The Ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits

C.L. Schoch; G.H. Sung; F. López-Giráldez; J.P. Townsend; J. Miadlikowska; V. Hofstetter; B. Robbertse; P. Brandon Matheny; F. Kauff; Z. Wang; C. Gueidan; R.M. Andrie; K. Trippe; L.M. Ciufetti; A. Wynns; E. Fraker; B.P. Hodkinson; G. Bonito; J.Z. Groenewald; M. Arzanlou; G.S. de Hoog; P.W. Crous; D. Hewitt; D.H. Pfister; K. Peterson; M. Gryzenhout; M.J. Wingfield; A. Aptroot; S.O. Suh; M. Blackwell; D.M. Hillis; G.W. Griffith; L.A. Castlebury; A.Y. Rossman; H.T. Lumbsch; R. Lücking; B. Büdel; A. Rauhut; P. Diederich; D. Ertz; D.M. Geiser; K. Hosaka; P. Inderbitzin; J. Kohlmeyer; B. Volkmann-Kohlmeyer; L. Mostert; K. O'Donnell; H. Sipman; J.D. Rogers; R.A. Shoemaker; J. Sugiyama; R.C. Summerbell; W. Untereiner; P.R. Johnston; S. Stenroos; A. Zuccaro; P.S. Dyer; P.D. Crittenden; M.S. Cole; K. Hansen; J.M. Trappe; R. Yahr; F. Lutzoni; J.W. Spatafora

doi:10.1093/sysbio/syp020

The Ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits

C.L. Schoch, G.H. Sung, F. López-Giráldez, J.P. Townsend, J. Miadlikowska, V. Hofstetter, B. Robbertse, P. Brandon Matheny, F. Kauff, Z. Wang, C. Gueidan, R.M. Andrie, K. Trippe, L.M. Ciufetti, A. Wynns, E. Fraker, B.P. Hodkinson, G. Bonito, J.Z. Groenewald, M. ArzanlouG.S. de Hoog, P.W. Crous, D. Hewitt, D.H. Pfister, K. Peterson, M. Gryzenhout, M.J. Wingfield, A. Aptroot, S.O. Suh, M. Blackwell, D.M. Hillis, G.W. Griffith, L.A. Castlebury, A.Y. Rossman, H.T. Lumbsch, R. Lücking, B. Büdel, A. Rauhut, P. Diederich, D. Ertz, D.M. Geiser, K. Hosaka, P. Inderbitzin, J. Kohlmeyer, B. Volkmann-Kohlmeyer, L. Mostert, K. O'Donnell, H. Sipman, J.D. Rogers, R.A. Shoemaker, J. Sugiyama, R.C. Summerbell, W. Untereiner, P.R. Johnston, S. Stenroos, A. Zuccaro, P.S. Dyer, P.D. Crittenden, M.S. Cole, K. Hansen, J.M. Trappe, R. Yahr, F. Lutzoni, J.W. Spatafora

Laboratory of Phytopathology

Research output: Contribution to journal › Article › Academic › peer-review

415 Citations (Scopus)

Abstract

We present a 6-gene, 420-species maximum-likelihood phylogeny of Ascomycota, the largest phylum of Fungi. This analysis is the most taxonomically complete to date with species sampled from all 15 currently circumscribed classes. A number of superclass-level nodes that have previously evaded resolution and were unnamed in classifications of the Fungi are resolved for the first time. Based on the 6-gene phylogeny we conducted a phylogenetic informativeness analysis of all 6 genes and a series of ancestral character state reconstructions that focused on morphology of sporocarps, ascus dehiscence, and evolution of nutritional modes and ecologies. A gene-by-gene assessment of phylogenetic informativeness yielded higher levels of informativeness for protein genes (RPB1, RPB2, and TEF1) as compared with the ribosomal genes, which have been the standard bearer in fungal systematics. Our reconstruction of sporocarp characters is consistent with 2 origins for multicellular sexual reproductive structures in Ascomycota, once in the common ancestor of Pezizomycotina and once in the common ancestor of Neolectomycetes. This first report of dual origins of ascomycete sporocarps highlights the complicated nature of assessing homology of morphological traits across Fungi. Furthermore, ancestral reconstruction supports an open sporocarp with an exposed hymenium (apothecium) as the primitive morphology for Pezizomycotina with multiple derivations of the partially (perithecia) or completely enclosed (cleistothecia) sporocarps. Ascus dehiscence is most informative at the class level within Pezizomycotina with most superclass nodes reconstructed equivocally. Character-state reconstructions support a terrestrial, saprobic ecology as ancestral. In contrast to previous studies, these analyses support multiple origins of lichenization events with the loss of lichenization as less frequent and limited to terminal, closely related species.

Original language	English
Pages (from-to)	224-239
Journal	Systematic Biology
Volume	58
Issue number	2
DOIs	https://doi.org/10.1093/sysbio/syp020
Publication status	Published - 2009

Keywords

rna-polymerase-ii
multiple sequence alignment
fungal lineages
cleistothecial fungi
classification
subunit
pezizomycotina
divergence
morphology
eukaryotes

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Schoch, C. L., Sung, G. H., López-Giráldez, F., Townsend, J. P., Miadlikowska, J., Hofstetter, V., Robbertse, B., Brandon Matheny, P., Kauff, F., Wang, Z., Gueidan, C., Andrie, R. M., Trippe, K., Ciufetti, L. M., Wynns, A., Fraker, E., Hodkinson, B. P., Bonito, G., Groenewald, J. Z., ... Spatafora, J. W. (2009). The Ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. Systematic Biology, 58(2), 224-239. https://doi.org/10.1093/sysbio/syp020

Schoch, C.L. ; Sung, G.H. ; López-Giráldez, F. ; Townsend, J.P. ; Miadlikowska, J. ; Hofstetter, V. ; Robbertse, B. ; Brandon Matheny, P. ; Kauff, F. ; Wang, Z. ; Gueidan, C. ; Andrie, R.M. ; Trippe, K. ; Ciufetti, L.M. ; Wynns, A. ; Fraker, E. ; Hodkinson, B.P. ; Bonito, G. ; Groenewald, J.Z. ; Arzanlou, M. ; de Hoog, G.S. ; Crous, P.W. ; Hewitt, D. ; Pfister, D.H. ; Peterson, K. ; Gryzenhout, M. ; Wingfield, M.J. ; Aptroot, A. ; Suh, S.O. ; Blackwell, M. ; Hillis, D.M. ; Griffith, G.W. ; Castlebury, L.A. ; Rossman, A.Y. ; Lumbsch, H.T. ; Lücking, R. ; Büdel, B. ; Rauhut, A. ; Diederich, P. ; Ertz, D. ; Geiser, D.M. ; Hosaka, K. ; Inderbitzin, P. ; Kohlmeyer, J. ; Volkmann-Kohlmeyer, B. ; Mostert, L. ; O'Donnell, K. ; Sipman, H. ; Rogers, J.D. ; Shoemaker, R.A. ; Sugiyama, J. ; Summerbell, R.C. ; Untereiner, W. ; Johnston, P.R. ; Stenroos, S. ; Zuccaro, A. ; Dyer, P.S. ; Crittenden, P.D. ; Cole, M.S. ; Hansen, K. ; Trappe, J.M. ; Yahr, R. ; Lutzoni, F. ; Spatafora, J.W. / The Ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. In: Systematic Biology. 2009 ; Vol. 58, No. 2. pp. 224-239.

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title = "The Ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits",

abstract = "We present a 6-gene, 420-species maximum-likelihood phylogeny of Ascomycota, the largest phylum of Fungi. This analysis is the most taxonomically complete to date with species sampled from all 15 currently circumscribed classes. A number of superclass-level nodes that have previously evaded resolution and were unnamed in classifications of the Fungi are resolved for the first time. Based on the 6-gene phylogeny we conducted a phylogenetic informativeness analysis of all 6 genes and a series of ancestral character state reconstructions that focused on morphology of sporocarps, ascus dehiscence, and evolution of nutritional modes and ecologies. A gene-by-gene assessment of phylogenetic informativeness yielded higher levels of informativeness for protein genes (RPB1, RPB2, and TEF1) as compared with the ribosomal genes, which have been the standard bearer in fungal systematics. Our reconstruction of sporocarp characters is consistent with 2 origins for multicellular sexual reproductive structures in Ascomycota, once in the common ancestor of Pezizomycotina and once in the common ancestor of Neolectomycetes. This first report of dual origins of ascomycete sporocarps highlights the complicated nature of assessing homology of morphological traits across Fungi. Furthermore, ancestral reconstruction supports an open sporocarp with an exposed hymenium (apothecium) as the primitive morphology for Pezizomycotina with multiple derivations of the partially (perithecia) or completely enclosed (cleistothecia) sporocarps. Ascus dehiscence is most informative at the class level within Pezizomycotina with most superclass nodes reconstructed equivocally. Character-state reconstructions support a terrestrial, saprobic ecology as ancestral. In contrast to previous studies, these analyses support multiple origins of lichenization events with the loss of lichenization as less frequent and limited to terminal, closely related species.",

keywords = "rna-polymerase-ii, multiple sequence alignment, fungal lineages, cleistothecial fungi, classification, subunit, pezizomycotina, divergence, morphology, eukaryotes",

author = "C.L. Schoch and G.H. Sung and F. L{\'o}pez-Gir{\'a}ldez and J.P. Townsend and J. Miadlikowska and V. Hofstetter and B. Robbertse and {Brandon Matheny}, P. and F. Kauff and Z. Wang and C. Gueidan and R.M. Andrie and K. Trippe and L.M. Ciufetti and A. Wynns and E. Fraker and B.P. Hodkinson and G. Bonito and J.Z. Groenewald and M. Arzanlou and {de Hoog}, G.S. and P.W. Crous and D. Hewitt and D.H. Pfister and K. Peterson and M. Gryzenhout and M.J. Wingfield and A. Aptroot and S.O. Suh and M. Blackwell and D.M. Hillis and G.W. Griffith and L.A. Castlebury and A.Y. Rossman and H.T. Lumbsch and R. L{\"u}cking and B. B{\"u}del and A. Rauhut and P. Diederich and D. Ertz and D.M. Geiser and K. Hosaka and P. Inderbitzin and J. Kohlmeyer and B. Volkmann-Kohlmeyer and L. Mostert and K. O'Donnell and H. Sipman and J.D. Rogers and R.A. Shoemaker and J. Sugiyama and R.C. Summerbell and W. Untereiner and P.R. Johnston and S. Stenroos and A. Zuccaro and P.S. Dyer and P.D. Crittenden and M.S. Cole and K. Hansen and J.M. Trappe and R. Yahr and F. Lutzoni and J.W. Spatafora",

year = "2009",

doi = "10.1093/sysbio/syp020",

language = "English",

volume = "58",

pages = "224--239",

journal = "Systematic Biology",

issn = "1063-5157",

publisher = "Oxford University Press",

number = "2",

}

Schoch, CL, Sung, GH, López-Giráldez, F, Townsend, JP, Miadlikowska, J, Hofstetter, V, Robbertse, B, Brandon Matheny, P, Kauff, F, Wang, Z, Gueidan, C, Andrie, RM, Trippe, K, Ciufetti, LM, Wynns, A, Fraker, E, Hodkinson, BP, Bonito, G, Groenewald, JZ, Arzanlou, M, de Hoog, GS, Crous, PW, Hewitt, D, Pfister, DH, Peterson, K, Gryzenhout, M, Wingfield, MJ, Aptroot, A, Suh, SO, Blackwell, M, Hillis, DM, Griffith, GW, Castlebury, LA, Rossman, AY, Lumbsch, HT, Lücking, R, Büdel, B, Rauhut, A, Diederich, P, Ertz, D, Geiser, DM, Hosaka, K, Inderbitzin, P, Kohlmeyer, J, Volkmann-Kohlmeyer, B, Mostert, L, O'Donnell, K, Sipman, H, Rogers, JD, Shoemaker, RA, Sugiyama, J, Summerbell, RC, Untereiner, W, Johnston, PR, Stenroos, S, Zuccaro, A, Dyer, PS, Crittenden, PD, Cole, MS, Hansen, K, Trappe, JM, Yahr, R, Lutzoni, F & Spatafora, JW 2009, 'The Ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits', Systematic Biology, vol. 58, no. 2, pp. 224-239. https://doi.org/10.1093/sysbio/syp020

The Ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. / Schoch, C.L.; Sung, G.H.; López-Giráldez, F.; Townsend, J.P.; Miadlikowska, J.; Hofstetter, V.; Robbertse, B.; Brandon Matheny, P.; Kauff, F.; Wang, Z.; Gueidan, C.; Andrie, R.M.; Trippe, K.; Ciufetti, L.M.; Wynns, A.; Fraker, E.; Hodkinson, B.P.; Bonito, G.; Groenewald, J.Z.; Arzanlou, M.; de Hoog, G.S.; Crous, P.W.; Hewitt, D.; Pfister, D.H.; Peterson, K.; Gryzenhout, M.; Wingfield, M.J.; Aptroot, A.; Suh, S.O.; Blackwell, M.; Hillis, D.M.; Griffith, G.W.; Castlebury, L.A.; Rossman, A.Y.; Lumbsch, H.T.; Lücking, R.; Büdel, B.; Rauhut, A.; Diederich, P.; Ertz, D.; Geiser, D.M.; Hosaka, K.; Inderbitzin, P.; Kohlmeyer, J.; Volkmann-Kohlmeyer, B.; Mostert, L.; O'Donnell, K.; Sipman, H.; Rogers, J.D.; Shoemaker, R.A.; Sugiyama, J.; Summerbell, R.C.; Untereiner, W.; Johnston, P.R.; Stenroos, S.; Zuccaro, A.; Dyer, P.S.; Crittenden, P.D.; Cole, M.S.; Hansen, K.; Trappe, J.M.; Yahr, R.; Lutzoni, F.; Spatafora, J.W.

In: Systematic Biology, Vol. 58, No. 2, 2009, p. 224-239.

Research output: Contribution to journal › Article › Academic › peer-review

TY - JOUR

T1 - The Ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits

AU - Schoch, C.L.

AU - Sung, G.H.

AU - López-Giráldez, F.

AU - Townsend, J.P.

AU - Miadlikowska, J.

AU - Hofstetter, V.

AU - Robbertse, B.

AU - Brandon Matheny, P.

AU - Kauff, F.

AU - Wang, Z.

AU - Gueidan, C.

AU - Andrie, R.M.

AU - Trippe, K.

AU - Ciufetti, L.M.

AU - Wynns, A.

AU - Fraker, E.

AU - Hodkinson, B.P.

AU - Bonito, G.

AU - Groenewald, J.Z.

AU - Arzanlou, M.

AU - de Hoog, G.S.

AU - Crous, P.W.

AU - Hewitt, D.

AU - Pfister, D.H.

AU - Peterson, K.

AU - Gryzenhout, M.

AU - Wingfield, M.J.

AU - Aptroot, A.

AU - Suh, S.O.

AU - Blackwell, M.

AU - Hillis, D.M.

AU - Griffith, G.W.

AU - Castlebury, L.A.

AU - Rossman, A.Y.

AU - Lumbsch, H.T.

AU - Lücking, R.

AU - Büdel, B.

AU - Rauhut, A.

AU - Diederich, P.

AU - Ertz, D.

AU - Geiser, D.M.

AU - Hosaka, K.

AU - Inderbitzin, P.

AU - Kohlmeyer, J.

AU - Volkmann-Kohlmeyer, B.

AU - Mostert, L.

AU - O'Donnell, K.

AU - Sipman, H.

AU - Rogers, J.D.

AU - Shoemaker, R.A.

AU - Sugiyama, J.

AU - Summerbell, R.C.

AU - Untereiner, W.

AU - Johnston, P.R.

AU - Stenroos, S.

AU - Zuccaro, A.

AU - Dyer, P.S.

AU - Crittenden, P.D.

AU - Cole, M.S.

AU - Hansen, K.

AU - Trappe, J.M.

AU - Yahr, R.

AU - Lutzoni, F.

AU - Spatafora, J.W.

PY - 2009

Y1 - 2009

N2 - We present a 6-gene, 420-species maximum-likelihood phylogeny of Ascomycota, the largest phylum of Fungi. This analysis is the most taxonomically complete to date with species sampled from all 15 currently circumscribed classes. A number of superclass-level nodes that have previously evaded resolution and were unnamed in classifications of the Fungi are resolved for the first time. Based on the 6-gene phylogeny we conducted a phylogenetic informativeness analysis of all 6 genes and a series of ancestral character state reconstructions that focused on morphology of sporocarps, ascus dehiscence, and evolution of nutritional modes and ecologies. A gene-by-gene assessment of phylogenetic informativeness yielded higher levels of informativeness for protein genes (RPB1, RPB2, and TEF1) as compared with the ribosomal genes, which have been the standard bearer in fungal systematics. Our reconstruction of sporocarp characters is consistent with 2 origins for multicellular sexual reproductive structures in Ascomycota, once in the common ancestor of Pezizomycotina and once in the common ancestor of Neolectomycetes. This first report of dual origins of ascomycete sporocarps highlights the complicated nature of assessing homology of morphological traits across Fungi. Furthermore, ancestral reconstruction supports an open sporocarp with an exposed hymenium (apothecium) as the primitive morphology for Pezizomycotina with multiple derivations of the partially (perithecia) or completely enclosed (cleistothecia) sporocarps. Ascus dehiscence is most informative at the class level within Pezizomycotina with most superclass nodes reconstructed equivocally. Character-state reconstructions support a terrestrial, saprobic ecology as ancestral. In contrast to previous studies, these analyses support multiple origins of lichenization events with the loss of lichenization as less frequent and limited to terminal, closely related species.

AB - We present a 6-gene, 420-species maximum-likelihood phylogeny of Ascomycota, the largest phylum of Fungi. This analysis is the most taxonomically complete to date with species sampled from all 15 currently circumscribed classes. A number of superclass-level nodes that have previously evaded resolution and were unnamed in classifications of the Fungi are resolved for the first time. Based on the 6-gene phylogeny we conducted a phylogenetic informativeness analysis of all 6 genes and a series of ancestral character state reconstructions that focused on morphology of sporocarps, ascus dehiscence, and evolution of nutritional modes and ecologies. A gene-by-gene assessment of phylogenetic informativeness yielded higher levels of informativeness for protein genes (RPB1, RPB2, and TEF1) as compared with the ribosomal genes, which have been the standard bearer in fungal systematics. Our reconstruction of sporocarp characters is consistent with 2 origins for multicellular sexual reproductive structures in Ascomycota, once in the common ancestor of Pezizomycotina and once in the common ancestor of Neolectomycetes. This first report of dual origins of ascomycete sporocarps highlights the complicated nature of assessing homology of morphological traits across Fungi. Furthermore, ancestral reconstruction supports an open sporocarp with an exposed hymenium (apothecium) as the primitive morphology for Pezizomycotina with multiple derivations of the partially (perithecia) or completely enclosed (cleistothecia) sporocarps. Ascus dehiscence is most informative at the class level within Pezizomycotina with most superclass nodes reconstructed equivocally. Character-state reconstructions support a terrestrial, saprobic ecology as ancestral. In contrast to previous studies, these analyses support multiple origins of lichenization events with the loss of lichenization as less frequent and limited to terminal, closely related species.

KW - rna-polymerase-ii

KW - multiple sequence alignment

KW - fungal lineages

KW - cleistothecial fungi

KW - classification

KW - subunit

KW - pezizomycotina

KW - divergence

KW - morphology

KW - eukaryotes

U2 - 10.1093/sysbio/syp020

DO - 10.1093/sysbio/syp020

M3 - Article

VL - 58

SP - 224

EP - 239

JO - Systematic Biology

JF - Systematic Biology

SN - 1063-5157

IS - 2

ER -