Transcriptomic atlas of mushroom development reveals conserved genes behind complex multicellularity in fungi
The evolution of complex multicellularity has been one of the major transitions in the history of life. In contrast to simple multicellular aggregates of cells, it has evolved only in a handful of lineages, including animals, embryophytes, red and brown algae, and fungi. Despite being a key step tow...
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| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 116; no. 15; pp. 7409 - 7418 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences
09.04.2019
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| Series | PNAS Plus |
| Subjects | |
| Online Access | Get full text |
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| Abstract | The evolution of complex multicellularity has been one of the major transitions in the history of life. In contrast to simple multicellular aggregates of cells, it has evolved only in a handful of lineages, including animals, embryophytes, red and brown algae, and fungi. Despite being a key step toward the evolution of complex organisms, the evolutionary origins and the genetic underpinnings of complex multicellularity are incompletely known. The development of fungal fruiting bodies from a hyphal thallus represents a transition from simple to complex multicellularity that is inducible under laboratory conditions. We constructed a reference atlas of mushroom formation based on developmental transcriptome data of six species and comparisons of >200 whole genomes, to elucidate the core genetic program of complex multicellularity and fruiting body development in mushroom-forming fungi (Agaricomycetes). Nearly 300 conserved gene families and >70 functional groups contained developmentally regulated genes from five to six species, covering functions related to fungal cell wall remodeling, targeted protein degradation, signal transduction, adhesion, and small secreted proteins (including effector-like orphan genes). Several of these families, including F-box proteins, expansin-like proteins, protein kinases, and transcription factors, showed expansions in Agaricomycetes, many of which convergently expanded in multicellular plants and/or animals too, reflecting convergent solutions to genetic hurdles imposed by complex multicellularity among independently evolved lineages. This study provides an entry point to studying mushroom development and complex multicellularity in one of the largest clades of complex eukaryotic organisms. |
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| AbstractList | The evolution of complex multicellularity has been one of the major transitions in the history of life. In contrast to simple multicellular aggregates of cells, it has evolved only in a handful of lineages, including animals, embryophytes, red and brown algae, and fungi. Despite being a key step toward the evolution of complex organisms, the evolutionary origins and the genetic underpinnings of complex multicellularity are incompletely known. The development of fungal fruiting bodies from a hyphal thallus represents a transition from simple to complex multicellularity that is inducible under laboratory conditions. We constructed a reference atlas of mushroom formation based on developmental transcriptome data of six species and comparisons of >200 whole genomes, to elucidate the core genetic program of complex multicellularity and fruiting body development in mushroom-forming fungi (Agaricomycetes). Nearly 300 conserved gene families and >70 functional groups contained developmentally regulated genes from five to six species, covering functions related to fungal cell wall remodeling, targeted protein degradation, signal transduction, adhesion, and small secreted proteins (including effector-like orphan genes). Several of these families, including F-box proteins, expansin-like proteins, protein kinases, and transcription factors, showed expansions in Agaricomycetes, many of which convergently expanded in multicellular plants and/or animals too, reflecting convergent solutions to genetic hurdles imposed by complex multicellularity among independently evolved lineages. This study provides an entry point to studying mushroom development and complex multicellularity in one of the largest clades of complex eukaryotic organisms. The evolution of complex multicellularity has been one of the major transitions in the history of life. In contrast to simple multicellular aggregates of cells, it has evolved only in a handful of lineages, including animals, embryophytes, red and brown algae, and fungi. Despite being a key step toward the evolution of complex organisms, the evolutionary origins and the genetic underpinnings of complex multicellularity are incompletely known. The development of fungal fruiting bodies from a hyphal thallus represents a transition from simple to complex multicellularity that is inducible under laboratory conditions. We constructed a reference atlas of mushroom formation based on developmental transcriptome data of six species and comparisons of >200 whole genomes, to elucidate the core genetic program of complex multicellularity and fruiting body development in mushroom-forming fungi (Agaricomycetes). Nearly 300 conserved gene families and >70 functional groups contained developmentally regulated genes from five to six species, covering functions related to fungal cell wall remodeling, targeted protein degradation, signal transduction, adhesion, and small secreted proteins (including effector-like orphan genes). Several of these families, including F-box proteins, expansin-like proteins, protein kinases, and transcription factors, showed expansions in Agaricomycetes, many of which convergently expanded in multicellular plants and/or animals too, reflecting convergent solutions to genetic hurdles imposed by complex multicellularity among independently evolved lineages. This study provides an entry point to studying mushroom development and complex multicellularity in one of the largest clades of complex eukaryotic organisms.The evolution of complex multicellularity has been one of the major transitions in the history of life. In contrast to simple multicellular aggregates of cells, it has evolved only in a handful of lineages, including animals, embryophytes, red and brown algae, and fungi. Despite being a key step toward the evolution of complex organisms, the evolutionary origins and the genetic underpinnings of complex multicellularity are incompletely known. The development of fungal fruiting bodies from a hyphal thallus represents a transition from simple to complex multicellularity that is inducible under laboratory conditions. We constructed a reference atlas of mushroom formation based on developmental transcriptome data of six species and comparisons of >200 whole genomes, to elucidate the core genetic program of complex multicellularity and fruiting body development in mushroom-forming fungi (Agaricomycetes). Nearly 300 conserved gene families and >70 functional groups contained developmentally regulated genes from five to six species, covering functions related to fungal cell wall remodeling, targeted protein degradation, signal transduction, adhesion, and small secreted proteins (including effector-like orphan genes). Several of these families, including F-box proteins, expansin-like proteins, protein kinases, and transcription factors, showed expansions in Agaricomycetes, many of which convergently expanded in multicellular plants and/or animals too, reflecting convergent solutions to genetic hurdles imposed by complex multicellularity among independently evolved lineages. This study provides an entry point to studying mushroom development and complex multicellularity in one of the largest clades of complex eukaryotic organisms. Complex multicellularity is a major evolutionary innovation in the history of life. Mushroom-forming fungi (Agaricomycetes) represent one of the most diverse complex multicellular clades, yet the genetic bases and evolutionary origins of their multicellular development are hardly known. We used readouts of gene expression in six species to find genes with a dynamic expression during the development of fruiting bodies. Comparisons across species and to 200 fungal genomes identified the gene families with a conserved expression dynamics in multicellular fruiting bodies and their ancient evolutionary origins. These data outline the major multicellularity-related and developmental processes of mushrooms, including the role of transcriptional reprogramming, gene coexpression networks, and alternative splicing, and reveal significant convergence with other complex multicellular lineages. The evolution of complex multicellularity has been one of the major transitions in the history of life. In contrast to simple multicellular aggregates of cells, it has evolved only in a handful of lineages, including animals, embryophytes, red and brown algae, and fungi. Despite being a key step toward the evolution of complex organisms, the evolutionary origins and the genetic underpinnings of complex multicellularity are incompletely known. The development of fungal fruiting bodies from a hyphal thallus represents a transition from simple to complex multicellularity that is inducible under laboratory conditions. We constructed a reference atlas of mushroom formation based on developmental transcriptome data of six species and comparisons of > 200 whole genomes, to elucidate the core genetic program of complex multicellularity and fruiting body development in mushroom-forming fungi (Agaricomycetes). Nearly 300 conserved gene families and > 70 functional groups contained developmentally regulated genes from five to six species, covering functions related to fungal cell wall remodeling, targeted protein degradation, signal transduction, adhesion, and small secreted proteins (including effector-like orphan genes). Several of these families, including F-box proteins, expansin-like proteins, protein kinases, and transcription factors, showed expansions in Agaricomycetes, many of which convergently expanded in multicellular plants and/or animals too, reflecting convergent solutions to genetic hurdles imposed by complex multicellularity among independently evolved lineages. This study provides an entry point to studying mushroom development and complex multicellularity in one of the largest clades of complex eukaryotic organisms. The evolution of complex multicellularity has been one of the major transitions in the history of life. In contrast to simple multicellular aggregates of cells, it has evolved only in a handful of lineages, including animals, embryophytes, red and brown algae, and fungi. Despite being a key step toward the evolution of complex organisms, the evolutionary origins and the genetic underpinnings of complex multicellularity are incompletely known. The development of fungal fruiting bodies from a hyphal thallus represents a transition from simple to complex multicellularity that is inducible under laboratory conditions. We constructed a reference atlas of mushroom formation based on developmental transcriptome data of six species and comparisons of >200 whole genomes, to elucidate the core genetic program of complex multicellularity and fruiting body development in mushroom-forming fungi (Agaricomycetes). Nearly 300 conserved gene families and >70 functional groups contained developmentally regulated genes from five to six species, covering functions related to fungal cell wall remodeling, targeted protein degradation, signal transduction, adhesion, and small secreted proteins (including effector-like orphan genes). Several of these families, including F-box proteins, expansin-like proteins, protein kinases, and transcription factors, showed expansions in Agaricomycetes, many of which convergently expanded in multicellular plants and/or animals too, reflecting convergent solutions to genetic hurdles imposed by complex multicellularity among independently evolved lineages. Finally, this study provides an entry point to studying mushroom development and complex multicellularity in one of the largest clades of complex eukaryotic organisms. The evolution of complex multicellularity has been one of the major transitions in the history of life. In contrast to simple multicellular aggregates of cells, it has evolved only in a handful of lineages, including animals, embryophytes, red and brown algae, and fungi. Despite being a key step toward the evolution of complex organisms, the evolutionary origins and the genetic underpinnings of complex multicellularity are incompletely known. The development of fungal fruiting bodies from a hyphal thallus represents a transition from simple to complex multicellularity that is inducible under laboratory conditions. We constructed a reference atlas of mushroom formation based on developmental transcriptome data of six species and comparisons of > 200 whole genomes, to elucidate the core genetic program of complex multicellularity and fruiting body development in mushroom-forming fungi (Agaricomycetes). Nearly 300 conserved gene families and > 70 functional groups contained developmentally regulated genes from five to six species, covering functions related to fungal cell wall remodeling, targeted protein degradation, signal transduction, adhesion, and small secreted proteins (including effector-like orphan genes). Several of these families, including F-box proteins, expansin-like proteins, protein kinases, and transcription factors, showed expansions in Agaricomycetes, many of which convergently expanded in multicellular plants and/or animals too, reflecting convergent solutions to genetic hurdles imposed by complex multicellularity among independently evolved lineages. This study provides an entry point to studying mushroom development and complex multicellularity in one of the largest clades of complex eukaryotic organisms. The evolution of complex multicellularity has been one of the major transitions in the history of life. In contrast to simple mul-ticellular aggregates of cells, it has evolved only in a handful of lineages, including animals, embryophytes, red and brown algae, and fungi. Despite being a key step toward the evolution of complex organisms, the evolutionary origins and the genetic underpinnings of complex multicellularity are incompletely known. The development of fungal fruiting bodies from a hyphal thallus represents a transition from simple to complex multicellularity that is inducible under laboratory conditions. We constructed a reference atlas of mushroom formation based on developmental transcriptome data of six species and comparisons of >200 whole genomes, to elucidate the core genetic program of complex multicellularity and fruiting body development in mushroom-forming fungi (Agaricomycetes). Nearly 300 conserved gene families and >70 functional groups contained developmentally regulated genes from five to six species, covering functions related to fungal cell wall remodeling, targeted protein degradation , signal transduction, adhesion, and small secreted proteins (including effector-like orphan genes). Several of these families, including F-box proteins, expansin-like proteins, protein kinases, and transcription factors, showed expansions in Agaricomycetes, many of which convergently expanded in multicellular plants and/or animals too, reflecting convergent solutions to genetic hurdles imposed by complex multicellularity among independently evolved lineages. This study provides an entry point to studying mushroom development and complex multicellularity in one of the largest clades of complex eukaryotic organisms. complex multicellularity | evolution | fungi | comparative genomics | fruiting body development F ungi represent a diverse lineage of complex multicellular organisms with a unique evolutionary history compared with complex multicellular animals, embryophytes, florideophytes, and laminarean brown algae (1-4). Within the fungal kingdom, complex multicellularity is discussed mostly in the context of fruiting bodies, which are found in at least eight independent lin-eages (2), of which the Pezizomycotina (Ascomycota) and the Agaricomycetes (Basidiomycota) contain the vast majority of species. The mushroom-forming fungi (Agaricomycetes) comprise >21,000 species and originated 350 million years ago (5), approximately coinciding with the origin of tetrapods. Fruiting bodies of mushroom-forming fungi have immense importance in agriculture, ecology, and medicine; they represent an important and sustainable food source, with favorable medicinal properties (e.g., antitumor, immunomodulatory) (6). Mushroom-forming fungi share a single origin of fruiting body formation that probably dates to the most recent common ancestor of the Agaricomycetes, Dacrymycetes, and Tremellomycetes (2). Fruiting body development in mushroom-forming fungi has been subject to surprisingly few studies (see, e.g., refs. 7-10), resulting in a paucity of information on the genetic underpinnings of the origins of complex multicellularity in this group (2). During fruiting body development, fungi deploy mechanisms for hypha-to-hypha adhesion, communication (e.g., via Significance Complex multicellularity is a major evolutionary innovation in the history of life. Mushroom-forming fungi (Agaricomycetes) represent one of the most diverse complex multicellular clades, yet the genetic bases and evolutionary origins of their multicellular development are hardly known. We used readouts of gene expression in six species to find genes with a dynamic expression during the development of fruit-ing bodies. Comparisons across species and to 200 fungal genomes identified the gene families with a conserved expression dynamics in multicellular fruiting bodies and their ancient evolutionary origins. These data outline the major multicellularity-related and developmental processes of mushrooms, including the role of transcriptional reprogramming , gene coexpression networks, and alternative splicing , and reveal significant convergence with other complex multicellular lineages. |
| Author | Lipzen, Anna Kües, Ursula Hegedüs, Botond Hibbett, David S. Almási, Éva Johnson, Jenifer Yan, Juying Pangilinan, Jasmyn Kószó, Tamás Bálint, Balázs Nagy, László G. Sahu, Neha Xiong, Yi Barry, Kerrie Henrissat, Bernard Virágh, Máté Kiss, Brigitta Mondo, Stephen Nagy, István Merényi, Zsolt Cseklye, Judit Krizsán, Krisztina Ohm, Robin A. Grigoriev, Igor V. |
| Author_xml | – sequence: 1 givenname: Krisztina surname: Krizsán fullname: Krizsán, Krisztina – sequence: 2 givenname: Éva surname: Almási fullname: Almási, Éva – sequence: 3 givenname: Zsolt surname: Merényi fullname: Merényi, Zsolt – sequence: 4 givenname: Neha surname: Sahu fullname: Sahu, Neha – sequence: 5 givenname: Máté surname: Virágh fullname: Virágh, Máté – sequence: 6 givenname: Tamás surname: Kószó fullname: Kószó, Tamás – sequence: 7 givenname: Stephen surname: Mondo fullname: Mondo, Stephen – sequence: 8 givenname: Brigitta surname: Kiss fullname: Kiss, Brigitta – sequence: 9 givenname: Balázs surname: Bálint fullname: Bálint, Balázs – sequence: 10 givenname: Ursula surname: Kües fullname: Kües, Ursula – sequence: 11 givenname: Kerrie surname: Barry fullname: Barry, Kerrie – sequence: 12 givenname: Judit surname: Cseklye fullname: Cseklye, Judit – sequence: 13 givenname: Botond surname: Hegedüs fullname: Hegedüs, Botond – sequence: 14 givenname: Bernard surname: Henrissat fullname: Henrissat, Bernard – sequence: 15 givenname: Jenifer surname: Johnson fullname: Johnson, Jenifer – sequence: 16 givenname: Anna surname: Lipzen fullname: Lipzen, Anna – sequence: 17 givenname: Robin A. surname: Ohm fullname: Ohm, Robin A. – sequence: 18 givenname: István surname: Nagy fullname: Nagy, István – sequence: 19 givenname: Jasmyn surname: Pangilinan fullname: Pangilinan, Jasmyn – sequence: 20 givenname: Juying surname: Yan fullname: Yan, Juying – sequence: 21 givenname: Yi surname: Xiong fullname: Xiong, Yi – sequence: 22 givenname: Igor V. surname: Grigoriev fullname: Grigoriev, Igor V. – sequence: 23 givenname: David S. surname: Hibbett fullname: Hibbett, David S. – sequence: 24 givenname: László G. surname: Nagy fullname: Nagy, László G. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30902897$$D View this record in MEDLINE/PubMed https://amu.hal.science/hal-02587458$$DView record in HAL https://www.osti.gov/servlets/purl/1604677$$D View this record in Osti.gov |
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| ContentType | Journal Article |
| Copyright | Copyright National Academy of Sciences Apr 9, 2019 Copyright 2019 |
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| DOI | 10.1073/pnas.1817822116 |
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| Issue | 15 |
| Keywords | evolution fungi complex multicellularity comparative genomics fruiting body development |
| Language | English |
| License | Copyright: http://hal.archives-ouvertes.fr/licences/copyright Published under the PNAS license. |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 AC02-05CH11231; LP2014/12; GINOP-2.3.2-15-2016-00001; 758161; 716132 USDOE Office of Science (SC) Hungarian Academy of Sciences European Research Council (ERC) Author contributions: K.K., D.S.H., and L.G.N. designed research; K.K., É.A., Z.M., N.S., M.V., B.B., J.C., and I.N. performed research; K.B., J.C., B. Henrissat, J.J., A.L., R.A.O., I.N., J.P., J.Y., Y.X., and I.V.G. contributed new reagents/analytic tools; K.K., É.A., Z.M., N.S., M.V., T.K., S.M., B.K., B.B., U.K., B. Hegedüs, B. Henrissat, and L.G.N. analyzed data; and K.K., M.V., U.K., K.B., I.V.G., D.S.H., and L.G.N. wrote the paper. Edited by W. Ford Doolittle, Dalhousie University, Halifax, NS, Canada, and approved February 25, 2019 (received for review October 18, 2018) |
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| Snippet | The evolution of complex multicellularity has been one of the major transitions in the history of life. In contrast to simple multicellular aggregates of... The evolution of complex multicellularity has been one of the major transitions in the history of life. In contrast to simple mul-ticellular aggregates of... Complex multicellularity is a major evolutionary innovation in the history of life. Mushroom-forming fungi (Agaricomycetes) represent one of the most diverse... |
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| SubjectTerms | Agaricales - genetics Agaricales - growth & development Agaricomycetes Algae Animals BASIC BIOLOGICAL SCIENCES Biodegradation Biological evolution Biological Sciences Cell walls comparative genetics complex multicellularity Convergence Databases, Nucleic Acid evolution Evolutionary genetics Fruit bodies Fruiting Bodies, Fungal - genetics Fruiting Bodies, Fungal - growth & development fruiting body development Functional groups Fungal Proteins - biosynthesis Fungal Proteins - genetics Fungi Gene Expression Regulation, Fungal - physiology Gene families Genes Genes, Fungal Genomes Kinases Life Sciences Mushrooms PNAS Plus Protein kinase Proteins Signal transduction Thallus Transcription factors Transcriptome - physiology Transduction Vegetal Biology |
| Title | Transcriptomic atlas of mushroom development reveals conserved genes behind complex multicellularity in fungi |
| URI | https://www.jstor.org/stable/26701398 https://www.ncbi.nlm.nih.gov/pubmed/30902897 https://www.proquest.com/docview/2221229649 https://www.proquest.com/docview/2196526630 https://amu.hal.science/hal-02587458 https://www.osti.gov/servlets/purl/1604677 https://pubmed.ncbi.nlm.nih.gov/PMC6462078 |
| Volume | 116 |
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