Phylogenetic analyses of RPB1 and RPB2 support a middle Cretaceous origin for a clade comprising all agriculturally and medically important fusaria

Kerry O'Donnell, Alejandro P. Rooney, Robert H. Proctor, Daren W. Brown, Susan P. McCormick, Todd J. Ward, Rasmus J.N. Frandsen, Erik Lysøe, Stephen A. Rehner, Takayuki Aoki, Vincent A.R.G. Robert, Pedro W. Crous, Johannes Z. Groenewald, Seogchan Kang, David Michael Geiser

Research output: Contribution to journalArticle

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Abstract

Fusarium (Hypocreales, Nectriaceae) is one of the most economically important and systematically challenging groups of mycotoxigenic phytopathogens and emergent human pathogens. We conducted maximum likelihood (ML), maximum parsimony (MP) and Bayesian (B) analyses on partial DNA-directed RNA polymerase II largest (RPB1) and second largest subunit (RPB2) nucleotide sequences of 93 fusaria to infer the first comprehensive and well-supported phylogenetic hypothesis of evolutionary relationships within the genus and 20 of its near relatives. Our analyses revealed that Cylindrocarpon formed a basal monophyletic sister to a 'terminal Fusarium clade' (TFC) comprising 20 strongly supported species complexes and nine monotypic lineages, which we provisionally recognize as Fusarium (hypothesis F1). The basal-most divergences within the TFC were only significantly supported by Bayesian posterior probabilities (B-PP 0.99-1). An internode of the remaining TFC, however, was strongly supported by MP and ML bootstrapping and B-PP (hypothesis F2). Analysis of seven Fusarium genome sequences and Southern analysis of fusaria elucidated the distribution of genes required for synthesis of 26 families of secondary metabolites within the phylogenetic framework. Diversification time estimates date the origin of the TFC to the middle Cretaceous 91.3. million years ago. We also dated the origin of several agriculturally important secondary metabolites as well as the lineage responsible for Fusarium head blight of cereals. Dating of several plant-associated species complexes suggests their evolution may have been driven by angiosperm diversification during the Miocene. Our results support two competing hypotheses for the circumscription of Fusarium and provide a framework for future comparative phylogenetic and genomic analyses of this agronomically and medically important genus.

Original languageEnglish (US)
Pages (from-to)20-31
Number of pages12
JournalFungal Genetics and Biology
Volume52
DOIs
StatePublished - Mar 1 2013

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Fusarium
Hypocreales
Angiosperms
Bayes Theorem
RNA Polymerase II
DNA-Directed RNA Polymerases
Sequence Analysis
Genome

All Science Journal Classification (ASJC) codes

  • Microbiology
  • Genetics

Cite this

O'Donnell, Kerry ; Rooney, Alejandro P. ; Proctor, Robert H. ; Brown, Daren W. ; McCormick, Susan P. ; Ward, Todd J. ; Frandsen, Rasmus J.N. ; Lysøe, Erik ; Rehner, Stephen A. ; Aoki, Takayuki ; Robert, Vincent A.R.G. ; Crous, Pedro W. ; Groenewald, Johannes Z. ; Kang, Seogchan ; Geiser, David Michael. / Phylogenetic analyses of RPB1 and RPB2 support a middle Cretaceous origin for a clade comprising all agriculturally and medically important fusaria. In: Fungal Genetics and Biology. 2013 ; Vol. 52. pp. 20-31.
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title = "Phylogenetic analyses of RPB1 and RPB2 support a middle Cretaceous origin for a clade comprising all agriculturally and medically important fusaria",
abstract = "Fusarium (Hypocreales, Nectriaceae) is one of the most economically important and systematically challenging groups of mycotoxigenic phytopathogens and emergent human pathogens. We conducted maximum likelihood (ML), maximum parsimony (MP) and Bayesian (B) analyses on partial DNA-directed RNA polymerase II largest (RPB1) and second largest subunit (RPB2) nucleotide sequences of 93 fusaria to infer the first comprehensive and well-supported phylogenetic hypothesis of evolutionary relationships within the genus and 20 of its near relatives. Our analyses revealed that Cylindrocarpon formed a basal monophyletic sister to a 'terminal Fusarium clade' (TFC) comprising 20 strongly supported species complexes and nine monotypic lineages, which we provisionally recognize as Fusarium (hypothesis F1). The basal-most divergences within the TFC were only significantly supported by Bayesian posterior probabilities (B-PP 0.99-1). An internode of the remaining TFC, however, was strongly supported by MP and ML bootstrapping and B-PP (hypothesis F2). Analysis of seven Fusarium genome sequences and Southern analysis of fusaria elucidated the distribution of genes required for synthesis of 26 families of secondary metabolites within the phylogenetic framework. Diversification time estimates date the origin of the TFC to the middle Cretaceous 91.3. million years ago. We also dated the origin of several agriculturally important secondary metabolites as well as the lineage responsible for Fusarium head blight of cereals. Dating of several plant-associated species complexes suggests their evolution may have been driven by angiosperm diversification during the Miocene. Our results support two competing hypotheses for the circumscription of Fusarium and provide a framework for future comparative phylogenetic and genomic analyses of this agronomically and medically important genus.",
author = "Kerry O'Donnell and Rooney, {Alejandro P.} and Proctor, {Robert H.} and Brown, {Daren W.} and McCormick, {Susan P.} and Ward, {Todd J.} and Frandsen, {Rasmus J.N.} and Erik Lys{\o}e and Rehner, {Stephen A.} and Takayuki Aoki and Robert, {Vincent A.R.G.} and Crous, {Pedro W.} and Groenewald, {Johannes Z.} and Seogchan Kang and Geiser, {David Michael}",
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O'Donnell, K, Rooney, AP, Proctor, RH, Brown, DW, McCormick, SP, Ward, TJ, Frandsen, RJN, Lysøe, E, Rehner, SA, Aoki, T, Robert, VARG, Crous, PW, Groenewald, JZ, Kang, S & Geiser, DM 2013, 'Phylogenetic analyses of RPB1 and RPB2 support a middle Cretaceous origin for a clade comprising all agriculturally and medically important fusaria', Fungal Genetics and Biology, vol. 52, pp. 20-31. https://doi.org/10.1016/j.fgb.2012.12.004

Phylogenetic analyses of RPB1 and RPB2 support a middle Cretaceous origin for a clade comprising all agriculturally and medically important fusaria. / O'Donnell, Kerry; Rooney, Alejandro P.; Proctor, Robert H.; Brown, Daren W.; McCormick, Susan P.; Ward, Todd J.; Frandsen, Rasmus J.N.; Lysøe, Erik; Rehner, Stephen A.; Aoki, Takayuki; Robert, Vincent A.R.G.; Crous, Pedro W.; Groenewald, Johannes Z.; Kang, Seogchan; Geiser, David Michael.

In: Fungal Genetics and Biology, Vol. 52, 01.03.2013, p. 20-31.

Research output: Contribution to journalArticle

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T1 - Phylogenetic analyses of RPB1 and RPB2 support a middle Cretaceous origin for a clade comprising all agriculturally and medically important fusaria

AU - O'Donnell, Kerry

AU - Rooney, Alejandro P.

AU - Proctor, Robert H.

AU - Brown, Daren W.

AU - McCormick, Susan P.

AU - Ward, Todd J.

AU - Frandsen, Rasmus J.N.

AU - Lysøe, Erik

AU - Rehner, Stephen A.

AU - Aoki, Takayuki

AU - Robert, Vincent A.R.G.

AU - Crous, Pedro W.

AU - Groenewald, Johannes Z.

AU - Kang, Seogchan

AU - Geiser, David Michael

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