
16. Dublessis S, Sorin C, Voiblet C, Palin B, Martin F, Tagu D (2001) Cloning and expression analysis of a new hydrophobin cDNA from the ectomycorrhizal basidiomycete Pisolithus. Curr Genet 39:335-339 (Pubitemid 32750410)
17. Fang W, Bidochka MJ (2006) Expression of genes involved in germination, conidiogenesis and pathogenesis in Metarhizium brunneum using quantitative real-time RT-PCR. Mycol Res 110:1165-1171 (Pubitemid 44572727)
18. Fang W, Pei Yan, Bidochka MJ (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 (Pubitemid 46605800)
19. Fang W, Pava-Ripoll M, Wang S, St Leger R (2009) Protein kinase A regulates production of virulence determinants by the entomopathogenic fungus, Metarhizium anisopliae. Fungal Gen Biol 46:277-285
20. Fuchs U, Czymmekb KJ, Sweigard JA (2004) Five hydrophobin genes in Fusarium verticillioides include two required for microconidial chain formation. Fungal Gen Biol 41:852-864 (Pubitemid 39043798)
21. Geu-Flores F, Nour-Eldin HH, Nielsen MT, Halkier BA (2007) USER fusion: A rapid and eYcient method for simultaneous fusion and cloning of multiple PCR products. Nucleic Acids Res 35:e55
22. Goettel MS, Eilenberg J, Glare T (2005) Entomopathogenic fungi and their role in regulation of insect populations. In: Gilbert LI, Iatrou K, Gill SS (eds) Comprehensive molecular insect science. Elsevier, Amsterdam, pp 361-405
23. Hajek AE, St Leger RJ (1994) Interactions between fungal pathogens and insect hosts. Annu Rev Entomol 39:293-322
24. Hall TA (1999) BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp 41:95-98
25. Izumitsu K, Kimura S, Kobayashi H, Morita A, Saitoh Y, Tanaka C (2010) Class I hydrophobin BcHpb1 is important for adhesion but not for later infection of Botrytis cinerea. J Gen Plant Pathol 76:254-260
26. Jensen BG, Andersen MR, Pederson MH, Frisvad JC, Sondergaard I (2010) Hydrophobins from Aspergillus species cannot be clearly divided into two classes. BMC Research Notes 3:344
27. Kazmierczak P, Kim DH, Turina M, Van Alfen NK (2005) A hydrophobin of the chestnut blight fungus, Cryphonectria parasitica, is required for stromal pustule eruption. Eukaryot Cell 4:931-936 (Pubitemid 40697757)
28. Kershaw MJ, Talbot NJ (1998) Hydrophobins and repellents: Proteins with fundamental roles in fungal morphogenesis. Fungal Gen Biol 23:18-33 (Pubitemid 28403135)
29. Khetan S (2001) Microbial pest control. Marcel Dekker, New York
30. Klimes A, Dobinson KF (2006) A hydrophobin gene, VDH1, is involved in microsclerotial development and spore viability in the plant pathogen Verticillium dahliae. Fungal Gen Biol 43:283-294
31. Kumar S, Nei M, Dudley J, Tamura K (2008) MEGA: A biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 4:299-306 (Pubitemid 351890826)
32. Kyte J, Doolittle RF (1982) A simple method for displaying the hydrophobic character of a protein. J Mol Biol 157:105-132
33. Li S, Myung K, Guse D, Donkin B, Proctor RH, Grayburn WS, Calvo AM (2006) FvVE1 regulates Wlamentous growth, the ratio of microconidia to macroconidia and cell wall formation in Fusarium verticillioides. Mol Microbiol 62:1418-1432 (Pubitemid 44707203)
34. Linder MB, Szilvay GR, Nakari-Setala T, Penttil ME (2005) Hydrophobins: The protein-amphiphiles of Wlamentous fungi. FEMS Microbiol Rev 29:877-896
35. Mankel A, Krause K, Kothe E (2002) Identification of a hydrophobin gene that is developmentally regulated in the ectomycorrhizal fungus Tricholoma terreum. Appl Environ Microbiol 68:1408-1413 (Pubitemid 34205383)
36. Mikus M, Hatvani L, Neuhof T, Komoj-Zelazowska M, Dieckmann R, Schwecke T, Druzhinina IS, von Döhren H, Kubicek CP (2009) Differential regulation and posttranslational processing of the class II hydrophobin genes from the biocontrol fungus Hypocrea atroviridis. Appl Environ Microbiol 75:3222-3229
37. Moon Y-S, Donzelli BD, Krasnoff SB, McLane H, Griggs MH, Cooke P, Vandenberg JD, Gibson DM, Churchill ACL (2008) Agrobacterium-mediated disruption of a nonribosomal peptide synthetase gene in the invertebrate pathogen Metarhizium anisopliae reveals a peptide spore factor. Appl Environ Microbiol 74:4366-4380 (Pubitemid 352031018)
38. Mosbach A, Leroch M, Mendgen KW, Hahn M (2011) Lack of evidence for a role of hydrophobins in conferring surface hydrophobicity to conidia and hyphae of Botrytis cinerea. BMC Microbiol 11:10
39. Muñoz G, Nakari-Setälä T, Agosin E, Penttilä M (1997) Hydrophobin gene srh1, expressed during sporulation of the biocontrol agent Trichoderma harzianum. Curr Genet 32:225-230 (Pubitemid 27458259)
40. Namiki F, Matsunaga M, Okuda M, Inoue I, Nishi K, Fujita Y, Tsuge T (2001) Mutation of an arginine biosynthesis gene causes reduced pathogenicity in Fusarium oxysporum f. sp. melonis. Mol Plant-Microbe Interact 14:580-584 (Pubitemid 32235591)
41. Ochman H, Gerber AS, Hartl DL (1988) Genetic applications of an inverse polymerase chain reaction. Genetics 120:621-623 (Pubitemid 18260496)
42. Paris S, Debeaupuis JP, Crameri R, Carey M, Charles F, Prevost MC, Schmitt C, Philippe B, Latge JP (2003) Conidial hydrophobins of Aspergillus fumigatus. Appl Environ Microbiol 69:1581-1588 (Pubitemid 36314298)
43. Parta M, Chang Y, Rulong S, Pinto-Dasilva P, Kwon-Chung KJ (1994) HYPI, a hydrophobin gene from Aspergillus fumigatus, complements the rodletless phenotype in Aspergillus nidulans. Infect Immun 62:4389-4395 (Pubitemid 24301968)
44. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning. Cold Spring Harbor Laboratory Press, NY
45. Santos C, Labarère J (1999) Aa-Pri2, a single-copy gene from Agrocybe aegerita, specifically expressed during fruiting initiation, encodes a hydrophobin with a leucine-zipper domain. Curr Genet 35:564-570 (Pubitemid 29299122)
46. Segers GC, Nuss DL (2003) Constitutively activated Ga negatively regulates virulence, reproduction and hydrophobin gene expression in the chestnut blight fungus Cryphonectria parasitica. Fungal Gen Biol 38:198-208 (Pubitemid 36279661)
47. Seidl-Seiboth V, Gruber S, Sezerman U, Schwecke T, Albayrak A, Neuhof T, von Döhren H, Baker SE, Kubicek CP (2011) Novel hydrophobins from Trichoderma define a new hydrophobin subclass: Protein properties, evolution, regulation and processing. J Mol Evol 72:339-351
48. Sevim A, Demir I, Höfte M, Humber RA, Demirbag Z (2010) Isolation and characterization of entomopathogenic fungi from hazelnutgrowing region of Turkey. Biocontrol 55:279-297
49. Shah PA, Pell JK (2003) Entomopathogenic fungi as biological control agents. Appl Microbiol Biotechnol 61:413-423 (Pubitemid 36751000)
50. St Leger RJ (2007) Metarhizium anisopliae as a model for studying bioinsecticidal host pathogen interactions. In: Vurro M, Gressel J (eds) Novel biotechnologies for biocontrol agent enhancement and management. Springer, The Netherlands, pp 179-204
51. St Leger RJ, Wang C (2010) Entomopathogenic fungi and genomics era. In: Stock SP, Vanderberg J, Boemare N, Glazer I (eds) Insect pathogens: Molecular approaches and techniques. Massachusetts, USA, pp 365-395
52. St Leger RJ, Frank DC, Roberts DW, Staples RC (1992a) Molecular cloning and regulatory analysis of the cuticle-degrading proteasestructural gene from entomopathogenic fungus Metarhizium anisopliae. Eur J Biochem 204:991-1001
53. St Leger RJ, Staples RC, Roberts DW (1992b) Cloning and regulatory analysis of starvation-stress gene, ssgA, encoding a hydrophobinlike protein from the entomopathogenic fungus, Metarhizium anisopliae. Gene 120:119-124
54. St Leger RJ, Joshi L, Bidochka MJ, Roberts DW (1996) Construction of an improved mycoinsecticide overexpressing a toxic protease. Proc Natl Acad Sci USA 93:6349-6354 (Pubitemid 26230308)
55. Stevens R (1974) Mycology guidebook. University of Washington Press, Seattle
56. Szilvay GR (2007) Self-assembly of hydrophobin proteins from the fungus Trichoderma reesei. Dissertation, University of Helsinki
57. Talbot NJ, Ebbole DJ, Liamera JE (1993) Identification and characterization of MPGI, a gene involved in pathogenicity from the rice blast fungus Magnaporthe grisea. Plant Cell 5:1575-1590 (Pubitemid 2021805)
58. Talbot NJ, Kershaw MJ, Wakley GE, De Vries O, Wessels J, Hamer JE (1996) MPG1 encodes a fungal hydrophobin involved in surface interactions during infection-related development of Magnaporthe grisea. Plant Cell 8:985-999 (Pubitemid 26329826)
59. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596-1599 (Pubitemid 47236692)
60. Thau N, Monod M, Crestani B, Rolland C, Tronchin G, Latgi JP, Paris S (1994) Rodletless mutants of Aspergillus fumigatus. Infect Immun 62:4380-4388 (Pubitemid 24301967)
61. Trembley ML, Ringli C, Honegger R (2002) Differential expression of hydrophobins DGH1, DGH2 and DGH3 and immunolocalization of DGH1 in strata of the lichenized basidiocarp of Dictyonema glabratum. New Phytol 154:175-184
62. Van Wetter MA, Schuren FHJ, Schuurs TA, Wessels JGH (1996) Targeted mutation of the SC3 hydrophobin gene of Schizophyllum commune affects formation of aerial hyphae. FEMS Microbiol Lett 140:265-269 (Pubitemid 26228637)
63. Vries OMH, Moore S, Arntz C, Wessels JGH, Tudzynski P (1999) Identification and characterization of a tri-partite hydrophobin from Claviceps fusiformis; a novel type of class II hydrophobin. Eur J Biochem 262:377-385 (Pubitemid 29266049)
64. Whiteford JR, Spanu PD (2001) The hydrophobin HCF-1 of Cladosporium fulvum is required for eYcient water-mediated dispersal of conidia. Fungal Gen Biol 32:159-168 (Pubitemid 34229821)
65. Wösten HAB (2001) Hydrophobins: Multipurpose proteins. Annu Rev Microbiol 55:625-646 (Pubitemid 32978118)
66. Wösten HAB, Wessels JGH (1997) Hydrophobins, from molecular structure to multiple functions in fungal development. Mycoscience 38:363-374
67. Wösten HAB, Schuren FHJ, Wessels JGH (1994) Interfacial selfassembly of a hydrophobin into an amphipathic membrane mediates fungal attachment to hydrophobic surfaces. EMBO J 13:5848-5854
68. Ypsilos IK, Magan N (2004) Impact of water-stress and washing treatments on production, synthesis and retention of endogenous sugar alcohols and germinability of Metarhizium anisopliae blastospores. Mycol Res 108:1337-1345 (Pubitemid 39554202)
69. Zhang S, Xia YX, Kim B, Keyhani NO (2011) Two hydrophobins are involved in fungal spore coat rodlet layer assembly and each play distinct roles in surface interactions, development and pathogenesis in the entomopathogenic fungus, Beauveria bassiana. Mol Micro 80:811-826
70. Zimmermann G (1993) The entomopathogenic fungus Metarhizium anisopliae and its potential as a biocontrol agent. Pestic Sci 37:375-379 (Pubitemid 24413161)