Purifying selection and birth-and-death evolution in the class II hydrophobin gene families of the ascomycete Trichoderma/Hypocrea
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- 作者：Christian P Kubicek (1)
Scott Baker (2)
Christian Gamauf (1)
Charles M Kenerley (3)
Irina S Druzhinina (1) - 刊名：BMC Evolutionary Biology
- 出版年：2008
- 出版时间：December 2008
- 年：2008
- 卷：8
- 期：1
- 全文大小：1998KB
- 参考文献：1. Wessels JG: Fungi in their own right. / Fungal Genet Biol 1999, 27: 134-45. CrossRef
2. Talbot NJ: Fungal biology. Coming up for air and sporulation. / Nature 1999, 398: 295-96. CrossRef
3. Linder MB, Szilvay GR, Nakari–Setala T, Penttila ME: Hydrophobins: the protein–amphiphiles of filamentous fungi. / FEMS Microbiol Rev 2005, 29: 877-96. CrossRef
4. W?sten HA: Hydrophobins: multipurpose proteins. / Annu Rev Microbiol 2001, 55: 625-46. CrossRef
5. Hakanpaa J, Paananen A, Askolin S, Nakari–Setala T, Parkkinen T, Penttila ME, Linder MB, Rouvinen J: Atomic resolution structure of the HFBII hydrophobin, a self–assembling amphiphile. / J Biol Chem 2004, 279: 534-39. CrossRef
6. Hakanpaa J, Szilvay GR, Kaljunen H, Maksimainen M, Linder M, Rouvinen J: Two crystal structures of Trichoderma reesei hydrophobin HFBI -the structure of a protein amphiphile with and without detergent interaction. / Protein Sci 2006, 15: 2129-140. CrossRef
7. Elliot MA, Talbot NJ: Building filaments in the air: aerial morphogenesis in bacteria and fungi. / Curr Opin Microbiol 2004, 7: 594-01. CrossRef
8. Tucker S, Talbot NJ: Surface attachment and pre–penetration stage development by plant pathogenic fungi. / Annu Rev Phytopathol 2001, 39: 385-17. CrossRef
9. Klimes A, Dobinson KF: A hydrophobin gene, VDH1, is involved in microsclerotial development and spore viability in the plant pathogen Verticillium dahliae . / Fungal Genet Biol 2006, 43: 283-94. CrossRef
10. Sakamoto Y, Ando A, Tamai Y, Yajima T: Pileus differentiation and pileus–specific protein expression in Flammulina velutipes . / Fungal Genet Biol 2007, 44: 14-4. CrossRef
11. Kwan AH, Winefield RD, Sunde M, Matthews JM, Haverkamp RG, Templeton MD, Mackay JP: Structural basis for rodlet assembly in fungal hydrophobins. / Proc Natl Acad Sci USA 2004, 103: 3621-626. CrossRef
12. Zhang J, Rosenberg HF, Nei M: Positive Darwinian selection after gene duplication in primate ribonuclease genes. / Proc Natl Acad Sci USA 1998, 95: 3708-713. CrossRef
13. Weber E, K?bnik R: Positive selection of the Hrp pilin HrpE of the plant pathogen Xanthomonas . / J Bacteriol 2006, 188: 1405-410. CrossRef
14. Benderoth M, Textor AJ, Windsor T, Mitchell–Olds J, Gershenzon J, Kroymann J: Positive selection driving diversification in plant secondary metabolism. / Annu Rev Phytopathol 2006, 44: 469-87. CrossRef
15. Brown NF, Wickham ME, Coombes BK, Finlay BB: Crossing the line: selection and evolution of virulence traits. / PLoS Patho 2006, 2: e42. Review. CrossRef
16. De Mita S, Santoni S, Hochu I, Ronfort J, Bataillon T: Molecular evolution and positive selection of the symbiotic gene NORK in Medicago truncatula . / J Mol Evol 2006, 62: 234-44. CrossRef
17. Haraguchi Y, Sasaki A: Host–parasite arms race in mutation modifications: indefinite escalation despite a heavy load? / J Theor Biol 1996, 183: 121-37. CrossRef
18. Nei M, Hughes AL: Balanced polymorphism and evolution by the birth–and–death process in the MHC loci. / HLA 1991. Proc 11th Histocompatibility Workshop and Conference / (Edited by: Tsuji K, Aizawa M, Sasazuli T). Oxford University Press 2: 27-8.
19. Ota T, Nei M: Divergent evolution and evolution by the birth–and–death process in the immunoglobulin VH gene family. / Mol Biol Evol 1994, 15: 469-82.
20. Nei M, Gu X, Sitnikova T: Evolution by a birth–and–death process in multigene families of the vertebrate immune system. / Proc Natl Acad Sci USA 1997, 94: 7799-806. CrossRef
21. Nei M, Rogozin IB, Piontkivska H: Purifying selection and birth–and–death evolution in the ubiquitin gene family. / Proc Natl Acad Sci USA 2000, 97: 10866-0871. CrossRef
22. Nei M, Rooney AP: Concerted and birth–and–death evolution of multigene families. / Annu Rev Genet 2005, 39: 121-52. CrossRef
23. Jiang RH, Tyler BM, Whisson SC, Hardham AR, Govers F: Ancient origin of elicitin gene clusters in Phytophthora genomes. / Mol Biol Evol 2006, 23: 338-51. CrossRef
24. Loria R, Kers J, Joshi M: Evolution of plant pathogenicity in Streptomyces . / Proc Natl Acad Sci USA 2006, 103: 9118-123. CrossRef
25. Klein D, Eveleigh DE: Ecology of Trichoderma . / Trichoderma and Gliocladium. Basic biology, taxonomy and genetics / (Edited by: Kubicek CP, Harman GE). Taylor & Francis Ltd, London, U 1998, 1: 57-4.
26. Harman GE, Howell CR, Viterbo A, Chet I, Lorito M: Trichoderma species -opportunistic, avirulent plant symbionts. / Nature Rev Microbiol 2004, 2: 43-6. CrossRef
27. Hjeljord L, Tronsmo A: Trichoderma and Gliocladium in biological control: an overview. / Trichoderma and Gliocladium. Enzymes, Biological Control and Commercial Applications / (Edited by: Harman GE, Kubicek CP). Taylor and Francis, London 1998, 2: 131-51.
28. Munoz G, Nakari–Setala T, Agosin E, Penttila ME: Hydrophobin gene srh1 , expressed during sporulation of the biocontrol agent Trichoderma harzianum . / Curr Genet 1997, 32: 225-30. CrossRef
29. Vizcaino JA, Gonzalez JF, Suarez MB, Redondo J, Heinrich J, Delgado–Jarana J, Hermosa R, Gutierrez S, Monte E, Llobell A, Rey M: Generation, annotation and analysis of ESTs from Trichoderma harzianum CECT 2413. / BMC Genomics 2006, 27;7: 193. CrossRef
30. Vizcaino JA, Redondo J, Suarez MB, Cardoza RE, Hermosa R, Gonzalez FJ, Rey M, Monte E: Generation, annotation, and analysis of ESTs from four different Trichoderma strains grown under conditions related to biocontrol. / Appl Microbiol Biotechnol 2007, 75: 853-62. CrossRef
31. Askolin S, Penttila ME, W?sten HA, Nakari–Setala T: The Trichoderma reesei hydrophobin genes hfb1 and hfb2 have diverse functions in fungal development. / FEMS Microbiol Letts 2005, 253: 281-88. CrossRef
32. Askolin S, Linder M, Scholtmeijer K, Tenkanen M, Penttila M, de Vocht ML, Wosten HA: Interaction and comparison of a class I hydrophobin from Schizophyllum commune and class II hydrophobins from Trichoderma reesei . / Biomacromolecules 2006, 7: 1295-301. CrossRef
33. Viterbo A, Chet I: TasHyd1, anew hydrophobin gene from the biocontrol agent Trichoderma asperellum , is involved in plant root colonization. / Mol Plant Pathol 2006, 7: 249-58. CrossRef
34. van Wetter MA, Wosten HA, Wessels JG: SC3 and SC4 hydrophobins have distinct roles in formation of aerial structures in dikaryons of Schizophyllum commune . / Mol Microbiol 2000, 36: 201-10. CrossRef
35. Kershaw MJ, Wakley G, Talbot NJ: Complementation of the mpg1 mutant phenotype in Magnaporthe grisea reveals functional relationships between fungal hydrophobins. / EMBO J 1998, 17: 3838-849. CrossRef
36. Lora JM, de la Cruz J, Benitez T, Llobell A, Pintor–Toro JH: A putative carbon catabolite repressed cell wall protein from the mycoparasitic fungus Trichoderma harzianum . / Mol Gen Genet 1994, 242: 461-66. CrossRef
37. Kullnig C, Krupica T, Woo SL, Mach RL, Rey M, Benitez T, Lorito M, Kubicek CP: Confusion abounds over identities of Trichoderma biocontrol isolates. / Mycol Res 2001, 105: 770-72. CrossRef
38. The TrichoEST database [trichoderma.org" class="a-plus-plus">http://www.trichoderma.org]
39. Bandelt HJ, Dress AW: Split decomposition: a new and useful approach to phylogenetic analysis of distance data. / Mol Phylogenet Evol 1992, 1: 242-52. CrossRef
40. Huson DH: SplitsTree: a program for analyzing and visualizing evolutionary data. / Bioinformatics 1998, 14: 68-3. CrossRef
41. Nei M, Gojobori T: Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. / Mol Biol Evol 1986, 3: 418-26.
42. Seidl V, Huemer B, Seiboth B, Kubicek CP: A complete survey of Trichoderma chitinases reveals a new family 18 subgroup. / The FEBS J 2005, 272: 5923-939. CrossRef
43. Rajashekar B, Samson P, Johansson T, Tunlid A: Evolution of nucleotide sequences and expression patterns of hydrophobin genes in the ectomycorrhizal fungus Paxillus involutus . / New Phytol 2007, 174: 399-11. CrossRef
44. Neuhof T, Dieckmann R, Druzhinina IS, Kubicek CP, Nakari–Setala T, Penttil? M, von D?hren H: Direct identification of hydrophobins and their processing in Trichoderma using intact–cell MALDI–TOF MS. / FEBS J 2007, 274: 841-52. CrossRef
45. Teertstra WR, Deelstra HJ, Vranes M, Bohlmann R, Kahmann R, K?mper J, W?sten HA: Repellents have functionally replaced hydrophobins in mediating attachment to a hydrophobic surface and in formation of hydrophobic aerial hyphae in Ustilago maydis . / Microbiology 2006, 152: 3607-2. CrossRef
46. Lora JM, Pintor–Toro JA, Benitez T, Romero LC: Qid3 protein links plant bimodular proteins with fungal hydrophobins. / Mol Microbiol 1995, 18: 380-82. CrossRef
47. Coupe SA, Taylor JE, Isaac PG, Roberts JA: Identification and characterization of a proline–rich mRNA that accumulates during pod development in oilseed rape ( Brassica napus L.). / Plant Mol Biol 1993, 23: 1223-232. CrossRef
48. Castonguay Y, Laberge S, Nadeau P, Vezina LP: A cold–induced gene from Medicago sativa encodes a bimodular protein similar to developmentally regulated proteins. / Plant Mol Biol 1994, 24: 799-04. CrossRef
49. He CY, Zhang JS, Chen SY: A soybean gene encoding a proline–rich protein is regulated by salicylic acid, an endogenous circadian rhythm and by various stresses. / Theor Appl Genet 2002, 104: 1125-131. CrossRef
50. Arntz C, Tudzynski P: Identification of genes induced in alkaloid–producing cultures of Claviceps sp. / Curr Genet 1997, 31: 357-60. CrossRef
51. De Vries OM, Moore S, Arntz C, Wessels JG, Tudzynski P: Identification and characterization of a tri–partite hydrophobin from Claviceps fusiformis . A novel type of class II hydrophobin. / Eur J Biochem 1999, 262: 377-85. CrossRef
52. Fierro F, Garcia–Estrada C, Castillo NI, Rodriguez R, Velasco–Conde T, Martin JF: Transcriptional and bioinformatic analysis of the 56.8 kb DNA region amplified in tandem repeats containing the penicillin gene cluster in Penicillium chrysogenum . / Fungal Genet Biol 2006, 43: 618-9. CrossRef
53. Kong H, Landherr LL, Fr?hlich MW, Leebens–Mack J, Ma H, Depamphilis CW: Patterns of gene duplication in the plant SKP1 gene family in angiosperms: evidence for multiple mechanisms of rapid gene birth. / Plant J, / in press. 2007, Apr 23
54. Lynch M, Conery JS: The evolutionary fate and consequences of duplicate genes. / Science 2001, 290: 1151-155. CrossRef
55. Kajava AV, Baxa U, Wickner RB, Steven AC: A model for Ure2p prion filaments and other amyloids: the parallel superpleated beta–structure. / Proc Natl Acad Sci USA 2004, 101: 7885-890. CrossRef
56. Wosten HA, de Vocht ML: Hydrophobins, the fungal coat unravelled. / Biochim Biophys Acta 2000, 1469: 79-6.
57. Butko P, Buford JP, Goodwin JS, Stroud PA, McCormick CL, Cannon GC: Spectroscopic evidence for amyloid–like interfacial self–assembly of hydrophobin Sc3. / Biochem Biophys Res Comm 2001, 280: 212-15. CrossRef
58. Mackay JP, Matthews JM, Winefield RD, Mackay LG, Haverkamp RG, Templeton MD: The hydrophobin EAS is largely unstructured in solution and functions by forming amyloid–like structures. / Structure 2001, 9: 83-1. CrossRef
59. Hektor HJ, Scholtmeijer K: Hydrophobins: proteins with potential. / Curr Opin Biotechnol 2005, 16: 434-39. CrossRef
60. Scholtmeijer K, Janssen MI, Gerssen B, de Vocht ML, van Leeuwen BM, van Kooten TG, W?sten HA, Wessels JG: Surface modifications created by using engineered hydrophobins. / Appl Environ Microbiol 2002, 68: 1367-373. CrossRef
61. Scholtmeijer K, Janssen MI, van Leeuwen MB, van Kooten TG, Hektor H, W?sten HA: The use of hydrophobins to functionalize surfaces. / Biomed Mater Engin 2004, 14: 447-54.
62. Chomczynski P, Sacchi N: Single–step method of RNA isolation by acid guanidinium thiocyanate–phenol–chloroform extraction. / Anal Biochem 1987, 162: 156-59. CrossRef
63. Nakari T, Alatalo E, Penttila ME: Isolation of Trichoderma reesei genes highly expressed on glucose–containing media: characterization of the tef1 gene encoding translation elongation factor 1 alpha. / Gene 1993, 136: 313-18. CrossRef
64. DOE Joint Genome Institute [http://genome.jgi-psf.org/Necha2/Necha2.home.html] / The Nectria cinnabarina genome database v 1.0 2006.
65. DOE Joint genome Institute [http://genome.jgi-psf.org/Mycgr1/Mycgr1.home.html] / The Mycophaerella graminicola genome database v 1.0 2007.
66. Broad Institute and Syngenta AG [http://www.broad.mit.edu/annotation/genome/botrytis_cinerea/Home.html] / The Botrytis cinerea assembly 2006.
67. Nicholas KB, Nicholas HB Jr: Genedoc: a tool for editing and annotating multiple sequence alignments. [http://www.psc.edu/biomed/genedoc] 1997.
68. Saitou N, Saitou M: The neighbor–joining method: a new method for reconstructing phylogenetic trees. / Mol Biol Evol 1987, 4: 406-25.
69. Kumar S, Tamura K, Nei M: MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. / Brief Bioinform 2004, 5: 150-3. CrossRef
70. McGuire G, Wright F: TOPAL 2.0: improved detection of mosaic sequences within multiple alignments. / Bioinformatics 2000, 16: 130-34. CrossRef
71. Milne I, Wright F, Rowe G, Marshall DF, Husmeier D, McGuire G: TOPALi: software for automatic identification of recombinant sequences within DNA multiple alignments. / Bioinformatics 2004, 20: 1806-807. CrossRef
72. Kimura M: Estimation of evolutionary distances between homologous nucleotide distances. / Proc Natl Acad Sci USA 1981, 78: 454-58. CrossRef
73. Tajima F, Nei M: Estimation of evolutionary distance between nucleotide sequences. / Mol Biol Evol 1984, 1: 269-85.
74. Rozas J, Sanchez–DelBarrio JC, Messeguer X, Rozas R: DnaSP, DNA polymorphism analyses by the coalescent and other methods. / Bioinformatics 2003, 19: 2496-497. CrossRef
75. Kupfer DM, Drabenstot SD, Buchanan KL, Lai H, Zhu H, Dyer DW, Roe BA, Murphy JW: Introns and splicing elements of five diverse fungi. / Eukaryot Cell 2004, 3: 1088-100. CrossRef
76. Rep M, Duyvesteijn RG, Gale L, Usgaard T, Cornelissen BJ, Ma LJ, Ward TJ: The presence of GC–AG introns in Neurospora crassa and other euascomycetes determined from analyses of complete genomes: implications for automated gene prediction. / Genomics 2006, 87: 338-47. CrossRef
77. Nei M, Kumar S: Molecular evolution and phylogenetics. Oxford University Press, New York 2000. - 作者单位：Christian P Kubicek (1)
Scott Baker (2)
Christian Gamauf (1)
Charles M Kenerley (3)
Irina S Druzhinina (1)
1. Research Area of Gene Technology and Applied Biochemistry, Institute of Chemical Engineering, Vienna University of Technology, Getreidemarkt 9-1665, A-1060, Vienna, Austria
2. Fungal Biotechnology Team, Chemical and Biological Process Development Group, Pacific Northwest National Laboratory, 902 Battelle Blvd., 99352, Richland, WA, USA
3. Department of Plant Pathology and Microbiology, Texas A&M University, 77843, College Station, TX, USA
文摘
Background Hydrophobins are proteins containing eight conserved cysteine residues that occur uniquely in mycelial fungi. Their main function is to confer hydrophobicity to fungal surfaces in contact with air or during attachment of hyphae to hydrophobic surfaces of hosts, symbiotic partners or themselves resulting in morphogenetic signals. Based on their hydropathy patterns and solubility characteristics, hydrophobins are divided into two classes (I and II), the latter being found only in ascomycetes. Results We have investigated the mechanisms driving the evolution of the class II hydrophobins in nine species of the mycoparasitic ascomycetous genus Trichoderma/Hypocrea, using three draft sequenced genomes (H. jecorina = T. reesei, H. atroviridis = T. atroviride; H. virens = T. virens) an additional 14,000 ESTs from six other Trichoderma spp. (T. asperellum, H. lixii = T. harzianum, T. aggressivum var. europeae, T. longibrachiatum, T. cf. viride). The former three contained six, ten and nine members, respectively. Ten is the highest number found in any ascomycete so far. All the hydrophobins we examined had the conserved four beta-strands/one helix structure, which is stabilized by four disulfide bonds. In addition, a small number of these hydrophobins (HFBs)contained an extended N-terminus rich in either proline and aspartate, or glycine-asparagine. Phylogenetic analysis reveals a mosaic of terminal clades containing duplicated genes and shows only three reasonably supported clades. Calculation of the ratio of differences in synonymous vs. non-synonymous nucleotide substitutions provides evidence for strong purifying selection (K S /K a >> 1). A genome database search for class II HFBs from other ascomycetes retrieved a much smaller number of hydrophobins (2-) from each species, and most were from Sordariomycetes. A combined phylogeny of these sequences with those of Trichoderma showed that the Trichoderma HFBs mostly formed their own clades, whereas those of other Sordariomycetes occurred in shared clades. Conclusion Our study shows that the genus Trichoderma/Hypocrea has a proliferated arsenal of class II hydrophobins which arose by birth-and-death evolution followed by purifying selection.