Abstract
The depiction of evolutionary relationships within phylum Ascomycota is still controversial because of unresolved branching orders in the radiation of major taxa. Here we generated a dataset of 166 small subunit (18S) rDNA sequences, representative of all groups of Fungi and used as input in a Bayesian phylogenetic analysis. This phylogeny suggests that Discomycetes are a basal group of filamentous Ascomycetes and probably maintain ancestor characters since their representatives are intermingled among other filamentous fungi. Also, we show that the evolutionary rate heterogeneity within Ascomycota precludes the assumption of a global molecular clock. Accordingly, we used the penalized likelihood method, and for calibration we included a 400 million-year-old Pyrenomycete fossil considering two distinct scenarios found in the literature, one with an estimated date of 1576 Myr for the plant–animal–fungus split and the other with an estimated date of 965 Myr for the animal–fungus split. Our data show that the current classification of the fossil as a Pyrenomycete is not compatible with the second scenario. Estimates under the first scenario are older than dates proposed in previous studies based on small subunit rDNA sequences but support estimates based on multiprotein analysis, suggesting that the radiation of the major Ascomycota groups occurred into the Proterozoic era.
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References
CJ Alexopoulos CW Mims MM Blackwell (1996) Introductory mycology John Wiley & Sons New York
ME Alfaro S Zoller F Lutzoni (2003) ArticleTitleBayes or bootstrap? A simulation study comparing the performance of Bayesian Markov chain sampling and bootstrapping in assessing phylogenetic confidence Mol Bio Evol 20 255–266 Occurrence Handle10.1093/molbev/msg028 Occurrence Handle1:CAS:528:DC%2BD3sXhsVOiuro%3D
ML Berbee (1996) ArticleTitleLoculoascomycete origins and evolution of filamentous ascomycetes morphology based on 18S rRNA gene sequence data Mol Biol Evol 13 462–470 Occurrence Handle1:CAS:528:DyaK28Xht1Kgurw%3D Occurrence Handle8742635
ML Berbee (2001) ArticleTitleThe phylogeny of plant and animal pathogens in the Ascomycota Physiol Mol Plant Pathol 59 165–187
ML Berbee JW Taylor (1992) ArticleTitleDetecting morphological convergence in true fungi, using 18S rRNA gene sequence data BioSystems 28 117–125 Occurrence Handle10.1016/0303-2647(92)90014-P Occurrence Handle1:STN:280:ByyC1cvhvVc%3D Occurrence Handle1292657
ML Berbee JW Taylor (1993) ArticleTitleDating the evolutionary radiations of true fungi Can J Bot 71 1114–1127
ML Berbee JW Taylor (2001) Fungal molecular evolution: gene trees and geologic time D McLaughlin E McLaughlin P Lemke (Eds) The Mycota Springer-Verlag Berlin 229–245
ML Berbee D Carmean K Winka (2000) ArticleTitleRibosomal DNA and resolution of branching order among the Ascomycota: How many nucleotides are enough? Mol Phylogenet Evol 17 337–344
L Bromham MD Hendy (2000) ArticleTitleCan fast early rates reconcile molecular dates with the Cambrian explosion? Proc Roy Soc Lond Ser B Biol Sci 267 1041–1047 Occurrence Handle10.1098/rspb.2000.1108 Occurrence Handle1:STN:280:DC%2BD3M%2FhsF2rtg%3D%3D
TD Bruns R Vilgalys SM Barns D Gonzales DS Hibbett DJ Lane L Simon S Stickel TM Szaro WG Weisburg ML Sogin (1992) ArticleTitleEvolutionary relationships within the Fungi: Analyses of nuclear small subunit rRNA sequences Mol Phylogenet Evol 1 231–241
A Cooper D Penny (1997) ArticleTitleMass survival of birds across the Cretaceous–Tertiary boundary: Molecular evidence Science 275 1109–1113 Occurrence Handle10.1126/science.275.5303.1109 Occurrence Handle1:CAS:528:DyaK2sXhtlGlsb8%3D Occurrence Handle9027308
DJ Cutler (2000) ArticleTitleEstimating divergence times in the presence of an overdispersed molecular clock Mol Biol Evol 17 1647–1660 Occurrence Handle11070053
R Dennis (1970) ArticleTitleA middle Pennsylvanian Basidiomycete mycelium with clamp connections Mycologia 62 578–584
RF Doolittle DF Feng S tsang G Cho E Little (1996) ArticleTitleDetermining divergence times of the major kingdoms of living organisms with a protein clock Science 271 470–477 Occurrence Handle1:CAS:528:DyaK28XmvFyktg%3D%3D Occurrence Handle8560259
C Douady F Delsuc Y Boucher W Ford Doolittle E Douzery (2003) ArticleTitleComparison of Bayesian and maximum likelihood bootstrap measures of phylogentic reliability Mol Biol Evol 20 248–254 Occurrence Handle10.1093/molbev/msg042 Occurrence Handle12598692
J Doyle M Donoghue (1993) ArticleTitlePhylogenies and angiosperm diversification Paleobiology 19 141–167
OE Eriksson HO Baral RS Currah K Hansen CP Kurtzman G Rambold T Laessoe (2004) ArticleTitleOutline of Ascomycota—2004 Myconet 10 1–89
J Felsenstein (1985) ArticleTitleConfidence limits on phylogenies: An approach using the bootstrap Evolution 39 783–791
J Felsenstein (1988) ArticleTitlePhylogenies from molecular sequences: Inference and reliability Annu Rev Genet 22 521–565
J Felsenstein (1993) PHYLIP: Phylogeny inference package Seattle WA
N Galtier M Guoy C Gautier (1996) ArticleTitleSeaView and Phylo_win, two graphic tools for sequence alignment and molecular phylogeny Comput Appl Biosci 12 543–548 Occurrence Handle1:CAS:528:DyaK2sXhtlWktLw%3D Occurrence Handle9021275
A Gargas JW Taylor (1995) ArticleTitlePhylogeny of Discomycetes and early radiations of the apothecial ascomycotina inferred from SSu rDNA sequence data Exp Mycol 19 7–15 Occurrence Handle10.1006/emyc.1995.1002 Occurrence Handle1:STN:280:ByqA3sbitVQ%3D Occurrence Handle7614369
M Hasegawa H Kishino T Yano (1989) ArticleTitleEstimation of branching dates among primates by molecular clocks of nuclear DNA which slowed down in hominoidea J Hum Evol 18 461–476 Occurrence Handle10.1016/0047-2484(89)90075-4
DS Heckman DM Geiser BR Eidell RL Stauffer NL Kardos SB Hedges (2001) ArticleTitleMolecular evidence for the early colonization of land by fungi and plants Science 293 1129–1133 Occurrence Handle10.1126/science.1061457 Occurrence Handle1:CAS:528:DC%2BD3MXmtVWrtLk%3D Occurrence Handle11498589
SB Hedges JE Blair ML Venturi JL Shoe (2004) ArticleTitleA molecular time scale of eukaryote evolution and the rise of complex multicellular life BMC Evol Biol 4 2 Occurrence Handle10.1186/1471-2148-4-2 Occurrence Handle15005799
DS Hibbet D Grimaldi MJ Donoghue (1995) ArticleTitleCretaceous mushrooms in amber Nature 377 487
J Huelsenbeck F Ronquist (2001) ArticleTitleMRBAYES: Bayesian inference of phylogenetic trees Bioinformatics 17 754–755 Occurrence Handle10.1093/bioinformatics/17.8.754 Occurrence Handle1:STN:280:DC%2BD3MvotV2isw%3D%3D Occurrence Handle11524383
J Huelsenbeck B Larget R Miller F Ronquist (2002) ArticleTitlePotential applications and pitfalls of Bayesian inference of phylogeny Syst Biol 51 673–688 Occurrence Handle12396583
F Jeanmougin J Thompson N Gouy D Higgins T Gibson (1998) ArticleTitleMultiple sequence alignment with Clustal X Trends Biochem Sci 23 403–405 Occurrence Handle1:CAS:528:DyaK1cXntlansLg%3D Occurrence Handle9810230
T Kasuga TJ White JW Taylor (2002) ArticleTitleEstimation of nucleotide substitution rates in Eurotiomycete Fungi Mol Biol Evol 19 2318–2324 Occurrence Handle12446823
CP Kurtzman (2000) Systematics and taxonomy of yeasts J Ernst A Schmidt (Eds) Dimorphism in human pathogenic and apathogenic yeasts Karger Basel 1–14
B Larget D Simon (1999) ArticleTitleMarkov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees Mol Biol Evol 16 750–759 Occurrence Handle1:CAS:528:DyaK1MXjslGitb8%3D
DD Leipe PO Wainright JH Gunderson D Porter DJ Patterson F Valois S Himmerich ML Sogin (1994) ArticleTitleThe stramenopiles from a molecular perspective: 16S-like rRNA sequences from Labyrinthuloides minuta and Cafeteria roenbergensis Phycologia 33 369–377
YJ Liu S Whelen BD Hall (1999) ArticleTitlePhylogenetic relationships among ascomycetes: Evidence from an RNA polymerase II subunit Mol Biol Evol 16 1799–1808 Occurrence Handle10605121
H Lumbsch (2000) ArticleTitlePhylogeny of filamentous ascomycetes Naturwissenschaften 87 335–342 Occurrence Handle10.1007/s001140050736 Occurrence Handle11013884
F Lutzoni M Pagel V Reeb (2001) ArticleTitleMajor fungal lineages are derived from lichen symbiotic ancestors Nature 411 937–940
DJ Patterson (1989) Stramenopiles: Chromophytes from a protistan perspective JC Green BSC Leadbeater WL Diver (Eds) The chromophyte algae problems and perspectives Clarendon Press Oxford 357–379
A Rambaut L Bromham (1998) ArticleTitleEstimating divergence dates from molecular sequences Mol Biol Evol 15 442–448 Occurrence Handle9549094
D Redecker (2002) ArticleTitleNew views on fungal evolution based on DNA markers and the fossil record Res Microbiol 153 125–130 Occurrence Handle10.1016/S0923-2508(02)01297-4 Occurrence Handle1:CAS:528:DC%2BD38XhvVWksrk%3D Occurrence Handle12002561
D Redecker R Kodner LE Graham (2000) ArticleTitleGlomalean fungi from the Ordovician Science 289 1920–1921 Occurrence Handle10.1126/science.289.5486.1920 Occurrence Handle1:CAS:528:DC%2BD3cXms1alsrk%3D Occurrence Handle10988069
F Rodríguez JL Oliver A Marín JR Medina (1990) ArticleTitleThe general stochastic model of nucleotide substitution J Theor Biol 142 485–501 Occurrence Handle2338834
N Saitou M Nei (1987) ArticleTitleThe neighbor-joining method: a new method for reconstructing phylogenetic trees Mol Biol Evol 4 406–425 Occurrence Handle1:STN:280:BieC1cbgtVY%3D Occurrence Handle3447015
MJ Sanderson (1997) ArticleTitleA nonparametric approach to estimating divergence times in the absence of rate constancy Mol Biol Evol 14 1218–1231 Occurrence Handle1:CAS:528:DyaK2sXnvVCrsbk%3D
MJ Sanderson (2002) ArticleTitleEstimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach Mol Biol Evol 19 101–109 Occurrence Handle11752195
S Shaul Graur (2002) ArticleTitlePlaying chicken (Gallus gallus): Methodological inconsistencies of molecular divergence date estimates due to secondary calibration points Gene 300 59–61 Occurrence Handle10.1016/S0378-1119(02)00851-X Occurrence Handle12468086
DL Swofford (1998) PAUP*. Phylogenetic analysis using parsimony (*and other methods) Sinauer Associates Sunderland, MA
T Taylor H Hass H Kerp (1999) ArticleTitleThe oldest fossil ascomycetes Nature 399 648
DYC Wang S Kumar SB Hedges (1999) ArticleTitleDivergence time estimates for the early history of animal phyla and the origin of plants, animals and fungi Proc Roy Soc London Ser B Biol Sci 266 163–171 Occurrence Handle10.1098/rspb.1999.0617
TP Wilcox DJ Zwickl TA Heath DM Hillis (2002) ArticleTitlePhylogenetic relationships of the dwarf boas and a comparison of Bayesian and bootstrap measures of phylogenetic support Mol Phylogenet Evol 25 361–371
Z Yang (1994) ArticleTitleMaximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods J Mol Evol 39 306–314 Occurrence Handle1:CAS:528:DyaK2cXmt1eit7c%3D Occurrence Handle7932792
AD Yoder Z Yang (2000) ArticleTitleEstimation of primate speciation dates using local molecular clocks Mol Biol Evol 17 1081–1090 Occurrence Handle1:CAS:528:DC%2BD3cXksVOlsr8%3D Occurrence Handle10889221
Acknowledgments
We thank Beatriz Schnabel for excellent technical assistance and help with the artwork. A.C.B.P. received a fellowship from FAPESP (Brazil). G.F.O.S. was supported by a Howard Hughes Medical Institute Post-Doctoral Fellowship (USA). A.B. received grants from FAPESP (Brazil) and M.R.S.B. received grants from FAPESP and CNPq (Brazil) and the International Research Scholars Program of the Howard Hughes Medical Institute (USA).
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Padovan, A.C.B., Sanson, G.F., Brunstein, A. et al. Fungi Evolution Revisited: Application of the Penalized Likelihood Method to a Bayesian Fungal Phylogeny Provides a New Perspective on Phylogenetic Relationships and Divergence Dates of Ascomycota Groups. J Mol Evol 60, 726–735 (2005). https://doi.org/10.1007/s00239-004-0164-y
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DOI: https://doi.org/10.1007/s00239-004-0164-y