Phylogenetic utility of protein (RPB2, β-tubulin) and ribosomal (LSU, SSU) gene sequences in the systematics of Sordariomycetes (Ascomycota, Fungi)

Antonie van Leeuwenhoek - Tập 91 - Trang 327-349 - 2006
Alvin M. C. Tang1, Rajesh Jeewon1, Kevin D. Hyde1
1Centre for Research in Fungal Diversity, Department of Ecology & Biodiversity, The University of Hong Kong, Hong Kong, SAR, Republic of China

Tóm tắt

The Sordariomycetes is an important group of fungi whose taxonomic relationships and classification is obscure. There is presently no multi-gene molecular phylogeny that addresses evolutionary relationships among different classes and orders. In this study, phylogenetic analyses with a broad taxon sampling of the Sordariomycetes were conducted to evaluate the utility of four gene regions (LSU rDNA, SSU rDNA, β-tubulin and RPB2) for inferring evolutionary relationships at different taxonomic ranks. Single and multi-gene genealogies inferred from Bayesian and Maximum Parsimony analyses were compared in individual and combined datasets. At the subclass level, SSU rDNA phylogenies demonstrate their utility as a marker to infer phylogenetic relationships at higher levels. All analyses with SSU rDNA alone, combined LSU rDNA and SSU rDNA, and the combined 28 S rDNA, SSU rDNA and RPB2 datasets resulted in three subclasses: Hypocreomycetidae, Sordariomycetidae and Xylariomycetidae, which correspond well to established morphological classification schemes. At the ordinal level, the best resolved phylogeny was obtained from the combined LSU rDNA and SSU rDNA datasets. Individually, the RPB2 gene dataset resulted in significantly higher number of parsimony informative characters. Our results supported the recent separation of Boliniaceae, Chaetosphaeriaceae and Coniochaetaceae from Sordariales and placement of Coronophorales in Hypocreomycetidae. Microascales was found to be paraphyletic and Ceratocystis is phylogenetically associated to Faurelina, while Microascus and Petriella formed another clade and basal to other members of Halosphaeriales. In addition, the order Lulworthiales does not appear to fit in any of the three subclasses. Congruence between morphological and molecular classification schemes is discussed.

Tài liệu tham khảo

Alfaro ME, Zoller S, Lutzoni F (2003) Bayes or bootstrap? A simulation study comparing the performance of Bayesian Markov chain Monte Carlo sampling and bootstrapping in assessing phylogenetic confidence. Mol Biol Evol 20:255–266 Alexopoulos CJ, Mims CW, Blackwell M (1996) Introductory Mycology, 4th edn. John Wiley and Sons Inc., New York Arenal F, Platas G, Peláez F (2005) Two new Preussia species defined based on morphological and molecular evidencerotein coding genes. 20:1–15 Arx JA von (1975) On Thielavia and some similar genera of ascomycetes. Stud Mycol 8:1–31 Arx JA, von (1978) Notes on the Microascaceae with the description of two new species. Persoonia 10:23–21 Arx JA von, Müller E (1954) Die Gattungen der amerosporen Pyrenomyceten. Beitrage szur Kreyptogämenflora der Schweiz 11:1–434 Barr ME (1983) The ascomycetes connection. Mycologia 75:1–13 Barr ME (1987) Prodromus to Class Loculoascomycetes. Newell, Amherst Mass Barr ME (1990) Prodromus to nonlichenized, pyrenomycetous members of Class Hymenoascomycetes. Mycotaxon 39:43–184 Benny GL, Kimbrough JW (1980) A synopsis of the families and orders of Plectomycetes with keys to genera. Mycotaxon 12:1–91 Berbee ML (1996) Loculoascomycete origin and evolution of filamentous ascomycete morphology based on 18 S rRNA gene sequence data. Mol Biol Evol 13:462–470 Berbee ML, Taylor JW (1992) Two ascomycete classes based on fruiting-body characters and ribosomal DNA sequence. Mol Bio Evol 9:278–284 Berbee ML, Carmean DA, Winka K (2000) Ribosomal. DNA and resolution of branching order among the ascomycota: how many nucleotides are enough?. Mol Phylogenet Evol 17:337–344 Campbell J, Shearer CA (2004) Annulusmagnus and Ascitendus, two new genera in the Annulatascaceae. Mycologia 96:822–833 Campbell J, Volkmann-Kohlmeyer B, Grafenhan T, Spatafora JM, Kohlmeyer J (2005) A re-evaluation of Lulworthiales: relationships based on 18 S and 28 S rDNA. Mycol Res 109:556–568 Cai L, Jeewon R, Hyde KD (2005) Phylogenetic evaluation and taxonomic revision of Schizothecium based on ribosomal DNA and protein coding genes. Fung Divers 19:1–17 Cai L, Jeewon R, Hyde KD (2006) Phylogenetic investigations of Sordariaceae based on multiple gene sequences and morphology. Mycol Res 110:137–150 Chaverri P, Castelbury LA, Samuels GJ, Geiser DM (2003) Multilocus phylogenetic structure within the Trichoderma harzianum/Hypocrea lixii complex. Mol Phylogenet Evol 27:302–313 Colless DH (1980) Congruence between morphometric and allozyme data for Menidia species: a reappraisal. Syst Zool 29:288–299 Cunnington JH, Lawrie AC, Pascoe IG (2004) Unexpected ribosomal DNA internal transcribed spacer sequence variation within Erysiphe aquilegiae sensu lato. Fung Divers 16:1–10 Dennis RWG (1960) British cup fungi and their allies. Ray Society, London Denton AL, McConaughy BL, Hall BD (1998) Usefulness of RNA polymerase II coding sequences for estimation of green plant phylogeny. Mol Biol Evol 15:1082–1085 Douady CJ, Delsuc F, Boucher Y, Doolittle WF, Douzery EJP (2003) Comparison of the Bayesian and maximum likelihood bootstrap measures of phylogenetic reliability. Mol Biol Evol 20:248–254 Duong ML, Lumyong S, Hyde KD, Jeewon R (2004) Emarcea castanopsicola gen. et sp. nov. from Thailand, a new xylariaceous taxon based on morphology and DNA sequences. Stud Mycol 50:253–260 Eriksson O, Hawksworth DL (1993) Outline of the Ascomycetes—1993. Syst Ascomycetum 12:1–257 Eriksson OE, Winka K (1997) Supraordinal taxa of Ascomycota. Myconet 1:1–16 Eriksson OE (ed) (2006) Outline of Ascomycota—2006. Myconet 12:1–82 Felsenstein J (1985) Confidence intervals on phylogenetics: an approach using bootstrap. Evolution 39:783–791 Freeman S, Minz D Jurkevitch E, Maymon M, Shabi E (2000) Molecular analyses of Colletotrichum species from almond and other fruits. Phytopathol 90:608–614 Frøslev TG, Matheny PB, Hibbett DS (2005) Lower level relationships in the mushroom genus Cortinarius (Basidiomycota, Agaricales): A comparison of RPB1, RPB2, and ITS phylogenies. Mol Phylogenet Evol 37:602–618 Glass NL, Donaldson GC (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microb 61:1323–1330 Goh TK, Hanlin RT (1994) Ascomal development in Melanospora zamiae. Mycologia 86:357–370 Hall TA (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98 Hansen K, LoBuglio KF, Pfister D (2005) Evolutionary relationships of the cup-fungus genus Peziza and Pezizaceae inferred from multiple nuclear genes: RPB2, β-tubulin, and LSU rDNA. Mol Phylogenet Evol 36:1–23 Hausner G, Reid J, Klassen GR (1993) On The Phylogeny of Ophiostoma, Ceratocystis s.s., Microascus, and relationships within Ophiostoma based on partial ribosomal DNA sequences. Can J Bot 71:1249–1265 Hirt RP, Logsdon JM Jr, Healy B, Dorey MW, Doolittle WF, Embley TM (1999) Microsporidia are related to fungi: evidence from the largest subunit of RNA polymerase II and other proteins. Proc Nat Acad Sci USA 96:580–585 Hsieh HM, Ju YM, Rogers JD (2005) Molecular phylogeny of Hypoxylon and closely related genera. Mycologia 97:844–865 Huelsenbeck JP (1995) The performance of phylogenetic methods in simulation. Syst Biol 44:17–48 Huelsenbeck JP, Ronquist FR (2001) MRBAYES: Bayesian inference of phylogenetic trees. Biometrics 17:754–755 Hunhndorf SM, Miller AN, Fernándes FA (2004a) Molecular systematics of the Sordariales: the order and the family Lasiosphaeriaceae redefined. Mycologia 96:368–387 Huhndorf SM, Miller AN, Fernández FA (2004b) Molecular systematics of the Coronophorales and new species of Bertia, Lasiobertia and Nitschkia. Mycol Res 108:1384–1398 Huhndorf SM, Fernández FA (2005) Teleomorph-anamorph connections: Chaetosphaeria raciborskii and related species, and their Craspedodidymum-like anamorphs. Fung Divers 19:23–49 Huhndorf SM, Miller AN, Fernández FA, Lodge DJ (2005) Neotropical Ascomycetes 13. Cornipulvina and Erythromada, two new genera from the Caribbean and elsewhere. Fung Divers 20:59–69 Issakainen J, Jalava J, Saari J, Campell CK (1999) Relationship of Scedosporium prolificans with Petriella confirmed by partial LSU rDNA sequences. Mycol Res 103:1179–1184 Jeewon R, Liew ECY, Hyde KD (2002) Phylogenetic relationships of Pestalotiopsis and allied genera inferred from ribosomal DNA sequences and morphological characters. Mol Phylogenet Evol 25:378–392 Jeewon R, Liew ECY, Hyde KD (2003) Molecular systematics of the Amphisphaeriaceae based on cladistics analyses of partial LSU rDNA gene sequences. Mycol Res 107:1392–1402 Jeewon R, Liew ECY, Hyde KD (2004) Phylogenetic evaluation of species nomenclature of Pestalotiopsis in relation to host association. Fung Divers 17:39–55 Kauff F, Lutzoni F (2002) Phylogeny of the Gyalectales and Ostropales (Ascomycota, Fungi): among and within order relationships based on nuclear ribosomal RNA small and large subunits. Mol Phylogenet Evol 25:138–156 Kirk PM, Cannon PF, David JC, Stalpers JA (2001) Ainsworth & Bisby’s dictionary of the Fungi, 9th ed. CABI International University Press, Wallingford, UK Klenk HP, Zillig W, Lanzendörfer M, Grampp B, Palm P (1995) Location of protist lineages in a phylogenetic tree inferred from sequences of DNA-dependent RNA polymerases. Arch Protist145:221–230 Kodsueb R, Jeewon R, Vijaykrishna D, McKenzie EHC, Lumyong P, Lumyong S, Hyde KD (2006) Systematic revision of Tubeufiaceae based on morphological and molecular data. Fung Divers 21:105–130 Kohlmeyer J, Spatafora JW, Volkmann-Kohlmeyer B (2000) Lulworthiales, a new order of marine Ascomycota. Mycologia 92:453–458 Landvik S, Egger KN, Schumacher T (1997) Towards a subordinal classification of the Pezizales (Ascomycota): phylogenetic analysis of SSU rDNA sequences. Nord J Bot 17:403–418 Liu Y, Whelen S, Hall BD (1999) Phylogenetic relationships among ascomycetes: evidence from an RNA polymerase II subunit. Mol Bio Evol 16:1799–1808 Liu Y, Hall BD (2004) Body plan evolution of ascomycetes, as inferred from an RNA polymerase II phylogeny. Proc Natl Acad Sci USA 101:4507–4512 Lavoué S, Sullivan JP (2004) Simultaneous analysis of five molecular markers provides a well-supported phylogenetic hypothesis for the living bony-tongue fishes (Osteoglossomorpha: Teleostei). Mol Phylogenet Evol 33:171–185 Lumbsch HT (2000) Phylogeny of filamentous ascomycetes. Naturwissenchaften 87:335–342 Lumbsch HT, Schmitt H, Lindemuth R, Miller A, Mangold A, Fernandez F, Huhndorf S (2005) Performance of four ribosomal DNA regions to infer higher-level phylogenetic relationships of inoperculate euascomycetes (Leotiomyceta). Mol Phylogenet Evol 34:512–524 Lundqvist N (1972) Nordic Sordariaceae s. lat. Symbolae Botanicae Upsalienses 20:1–374 Luttrell ES (1951) Taxonomy of the Pyrenomycetes. University Missouri Stud Sci Ser 24:1–120 Lutzoni F, Kauff F, Cox CJ, McLaughlin D, Celio G, Dentinger B, Padamsee M, Hibbett D, James TY, Baloch E, Grube M, Reeb V, Hofstetter V, Schoch C, Arnold AE, Miadlikowska J, Spatafora J, Johnson D, Hambleton S, Crockett M, Shoemaker R, Sung GH, Lücking R, Lumbsch T, O’Donnell K, Binder M, Diederich P, Ertz D, Gueidan C, Hall B, Hansen K, Harris RC, Hosaka K, Lim YW, Liu Y, Matheny B, Nishida H, Pfister D, Rogers J, Rossman A, Schmitt I, Sipman H, Stone J, Sugiyama J, Yahr R, Vilgalys R (2004) Assembling the fungal tree of life: progress, classification, and evolution of subcellular traits. Am J Bot 91:1446–1480 Matheny PB (2005) Improving phylogenetic inference of mushrooms with RPB1 and RPB2 nucleotide sequences (Inocybe; Agaricales). Mol Phylogenet Evol 35:1–20 Miller JH (1949) A revision of the classification of the ascomycetes with special emphasis on the pyrenomycetes. Mycologia 41:99–127 Miller AN, Huhndorf SM (2005) Multi-gene phylogenies indicate ascomal wall morphology is a better predictor of phylogenetic relationships than ascospore morphology in the Sordariales (Ascomycota, Fungi). Mol Phylogent Evol 35:60–75 Mitchell JI, Roberts PJ, Moss ST (1995) Sequence or structure? a short review on the application of nucleic acid sequence information of fungal taxonomy. Mycologist 9:67–75 Moncalvo JM, Vilgalys R, Redhead SA, Johnson JE, James TY, Aime CM, Hofstetter V, Verduin SJW, Larsson E, Baroni TJ, Thorn RG, Jacobsson S, Clemencon H, Miller OK Jr (2002) One hundred and seventeen clades of euagarics. Mol Phylogenet Evol 23:357–400 Munk A (1953) The system of the pyrenomycetes. Dansk Botanisk Arkiv 15:1–163 Neuveglise C, Brygoo Y, Vercambre B, Riba G (1994) Comparative-analysis of molecular and biological characteristics of strains of Beauveria brongniartii isolated from insects. Mycol Res 98:322–328 Nickerson J, Drouin G (2004) The sequence of the largest subunit of RNA polymerase II is a useful marker for inferring seed plant phylogeny. Mol Phylogenet Evol 31:403–415 Nylander JAA (2004) MrModeltest 2.1. Program distributed by the author. Evolutionary Biology Centre, Uppsala University Parquey-Leduc A, Locuqin-Linard M (1976) L’ontogenie et la structure des peritheces de Faurelina fimigenes Locquin-Linard. Rev Mycol (Paris) 40:161–175 Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818 Réblová M, Winka K (2001)Generic concepts and correlations in ascomycetes based on molecular and morphological data: Lecythothecium duriligni gen. et sp. nov. with a Sporidesmium anamorph, and Ascolacicola austriaca sp. nov. Mycologia 93:479–493 Reeb V, Lutzoni F, Roux C (2004) Contribution of RPB2 to multilocus phylogenetic studies of the euascomycetes (Pezizomycotina, Fungi) with special emphasis on the lichen-forming Acarosporaceae and evolution of polyspory. Mol Phylogenet Evol 2:1036–1060 Rehner SA, Samuels GJ (1995) Molecular systematics of the Hypocreales: a teleomorph gene phylogeny and the status of their anamorphs. Can J Bot 73:S816–S823 Samuels GJ, Blackwell M (2001) Pyrenomycetes. In DJ McLaughlin, EG McLanghlin, PA Lemke (ed) The Mycota. vol. VII, Part A. Systematics and evolution. Springer-Verlag, Berlin, Germany Sidow A, Thomas WK (1994) A molecular evolutionary framework for eukaryotic model organisms. Curr Biol 4:596–603 Silva-Hanlin DMW, Hanlin RT (1999) Small subunit ribosomal RNA gene phylogeny of several loculoascomycetes and its taxonomic implications. Mycol Res 103:153–160 Simmons MP, Pickett KM, Miya M (2004) How meaningful are Bayesian support values? Mol Biol Evol 21:188–199 Smith GJ, Liew ECY, Hyde KD (2003) The Xylariales: a monophyletic order contining 7 families. Fung Divers 13:175–208 Spatafora JW (1995) Ascomal evolution of filamentous ascomycetes: evidence from molecular. Can J Bot S73:811–815 Spatafora JW, Blackwell M (1993) Molecular systematics of unitunicate perithecial ascomycetes: the Clavicipitales–Hypocreales connection. Mycologia 85:912–922 Spatafora JW, Blackwell M (1994) Polyphyletic origins of ophiostomatoid fungi. Mycol Res 98:1–9 Spatafora JW, Volkmann-Kohlmeyer B, Kohlmeyer J (1998) Independent terrestrial origins of the Halosphaeriales (marine Ascomycota). Amer J Bot 85:1569–1580 Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4.0b10. Sinauer Associates, Sunderland, Massachusetts, USA Tanabe Y, Saikawa M, Watanabe MM, Sugiyama J (2004) Molecular phylogeny of Zygomycota based on EF-1a and RPB1 sequences: limitations and utility of alternative markers to rDNA. Mol Phylogenet Evol 30:438–449 Thell A, Feuerer T, Kärnefelt I, Myllys L, Stenroos S (2004) Monophyletic groups within the Parmeliaceae identified by ITS rDNA, β-tubulin and GAPDH sequences: Mycol Progress 3:297–314 Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882 Thorley JL, Wilkinson M (2000) The RadCon manual 1.1.2. Bristol University, UK Tsui CKM, Berbee ML, Jeewon R, Hyde KD (2006) Molecular phylogeny of Dictyosporium and allied genera inferred from ribosomal DNA. Fung Divers 21:157–166 Vijaykrishna D, Jeewon R, Hyde KD (2006) Fusoidispora aquatica: New freshwater ascomycetes from Hong Kong based on morphology and molecules. Sydowia 57:267–280 Villegas M, Cifuentes J, Torres AE (2005) Sporal characters in Gomphales and their significance for phylogenetics. Fung Divers 18:157–175 Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246 Wang Y, Guo LD, Hyde KD (2005) Taxonomic placement of sterile morphotypes of endophytic fungi from Pinus tabulaeformis (Pinaceae) in northeast China based on rDNA sequences. Fung Divers 20:235–260 Wiens JJ (2003) Missing data, incomplete taxa, and phylogenetic accuracy. Syst Biol 52:528–538 White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetic. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322 Witthuhn RC, Wingfield BD, Wingfield MJ, Harrington TC (1999) PCR-based identification and phylogeny of species of Ceratocystis sensu stricto. Mycol Res 103:743–749 Wyk PWJ van, Wingfield MJ, Wyk PS van (1991) Ascospore development on Ceratocystis moniliformis. Mycol Res 95:96–103 Zhang N, Blackwell M (2002) Molecular phylogeny of Melanospora corda and similar pyrenomycetous fungi. Mycol Res 106:148–155 Zhang L, Yang J, Yang Z (2004) Molecular phylogeny of eastern Asian species of Amanita (Agaricales, Basidiomycota): taxonomic and biogeographic implications. Fung Divers 17:219–238