Title: Diploid-dominant life cycles characterize the early evolution of Fungi

Abstract

Most of the described species in kingdom Fungi are contained in two phyla, the Ascomycota and the Basidiomycota (subkingdom Dikarya). As a result, our understanding of the biology of the kingdom is heavily influenced by traits observed in Dikarya, such as aerial spore dispersal and life cycles dominated by mitosis of haploid nuclei. We now appreciate that Fungi comprises numerous phylum-level lineages in addition to those of Dikarya, but the phylogeny and genetic characteristics of most of these lineages are poorly understood due to limited genome sampling. Here, we addressed major evolutionary trends in the non-Dikarya fungi by phylogenomic analysis of 69 newly generated draft genome sequences of the zoosporic (flagellated) lineages of true fungi. Our phylogeny indicated five lineages of zoosporic fungi and placed Blastocladiomycota, which has an alternation of haploid and diploid generations, as branching closer to the Dikarya than to the Chytridiomyceta. Our estimates of heterozygosity based on genome sequence data indicate that the zoosporic lineages plus the Zoopagomycota are frequently characterized by diploid-dominant life cycles. We mapped additional traits, such as ancestral cell-cycle regulators, cell-membrane– and cell-wall–associated genes, and the use of the amino acid selenocysteine on the phylogeny and found that these ancestral traits thatmore » are shared with Metazoa have been subject to extensive parallel loss across zoosporic lineages. Together, our results indicate a gradual transition in the genetics and cell biology of fungi from their ancestor and caution against assuming that traits measured in Dikarya are typical of other fungal lineages.« less

Authors:

Amses, Kevin R. ^[1]; Simmons, D. Rabern  ^[1];

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• Search DOE PAGES for ORCID "0000-0002-7033-225X"

Longcore, Joyce E.  ^[2];

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• Search DOE PAGES for ORCID "0000-0003-3632-8772"

Mondo, Stephen J. ^[3]; Seto, Kensuke ^[1]; Jerônimo, Gustavo H.  ^[4];

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• Search DOE PAGES for ORCID "0000-0002-0906-337X"

Bonds, Anne E. ^[1]; Quandt, C. Alisha  ^[5];

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• Search DOE PAGES for ORCID "0000-0003-0260-8995"

Davis, William J.  ^[1];

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• Search DOE PAGES for ORCID "0000-0002-3689-1592"

Chang, Ying ^[6]; Federici, Brian A.  ^[7];

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• Search DOE PAGES for ORCID "0000-0003-1789-6950"

Kuo, Alan  ^[3];

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LaButti, Kurt  ^[3];

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Pangilinan, Jasmyn ^[3]; Andreopoulos, William  ^[3];

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• Search DOE PAGES for ORCID "0000-0001-9097-1123"

Tritt, Andrew  ^[3];

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Riley, Robert ^[3]; Hundley, Hope  ^[3];

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• Search DOE PAGES for ORCID "0000-0001-5071-4587"

Johnson, Jenifer ^[3]; Lipzen, Anna ^[3] more »; Barry, Kerrie ^[3]; Lang, B. Franz  ^[8];

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• Search DOE PAGES for ORCID "0000-0003-1035-5449"

Cuomo, Christina A.  ^[9];

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• Search DOE PAGES for ORCID "0000-0002-5778-960X"

Buchler, Nicolas E.  ^[10];

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• Search DOE PAGES for ORCID "0000-0003-3940-3432"

Grigoriev, Igor V.  ^[11];

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• Search DOE PAGES for ORCID "0000-0002-3136-8903"

Spatafora, Joseph W. ^[12]; Stajich, Jason E.  ^[13];

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• Search DOE PAGES for ORCID "0000-0002-7591-0020"

James, Timothy Y.  ^[1]

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• Search DOE PAGES for ORCID "0000-0002-1123-5986"

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+ Show Author Affiliations

1. Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109
2. School of Biology and Ecology, University of Maine, Orono, ME 04473
3. US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94720
4. Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, Secretaria de Infraestrutura e Meio Ambiente, Instituto de Pesquisas Ambientais, São Paulo 04301-902, Brazil
5. Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80309
6. Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331, Life Sciences, Yale-NUS College, 138527 Singapore
7. Department of Entomology, University of California, Riverside, CA 92521
8. Department of Biochemistry, Robert Cedergren Centre, Université de Montréal, Montréal, QC H3C 3J7, Canada
9. Infectious Disease and Microbiome Program, Broad Institute of MIT and Harvard, Cambridge, MA 02142
10. Department of Molecular Biomedical Sciences, North Carolina State University, Raleigh, NC 27606
11. US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720
12. Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331
13. Department of Plant Pathology &, Microbiology, University of California, Riverside, CA 92521, Institute for Integrative Genome Biology, University of California, Riverside, CA 92521

Publication Date:

Mon Aug 29 00:00:00 EDT 2022

Research Org.:

Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Org.:

USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); National Science Foundation (NSF); National Human Genome Research Institute

OSTI Identifier:

1884334

Alternate Identifier(s):

OSTI ID: 1969051

Grant/Contract Number:  

AC02-05CH11231; DBI-1756202; DBI-1910720; DEB-1929738; DEB-1557110; DEB-1441715; DEB-1441604; IOS-1915750; U54HG003067

Resource Type:

Published Article

Journal Name:

Proceedings of the National Academy of Sciences of the United States of America

Additional Journal Information:

Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 119 Journal Issue: 36; Journal ID: ISSN 0027-8424

Publisher:

Proceedings of the National Academy of Sciences

Country of Publication:

United States

Language:

English

Subject:

59 BASIC BIOLOGICAL SCIENCES; life cycle evolution; phylogenomics; aquatic fungi; plesiomorphy