Genome-scale phylogeny and comparative genomics of the fungal order Sordariales

Noah Hensen; Lucas Bonometti; Ivar Westerberg; Ioana Onut Brännström; Sonia Guillou; Sandrine Cros-Aarteil; Sara Calhoun; Sajeet Haridas; Alan Kuo; Stephen Mondo; Jasmyn Pangilinan; Robert Riley; Kurt LaButti; Bill Andreopoulos; Anna Lipzen; Cindy Chen; Mi Yan; Chris Daum; Vivian Ng; Alicia Clum; Andrei Steindorff; Robin A. Ohm; Francis Martin; Philippe Silar; Donald O. Natvig; Christophe Lalanne; Valérie Gautier; Sandra Lorena Ament-Velásquez; Åsa Kruys; Miriam I. Hutchinson; Amy Jo Powell; Kerrie Barry; Igor V. Grigoriev; Robert Debuchy; Pierre Gladieux; Markus Hiltunen Thorén; Hanna Johannesson

doi:10.1016/j.ympev.2023.107938

Genome-scale phylogeny and comparative genomics of the fungal order Sordariales

Noah Hensen, Lucas Bonometti, Ivar Westerberg, Ioana Onut Brännström, Sonia Guillou, Sandrine Cros-Aarteil, Sara Calhoun, Sajeet Haridas, Alan Kuo, Stephen Mondo, Jasmyn Pangilinan, Robert Riley, Kurt LaButti, Bill Andreopoulos, Anna Lipzen, Cindy Chen, Mi Yan, Chris Daum, Vivian Ng, Alicia ClumAndrei Steindorff, Robin A. Ohm, Francis Martin, Philippe Silar, Donald O. Natvig, Christophe Lalanne, Valérie Gautier, Sandra Lorena Ament-Velásquez, Åsa Kruys, Miriam I. Hutchinson, Amy Jo Powell, Kerrie Barry, Igor V. Grigoriev, Robert Debuchy, Pierre Gladieux, Markus Hiltunen Thorén, Hanna Johannesson^*

^*Corresponding author for this work

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

Abstract

The order Sordariales is taxonomically diverse, and harbours many species with different lifestyles and large economic importance. Despite its importance, a robust genome-scale phylogeny, and associated comparative genomic analysis of the order is lacking. In this study, we examined whole-genome data from 99 Sordariales, including 52 newly sequenced genomes, and seven outgroup taxa. We inferred a comprehensive phylogeny that resolved several contentious relationships amongst families in the order, and cleared-up intrafamily relationships within the Podosporaceae. Extensive comparative genomics showed that genomes from the three largest families in the dataset (Chaetomiaceae, Podosporaceae and Sordariaceae) differ greatly in GC content, genome size, gene number, repeat percentage, evolutionary rate, and genome content affected by repeat-induced point mutations (RIP). All genomic traits showed phylogenetic signal, and ancestral state reconstruction revealed that the variation of the properties stems primarily from within-family evolution. Together, the results provide a thorough framework for understanding genome evolution in this important group of fungi.

Original language	English
Article number	107938
Journal	Molecular Phylogenetics and Evolution
Volume	189
DOIs	https://doi.org/10.1016/j.ympev.2023.107938
Publication status	Published - Dec 2023
Externally published	Yes

Bibliographical note

Publisher Copyright:
© 2023 The Authors

Funding

This work was funded by JGI's Community Science Program grant #504394 and Marie Curie postdoctoral fellowship FP7-PEOPLE-2010-IOF-No.273086 to Pierre Gladieux. The work (proposal: 10.46936/10.25585/60000837, 10.46936/10.25585/60001060 and 10.46936/10.25585/60001199) conducted by the U.S. Department of Energy Joint Genome Institute (https://ror.org/04xm1d337) , a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy operated under Contract No. DE-AC02-05CH11231. We further acknowledge funding from The Bergianus Foundation of The Royal Swedish Academy of Sciences.

Funders	Funder number
Bergianus Foundation of The Royal Swedish Academy of Sciences
National Center for Biotechnology Information	504394
U.S. Department of Energy Joint Genome Institute
U.S. Department of Energy
Office of Science	DE-AC02-05CH11231
National Nuclear Security Administration	DE-NA0003525
European Union (Marie Curie Programme)
Vetenskapsrådet	2018-05973

Keywords

Chaetomiaceae
Genome evolution
Podosporaceae
Sordariaceae
Whole-genome phylogeny

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Cite this

Hensen, N., Bonometti, L., Westerberg, I., Brännström, I. O., Guillou, S., Cros-Aarteil, S., Calhoun, S., Haridas, S., Kuo, A., Mondo, S., Pangilinan, J., Riley, R., LaButti, K., Andreopoulos, B., Lipzen, A., Chen, C., Yan, M., Daum, C., Ng, V., ... Johannesson, H. (2023). Genome-scale phylogeny and comparative genomics of the fungal order Sordariales. Molecular Phylogenetics and Evolution, 189, Article 107938. https://doi.org/10.1016/j.ympev.2023.107938

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title = "Genome-scale phylogeny and comparative genomics of the fungal order Sordariales",

abstract = "The order Sordariales is taxonomically diverse, and harbours many species with different lifestyles and large economic importance. Despite its importance, a robust genome-scale phylogeny, and associated comparative genomic analysis of the order is lacking. In this study, we examined whole-genome data from 99 Sordariales, including 52 newly sequenced genomes, and seven outgroup taxa. We inferred a comprehensive phylogeny that resolved several contentious relationships amongst families in the order, and cleared-up intrafamily relationships within the Podosporaceae. Extensive comparative genomics showed that genomes from the three largest families in the dataset (Chaetomiaceae, Podosporaceae and Sordariaceae) differ greatly in GC content, genome size, gene number, repeat percentage, evolutionary rate, and genome content affected by repeat-induced point mutations (RIP). All genomic traits showed phylogenetic signal, and ancestral state reconstruction revealed that the variation of the properties stems primarily from within-family evolution. Together, the results provide a thorough framework for understanding genome evolution in this important group of fungi.",

keywords = "Chaetomiaceae, Genome evolution, Podosporaceae, Sordariaceae, Whole-genome phylogeny",

author = "Noah Hensen and Lucas Bonometti and Ivar Westerberg and Br{\"a}nnstr{\"o}m, {Ioana Onut} and Sonia Guillou and Sandrine Cros-Aarteil and Sara Calhoun and Sajeet Haridas and Alan Kuo and Stephen Mondo and Jasmyn Pangilinan and Robert Riley and Kurt LaButti and Bill Andreopoulos and Anna Lipzen and Cindy Chen and Mi Yan and Chris Daum and Vivian Ng and Alicia Clum and Andrei Steindorff and Ohm, {Robin A.} and Francis Martin and Philippe Silar and Natvig, {Donald O.} and Christophe Lalanne and Val{\'e}rie Gautier and Ament-Vel{\'a}squez, {Sandra Lorena} and {\AA}sa Kruys and Hutchinson, {Miriam I.} and Powell, {Amy Jo} and Kerrie Barry and Grigoriev, {Igor V.} and Robert Debuchy and Pierre Gladieux and {Hiltunen Thor{\'e}n}, Markus and Hanna Johannesson",

note = "Publisher Copyright: {\textcopyright} 2023 The Authors",

year = "2023",

month = dec,

doi = "10.1016/j.ympev.2023.107938",

language = "English",

volume = "189",

journal = "Molecular Phylogenetics and Evolution",

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Hensen, N, Bonometti, L, Westerberg, I, Brännström, IO, Guillou, S, Cros-Aarteil, S, Calhoun, S, Haridas, S, Kuo, A, Mondo, S, Pangilinan, J, Riley, R, LaButti, K, Andreopoulos, B, Lipzen, A, Chen, C, Yan, M, Daum, C, Ng, V, Clum, A, Steindorff, A, Ohm, RA, Martin, F, Silar, P, Natvig, DO, Lalanne, C, Gautier, V, Ament-Velásquez, SL, Kruys, Å, Hutchinson, MI, Powell, AJ, Barry, K, Grigoriev, IV, Debuchy, R, Gladieux, P, Hiltunen Thorén, M & Johannesson, H 2023, 'Genome-scale phylogeny and comparative genomics of the fungal order Sordariales', Molecular Phylogenetics and Evolution, vol. 189, 107938. https://doi.org/10.1016/j.ympev.2023.107938

TY - JOUR

T1 - Genome-scale phylogeny and comparative genomics of the fungal order Sordariales

AU - Hensen, Noah

AU - Bonometti, Lucas

AU - Westerberg, Ivar

AU - Brännström, Ioana Onut

AU - Guillou, Sonia

AU - Cros-Aarteil, Sandrine

AU - Calhoun, Sara

AU - Haridas, Sajeet

AU - Kuo, Alan

AU - Mondo, Stephen

AU - Pangilinan, Jasmyn

AU - Riley, Robert

AU - LaButti, Kurt

AU - Andreopoulos, Bill

AU - Lipzen, Anna

AU - Chen, Cindy

AU - Yan, Mi

AU - Daum, Chris

AU - Ng, Vivian

AU - Clum, Alicia

AU - Steindorff, Andrei

AU - Ohm, Robin A.

AU - Martin, Francis

AU - Silar, Philippe

AU - Natvig, Donald O.

AU - Lalanne, Christophe

AU - Gautier, Valérie

AU - Ament-Velásquez, Sandra Lorena

AU - Kruys, Åsa

AU - Hutchinson, Miriam I.

AU - Powell, Amy Jo

AU - Barry, Kerrie

AU - Grigoriev, Igor V.

AU - Debuchy, Robert

AU - Gladieux, Pierre

AU - Hiltunen Thorén, Markus

AU - Johannesson, Hanna

PY - 2023/12

Y1 - 2023/12

N2 - The order Sordariales is taxonomically diverse, and harbours many species with different lifestyles and large economic importance. Despite its importance, a robust genome-scale phylogeny, and associated comparative genomic analysis of the order is lacking. In this study, we examined whole-genome data from 99 Sordariales, including 52 newly sequenced genomes, and seven outgroup taxa. We inferred a comprehensive phylogeny that resolved several contentious relationships amongst families in the order, and cleared-up intrafamily relationships within the Podosporaceae. Extensive comparative genomics showed that genomes from the three largest families in the dataset (Chaetomiaceae, Podosporaceae and Sordariaceae) differ greatly in GC content, genome size, gene number, repeat percentage, evolutionary rate, and genome content affected by repeat-induced point mutations (RIP). All genomic traits showed phylogenetic signal, and ancestral state reconstruction revealed that the variation of the properties stems primarily from within-family evolution. Together, the results provide a thorough framework for understanding genome evolution in this important group of fungi.

AB - The order Sordariales is taxonomically diverse, and harbours many species with different lifestyles and large economic importance. Despite its importance, a robust genome-scale phylogeny, and associated comparative genomic analysis of the order is lacking. In this study, we examined whole-genome data from 99 Sordariales, including 52 newly sequenced genomes, and seven outgroup taxa. We inferred a comprehensive phylogeny that resolved several contentious relationships amongst families in the order, and cleared-up intrafamily relationships within the Podosporaceae. Extensive comparative genomics showed that genomes from the three largest families in the dataset (Chaetomiaceae, Podosporaceae and Sordariaceae) differ greatly in GC content, genome size, gene number, repeat percentage, evolutionary rate, and genome content affected by repeat-induced point mutations (RIP). All genomic traits showed phylogenetic signal, and ancestral state reconstruction revealed that the variation of the properties stems primarily from within-family evolution. Together, the results provide a thorough framework for understanding genome evolution in this important group of fungi.

KW - Chaetomiaceae

KW - Genome evolution

KW - Podosporaceae

KW - Sordariaceae

KW - Whole-genome phylogeny

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U2 - 10.1016/j.ympev.2023.107938

DO - 10.1016/j.ympev.2023.107938

M3 - Article

AN - SCOPUS:85174351665

SN - 1055-7903

VL - 189

JO - Molecular Phylogenetics and Evolution

JF - Molecular Phylogenetics and Evolution

M1 - 107938

ER -

Genome-scale phylogeny and comparative genomics of the fungal order Sordariales

Abstract

Bibliographical note

Funding

Keywords

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