Novel hydrophobins from trichoderma define a new hydrophobin subclass: Protein properties, evolution, regulation and processing

Journal of Molecular Evolution

Volumn 72, Issue 4, 2011, Pages 339-351

  Seidl Seiboth, Verena ^a   Gruber, Sabine ^a   Sezerman, Ugur ^b   Schwecke, Torsten ^c,d   Albayrak, Aydin ^b   Neuhof, Torsten ^c   Von Döhren, Hans ^d   Baker, Scott E ^e   Kubicek, Christian P ^a  

^a VIENNA UNIVERSITY OF TECHNOLOGY   (Austria)

^b SABANCI UNIVERSITY   (Turkey)

^c AnagnosTec Gesellschaft fur Analytische Biochemie & Diagnostik mbH   (Germany)

^d TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

^e PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

Author keywords

Hydrophobin; Hypocrea; Peptidomics; Protein evolution; Protein processing; Splicing; Trichoderma

Indexed keywords

CYSTEINE; FUNGAL PROTEIN; GLUCOSE;

AMINO ACID SEQUENCE; ARTICLE; ASCOMYCETES; CHEMISTRY; CLASSIFICATION; GENETICS; HYPOCREA; MASS SPECTROMETRY; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PHYLOGENY; PROTEIN PROCESSING; SEQUENCE ALIGNMENT; SOLUBILITY; TRICHODERMA;

AMINO ACID SEQUENCE; ASCOMYCOTA; CYSTEINE; EVOLUTION, MOLECULAR; FUNGAL PROTEINS; GLUCOSE; HYPOCREA; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN SPLICING; SEQUENCE ALIGNMENT; SOLUBILITY; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TRICHODERMA;

ASCOMYCOTA; BASIDIOMYCOTA; FUNGI; HYPOCREA; TRICHODERMA; TRICHODERMA ATROVIRIDE;

EID: 79958231350     PISSN: 00222844     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00239-011-9438-3     Document Type: Article

References (48)

1. Albayrak A, Otu HH, Sezerman UO (2010) Clustering of protein families into functional subtypes using Relative Complexity Measure with reduced amino acid alphabets. BMC Bioinform 11:428
2. P Albuquerque CM Kyaw RR Saldanha MM Brigido MS Felipe I Silva-Pereira 2004 Pbhyd1 and Pbhyd2: two mycelium-specific hydrophobin genes from the dimorphic fungus Paracoccidioides brasiliensis Fungal Genet Biol 41 510 520 15050540 10.1016/j.fgb.2004.01.001 1:CAS:528:DC%2BD2cXis1Wgsbg%3D (Pubitemid 38429774)
3. DB Archer JF Peberdy 1997 The molecular biology of secreted enzyme production by fungi Crit Rev Biotechnol 17 273 306 9397531 10.3109/ 07388559709146616 1:CAS:528:DyaK2sXotVCku78%3D (Pubitemid 127716529)
4. T Benitez AM Rincon MC Limon AC Codon 2004 Biocontrol mechanisms of Trichoderma strains Int Microbiol 7 249 260 15666245 1:CAS:528: DC%2BD2MXhs1Cjtb8%3D (Pubitemid 43126708)
5. MT Cheah A Wachter N Sudarsan RR Breaker 2007 Control of alternative RNA splicing and gene expression by eukaryotic riboswitches Nature 447 497 500 17468745 10.1038/nature05769 1:CAS:528:DC%2BD2sXlsFOhu7k%3D (Pubitemid 46816734)
6. P Chomczynski N Sacchi 1987 Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction Anal Biochem 162 156 159 2440339 10.1016/0003-2697(87)90021-2 1:CAS:528:DyaL2sXitFSns7Y%3D (Pubitemid 17064313)
7. ML de Vocht K Scholtmeijer EW van der Vegte OM de Vries N Sonveaux HA Wosten JM Ruysschaert G Hadziloannou JG Wessels GT Robillard 1998 Structural characterization of the hydrophobin SC3, as a monomer and after self-assembly at hydrophobic/hydrophilic interfaces Biophys J 74 2059 2068 9545064 10.1016/S0006-3495(98)77912-3 (Pubitemid 28157940)
8. IS Druzhinina AG Kopchinskiy CP Kubicek 2006 The first 100 Trichoderma species characterized by molecular data Mycoscience 47 55 64 10.1007/s10267-006-0279-7 1:CAS:528:DC%2BD28XntFensLc%3D
9. O Emanuelsson S Brunak G von Heijne H Nielsen 2007 Locating proteins in the cell using TargetP, SignalP and related tools Nat Protoc 2 953 971 17446895 10.1038/nprot.2007.131 1:CAS:528:DC%2BD2sXhtFGnur%2FF (Pubitemid 46745592)
10. C Etchebest C Benros A Bornot AC Camproux AG de Brevern 2007 A reduced amino acid alphabet for understanding and designing protein adaptation to mutation Eur Biophys J 36 1059 1069 17565494 10.1007/s00249-007-0188-5 1:CAS:528:DC%2BD2sXht1CnsLfP (Pubitemid 350045038)
11. J Felsenstein 1989 PHYLIP (Phylogeny Inference Package) Cladistics 5 164 166
12. AS Fiser A Sali 2003 MODELLER: generation and refinement of homology-based protein structure models Methods Enzymol 374 461 491 14696385 10.1016/S0076-6879(03)74020-8 1:CAS:528:DC%2BD2cXotlyntA%3D%3D (Pubitemid 37531821)
13. Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Barioch A (2005) Protein identification and analysis tools on the ExPASy server. In: Walker JM (ed) The proteomics protocols handbook. Humana Press, Totowa, NJ, pp 571-607
14. GE Harman R Petzold A Comis J Chen 2004 Interactions between Trichoderma harzianum strain T22 and maize inbred line Mo17 and effects of these interactions on diseases caused by Pythium ultimum and Colletotrichum graminicola Phytopathology 94 147 153 18943537 10.1094/PHYTO.2004.94.2.147 (Pubitemid 38504026)
15. HJ Hektor K Scholtmeijer 2005 Hydrophobins: proteins with potential Curr Opin Biotechnol 16 434 439 15950452 10.1016/j.copbio.2005.05.004 1:CAS:528:DC%2BD2MXntVCqtb0%3D (Pubitemid 41111530)
16. M Komoń-Zelazowska J Bissett D Zafari L Hatvani L Manczinger S Woo M Lorito L Kredics CP Kubicek IS Druzhinina 2007 Genetically closely related but phenotypically divergent Trichoderma species cause green mold disease in oyster mushroom farms worldwide Appl Environ Microbiol 73 7415 7426 17827333 10.1128/AEM.01059-07 (Pubitemid 350196695)
17. CP Kubicek S Baker C Gamauf CM Kenerley IS Druzhinina 2008 Purifying selection and birth-and-death evolution in the class II hydrophobin gene families of the ascomycete Trichoderma/Hypocrea BMC Evol Biol 8 4 18186925 10.1186/1471-2148-8-4 (Pubitemid 351295159)
18. AH Kwan RD Winefield M Sunde JM Matthews RG Haverkamp MD Templeton JP Mackay 2006 Structural basis for rodlet assembly in fungal hydrophobins Proc Natl Acad Sci USA 103 3621 3626 16537446 10.1073/pnas.0505704103 1:CAS:528:DC%2BD28XivFWju78%3D (Pubitemid 43376605)
19. MB Linder GR Szilvay T Nakari-Setälä ME Penttilä 2005 Hydrophobins: the protein-amphiphiles of filamentous fungi FEMS Microbiol Rev 29 877 896 16219510 10.1016/j.femsre.2005.01.004 1:CAS:528:DC%2BD2MXhtFSisLjL (Pubitemid 41416842)
20. LG Lugones HA Wosten JG Wessels 1998 A hydrophobin (ABH3) specifically secreted by vegetatively growing hyphae of Agaricus bisporus (common white button mushroom) Microbiology 144 Pt 8 2345 2353 9720057 10.1099/00221287-144-8- 2345 1:CAS:528:DyaK1cXlsFyjtLg%3D (Pubitemid 28403048)
21. LJ McGuffin K Bryson DT Jones 2000 The PSIPRED protein structure prediction server Bioinformatics 16 404 405 10869041 10.1093/bioinformatics/16. 4.404 1:CAS:528:DC%2BD3cXltFOksrw%3D (Pubitemid 30417087)
22. M Mikus L Hatvani T Neuhof M Komon-Zelazowska R Dieckmann T Schwecke IS Druzhinina H von Dohren CP Kubicek 2009 Differential regulation and posttranslational processing of the class II hydrophobin genes from the biocontrol fungus Hypocrea atroviridis Appl Environ Microbiol 75 3222 3229 19329667 10.1128/AEM.01764-08 1:CAS:528:DC%2BD1MXmsFWisbg%3D
23. LR Murphy A Wallqvist RM Levy 2000 Simplified amino acid alphabets for protein fold recognition and implications for folding Protein Eng 13 149 152 10775656 10.1093/protein/13.3.149 1:CAS:528:DC%2BD3cXjtlKmtbY%3D (Pubitemid 30237589)
24. Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York
25. M Nei AP Rooney 2005 Concerted and birth-and-death evolution of multigene families Annu Rev Genet 39 121 152 16285855 10.1146/annurev.genet.39.073003. 112240 1:CAS:528:DC%2BD28Xlt1Wktw%3D%3D (Pubitemid 43011110)
26. M Nei X Gu T Sitnikova 1997 Evolution by the birth-and-death process in multigene families of the vertebrate immune system Proc Natl Acad Sci USA 94 7799 7806 9223266 10.1073/pnas.94.15.7799 1:CAS:528:DyaK2sXksl2nsbg%3D (Pubitemid 27343728)
27. T Neuhof R Dieckmann IS Druzhinina CP Kubicek T Nakari-Setälä M Penttilä H von Döhren 2007 Direct identification of hydrophobins and their processing in Trichoderma using intact-cell MALDI-TOF MS FEBS J 274 841 852 17288563 10.1111/j.1742-4658.2007.05636.x 1:CAS:528:DC%2BD2sXitVOhur4%3D (Pubitemid 46144043)
28. A Nicholls B Honig 1990 A rapid finite difference algorithm, utilizing successive over-relaxation to solve the Poisson-Bolzmann equation J Comput Chem 12 435 445 10.1002/jcc.540120405
29. HH Otu K Sayood 2003 A new sequence distance measure for phylogenetic tree construction Bioinformatics 19 2122 2130 14594718 10.1093/bioinformatics/ btg295 1:CAS:528:DC%2BD3sXovVeksrw%3D (Pubitemid 37408164)
30. JA Pleiss GB Whitworth M Bergkessel C Guthrie 2007 Rapid, transcript-specific changes in splicing in response to environmental stress Mol Cell 27 928 937 17889666 10.1016/j.molcel.2007.07.018 1:CAS:528: DC%2BD2sXhtFahtr%2FJ (Pubitemid 47489768)
31. B Rajashekar P Samson T Johansson A Tunlid 2007 Evolution of nucleotide sequences and expression patterns of hydrophobin genes in the ectomycorrhizal fungus Paxillus involutus New Phytol 174 399 411 17388902 10.1111/j.1469-8137. 2007.02022.x 1:CAS:528:DC%2BD2sXls12lur4%3D (Pubitemid 46457393)
32. J Rozas JC Sanchez-DelBarrio X Messeguer R Rozas 2003 DnaSP, DNA polymorphism analyses by the coalescent and other methods Bioinformatics 19 2496 2497 14668244 10.1093/bioinformatics/btg359 1:CAS:528:DC%2BD3sXpvVSisLo%3D (Pubitemid 38016658)
33. N Saitou M Nei 1987 The neighbor-joining method: a new method for reconstructing phylogenetic trees Mol Biol Evol 4 406 425 3447015 1:STN:280:DyaL1c7ovFSjsA%3D%3D
34. K Scholtmeijer MI Janssen MB van Leeuwen TG van Kooten H Hektor HA Wösten 2004 The use of hydrophobins to functionalize surfaces Biomed Mater Eng 14 447 454 15472393 1:STN:280:DC%2BD2crgtlSrsw%3D%3D (Pubitemid 40916716)
35. V Seidl B Seiboth L Karaffa CP Kubicek 2004 The fungal STRE-element-binding protein Seb1 is involved but not essential for glycerol dehydrogenase (gld1) gene expression and glycerol accumulation in Trichoderma atroviride during osmotic stress Fungal Genet Biol 41 1132 1140 15531216 10.1016/j.fgb.2004.09.002 1:CAS:528:DC%2BD2cXpsVOktb8%3D (Pubitemid 39516941)
36. V Seidl B Huemer B Seiboth CP Kubicek 2005 A complete survey of Trichoderma chitinases reveals three distinct subgroups of family 18 chitinases FEBS J 272 5923 5939 16279955 10.1111/j.1742-4658.2005.04994.x 1:CAS:528:DC%2BD2MXht1Kgu7rF (Pubitemid 41689363)
37. V Seidl M Schmoll B Scherm V Balmas B Seiboth Q Migheli CP Kubicek 2006 Antagonism of Pythium blight of zucchini by Hypocrea jecorina does not require cellulase gene expression but is improved by carbon catabolite derepression FEMS Microbiol Lett 257 145 151 16553845 10.1111/j.1574-6968.2006.00157.x 1:CAS:528:DC%2BD28Xjslyksbc%3D
38. MA Stringer RA Dean TC Sewall WE Timberlake 1991 Rodletless, a new Aspergillus developmental mutant induced by directed gene inactivation Genes Dev 5 1161 1171 2065971 10.1101/gad.5.7.1161 1:CAS:528:DyaK38XhtVSgu7s%3D (Pubitemid 21906027)
39. M Sunde AH Kwan MD Templeton RE Beever JP Mackay 2008 Structural analysis of hydrophobins Micron 39 773 784 17875392 10.1016/j.micron.2007.08.003 1:CAS:528:DC%2BD1cXps1Wgt78%3D
40. F Tajima M Nei 1984 Estimation of evolutionary distance between nucleotide sequences Mol Biol Evol 1 269 285 6599968 1:CAS:528: DyaL2MXhvF2kt7c%3D (Pubitemid 15218644)
41. NJ Talbot 1999 Fungal biology. Coming up for air and sporulation Nature 398 295 296 10192329 10.1038/18575 1:CAS:528:DyaK1MXitlCntb4%3D (Pubitemid 29161672)
42. K Tamura J Dudley M Nei S Kumar 2007 MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0 Mol Biol Evol 24 1596 1599 17488738 10.1093/molbev/msm092 1:CAS:528:DC%2BD2sXpsVGrsL8%3D (Pubitemid 47236692)
43. P Vargovic R Pokorny U Holker M Hofer L Varecka 2006 Light accelerates the splicing of srh1 homologue gene transcripts in aerial mycelia of Trichoderma viride FEMS Microbiol Lett 254 240 244 16445751 10.1111/j.1574-6968.2005.00047. x 1:CAS:528:DC%2BD28XhsFWrsr8%3D
44. A Viterbo I Chet 2006 TasHyd1, a new hydrophobin gene from the biocontrol agent Trichoderma asperellum, is involved in plant root colonization Mol Plant Pathol 7 249 258 20507444 10.1111/j.1364-3703.2006.00335.x 1:CAS:528: DC%2BD28XoslWks7k%3D (Pubitemid 43926830)
45. JA Vizcaino J Redondo MB Suarez RE Cardoza R Hermosa FJ Gonzalez M Rey E Monte 2007 Generation, annotation, and analysis of ESTs from four different Trichoderma strains grown under conditions related to biocontrol Appl Microbiol Biotechnol 75 853 862 17333173 10.1007/s00253-007-0885-0 1:CAS:528: DC%2BD2sXlslClurY%3D (Pubitemid 47164903)
46. JG Wessels 1999 Fungi in their own right Fungal Genet Biol 27 134 145 10441439 10.1006/fgbi.1999.1125 1:STN:280:DyaK1MzntlCltw%3D%3D (Pubitemid 29412835)
47. JR Whiteford PD Spanu 2002 Hydrophobins and the interaction between fungi and plants Mol Plant Pathol 3 391 400 20569345 10.1046/j.1364-3703.2002.00129.x 1:CAS:528:DC%2BD38XotVSlsL0%3D
48. BT Wilhelm S Marguerat S Watt F Schubert V Wood I Goodhead CJ Penkett J Rogers J Bähler 2008 Dynamic repertoire of a eukaryotic transcriptome surveyed at single-nucleotide resolution Nature 453 1239 1243 18488015 10.1038/nature07002 1:CAS:528:DC%2BD1cXnslGksLs%3D (Pubitemid 351913597)