Genome expansion and lineage-specific genetic innovations in the forest pathogenic fungi Armillaria

Armillaria species are both devastating forest pathogens and some of the largest terrestrial organisms on Earth. They forage for hosts and achieve immense colony sizes via rhizomorphs, root-like multicellular structures of clonal dispersal. Here, we sequenced and analysed the genomes of four Armilla...

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Published inNature ecology & evolution Vol. 1; no. 12; pp. 1931 - 1941
Main Authors Sipos, György, Prasanna, Arun N., Walter, Mathias C., O’Connor, Eoin, Bálint, Balázs, Krizsán, Krisztina, Kiss, Brigitta, Hess, Jaqueline, Varga, Torda, Slot, Jason, Riley, Robert, Bóka, Bettina, Rigling, Daniel, Barry, Kerrie, Lee, Juna, Mihaltcheva, Sirma, LaButti, Kurt, Lipzen, Anna, Waldron, Rose, Moloney, Nicola M., Sperisen, Christoph, Kredics, László, Vágvölgyi, Csaba, Patrignani, Andrea, Fitzpatrick, David, Nagy, István, Doyle, Sean, Anderson, James B., Grigoriev, Igor V., Güldener, Ulrich, Münsterkötter, Martin, Nagy, László G.
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.12.2017
Nature Publishing Group
Subjects
631/136
631/181/2474
631/208/212
BASIC BIOLOGICAL SCIENCES
Biological and Physical Anthropology
Biomedical and Life Sciences
Decay fungi
Developmental stages
Dispersal
Dispersion
Ecology
Evolutionary Biology
Fruit bodies
Fungi
Gene expression
Gene sequencing
Genes
Genomes
Life Sciences
Lignocellulose
Morphogenesis
Mycelia
Paleontology
Pathogenicity
Pathogens
Plant diseases
Proteomics
Rhizomorphs
Ribonucleic acid
RNA
Root rot
Species
Toolkits
Zoology
Online AccessGet full text
ISSN2397-334X
2397-334X
DOI10.1038/s41559-017-0347-8

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Abstract Armillaria species are both devastating forest pathogens and some of the largest terrestrial organisms on Earth. They forage for hosts and achieve immense colony sizes via rhizomorphs, root-like multicellular structures of clonal dispersal. Here, we sequenced and analysed the genomes of four Armillaria species and performed RNA sequencing and quantitative proteomic analysis on the invasive and reproductive developmental stages of A. ostoyae . Comparison with 22 related fungi revealed a significant genome expansion in Armillaria , affecting several pathogenicity-related genes, lignocellulose-degrading enzymes and lineage-specific genes expressed during rhizomorph development. Rhizomorphs express an evolutionarily young transcriptome that shares features with the transcriptomes of both fruiting bodies and vegetative mycelia. Several genes show concomitant upregulation in rhizomorphs and fruiting bodies and share cis -regulatory signatures in their promoters, providing genetic and regulatory insights into complex multicellularity in fungi. Our results suggest that the evolution of the unique dispersal and pathogenicity mechanisms of Armillaria might have drawn upon ancestral genetic toolkits for wood-decay, morphogenesis and complex multicellularity. Fungi of the genus Armillaria include devastating forest pathogens that cause root rot disease in many plants. Sequencing genomes and transcriptomes of several species, the authors reveal the genetic basis of dispersal, multicellular development and pathogenic mechanisms in Armillaria .
AbstractList Armillaria species are both devastating forest pathogens and some of the largest terrestrial organisms on Earth. They forage for hosts and achieve immense colony sizes via rhizomorphs, root-like multicellular structures of clonal dispersal. Here, we sequenced and analysed the genomes of four Armillaria species and performed RNA sequencing and quantitative proteomic analysis on the invasive and reproductive developmental stages of A. ostoyae. Comparison with 22 related fungi revealed a significant genome expansion in Armillaria, affecting several pathogenicity-related genes, lignocellulose-degrading enzymes and lineage-specific genes expressed during rhizomorph development. Rhizomorphs express an evolutionarily young transcriptome that shares features with the transcriptomes of both fruiting bodies and vegetative mycelia. Several genes show concomitant upregulation in rhizomorphs and fruiting bodies and share cis-regulatory signatures in their promoters, providing genetic and regulatory insights into complex multicellularity in fungi. Our results suggest that the evolution of the unique dispersal and pathogenicity mechanisms of Armillaria might have drawn upon ancestral genetic toolkits for wood-decay, morphogenesis and complex multicellularity.Armillaria species are both devastating forest pathogens and some of the largest terrestrial organisms on Earth. They forage for hosts and achieve immense colony sizes via rhizomorphs, root-like multicellular structures of clonal dispersal. Here, we sequenced and analysed the genomes of four Armillaria species and performed RNA sequencing and quantitative proteomic analysis on the invasive and reproductive developmental stages of A. ostoyae. Comparison with 22 related fungi revealed a significant genome expansion in Armillaria, affecting several pathogenicity-related genes, lignocellulose-degrading enzymes and lineage-specific genes expressed during rhizomorph development. Rhizomorphs express an evolutionarily young transcriptome that shares features with the transcriptomes of both fruiting bodies and vegetative mycelia. Several genes show concomitant upregulation in rhizomorphs and fruiting bodies and share cis-regulatory signatures in their promoters, providing genetic and regulatory insights into complex multicellularity in fungi. Our results suggest that the evolution of the unique dispersal and pathogenicity mechanisms of Armillaria might have drawn upon ancestral genetic toolkits for wood-decay, morphogenesis and complex multicellularity.
Armillaria species are both devastating forest pathogens and some of the largest terrestrial organisms on Earth. They forage for hosts and achieve immense colony sizes via rhizomorphs, root-like multicellular structures of clonal dispersal. Here, we sequenced and analysed the genomes of four Armillaria species and performed RNA sequencing and quantitative proteomic analysis on the invasive and reproductive developmental stages of A. ostoyae . Comparison with 22 related fungi revealed a significant genome expansion in Armillaria , affecting several pathogenicity-related genes, lignocellulose-degrading enzymes and lineage-specific genes expressed during rhizomorph development. Rhizomorphs express an evolutionarily young transcriptome that shares features with the transcriptomes of both fruiting bodies and vegetative mycelia. Several genes show concomitant upregulation in rhizomorphs and fruiting bodies and share cis -regulatory signatures in their promoters, providing genetic and regulatory insights into complex multicellularity in fungi. Our results suggest that the evolution of the unique dispersal and pathogenicity mechanisms of Armillaria might have drawn upon ancestral genetic toolkits for wood-decay, morphogenesis and complex multicellularity. Fungi of the genus Armillaria include devastating forest pathogens that cause root rot disease in many plants. Sequencing genomes and transcriptomes of several species, the authors reveal the genetic basis of dispersal, multicellular development and pathogenic mechanisms in Armillaria .
Armillaria species are both devastating forest pathogens and some of the largest terrestrial organisms on Earth. They forage for hosts and achieve immense colony sizes via rhizomorphs, root-like multicellular structures of clonal dispersal. Here, we sequenced and analysed the genomes of four Armillaria species and performed RNA sequencing and quantitative proteomic analysis on the invasive and reproductive developmental stages of A. ostoyae. Comparison with 22 related fungi revealed a significant genome expansion in Armillaria, affecting several pathogenicity-related genes, lignocellulose-degrading enzymes and lineage-specific genes expressed during rhizomorph development. Rhizomorphs express an evolutionarily young transcriptome that shares features with the transcriptomes of both fruiting bodies and vegetative mycelia. Several genes show concomitant upregulation in rhizomorphs and fruiting bodies and share cis-regulatory signatures in their promoters, providing genetic and regulatory insights into complex multicellularity in fungi. Our results suggest that the evolution of the unique dispersal and pathogenicity mechanisms of Armillaria might have drawn upon ancestral genetic toolkits for wood-decay, morphogenesis and complex multicellularity.
Armillaria species are both devastating forest pathogens and some of the largest terrestrial organisms on Earth. They forage for hosts and achieve immense colony sizes via rhizomorphs, root-like multicellular structures of clonal dispersal. Here, we sequenced and analysed the genomes of four Armillaria species and performed RNA sequencing and quantitative proteomic analysis on the invasive and reproductive developmental stages of A. ostoyae . Comparison with 22 related fungi revealed a significant genome expansion in Armillaria , affecting several pathogenicity-related genes, lignocellulose-degrading enzymes and lineage-specific genes expressed during rhizomorph development. Rhizomorphs express an evolutionarily young transcriptome that shares features with the transcriptomes of both fruiting bodies and vegetative mycelia. Several genes show concomitant upregulation in rhizomorphs and fruiting bodies and share cis -regulatory signatures in their promoters, providing genetic and regulatory insights into complex multicellularity in fungi. Our results suggest that the evolution of the unique dispersal and pathogenicity mechanisms of Armillaria might have drawn upon ancestral genetic toolkits for wood-decay, morphogenesis and complex multicellularity.
Armillaria species are both devastating forest pathogens and some of the largest terrestrial organisms on Earth. They forage for hosts and achieve immense colony sizes via rhizomorphs, root-like multicellular structures of clonal dispersal. Here, we sequenced and analysed the genomes of four Armillaria species and performed RNA sequencing and quantitative proteomic analysis on the invasive and reproductive developmental stages of A. ostoyae. Comparison with 22 related fungi revealed a significant genome expansion in Armillaria, affecting several pathogenicity-related genes, lignocellulose-degrading enzymes and lineage-specific genes expressed during rhizomorph development. Rhizomorphs express an evolutionarily young transcriptome that shares features with the transcriptomes of both fruiting bodies and vegetative mycelia. Several genes show concomitant upregulation in rhizomorphs and fruiting bodies and share cis-regulatory signatures in their promoters, providing genetic and regulatory insights into complex multicellularity in fungi. Our results suggest that the evolution of the unique dispersal and pathogenicity mechanisms of Armillaria might have drawn upon ancestral genetic toolkits for wood-decay, morphogenesis and complex multicellularity.
Armillaria species are both devastating forest pathogens and some of the largest terrestrial organisms on Earth. They forage for hosts and achieve immense colony sizes via rhizomorphs, root-like multicellular structures of clonal dispersal. Here, we sequenced and analysed the genomes of four Armillaria species and performed RNA sequencing and quantitative proteomic analysis on the invasive and reproductive developmental stages of A. ostoyae. Comparison with 22 related fungi revealed a significant genome expansion in Armillaria, affecting several pathogenicity-related genes, lignocellulose-degrading enzymes and lineage-specific genes expressed during rhizomorph development. Rhizomorphs express an evolutionarily young transcriptome that shares features with the transcriptomes of both fruiting bodies and vegetative mycelia. Several genes show concomitant upregulation in rhizomorphs and fruiting bodies and share cis-regulatory signatures in their promoters, providing genetic and regulatory insights into complex multicellularity in fungi. Our results suggest that the evolution of the unique dispersal and pathogenicity mechanisms of Armillaria might have drawn upon ancestral genetic toolkits for wood-decay, morphogenesis and complex multicellularity.Fungi of the genus Armillaria include devastating forest pathogens that cause root rot disease in many plants. Sequencing genomes and transcriptomes of several species, the authors reveal the genetic basis of dispersal, multicellular development and pathogenic mechanisms in Armillaria.
Author Lipzen, Anna
Prasanna, Arun N.
Rigling, Daniel
Lee, Juna
Walter, Mathias C.
Güldener, Ulrich
Vágvölgyi, Csaba
Anderson, James B.
Slot, Jason
Fitzpatrick, David
LaButti, Kurt
Münsterkötter, Martin
Hess, Jaqueline
Sperisen, Christoph
Waldron, Rose
Varga, Torda
Riley, Robert
Sipos, György
Mihaltcheva, Sirma
Bálint, Balázs
Nagy, László G.
O’Connor, Eoin
Kredics, László
Barry, Kerrie
Kiss, Brigitta
Bóka, Bettina
Patrignani, Andrea
Nagy, István
Moloney, Nicola M.
Doyle, Sean
Krizsán, Krisztina
Grigoriev, Igor V.
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  organization: Functional Genomics and Bioinformatics Group, Research Center for Forestry and Wood Industry, University of Sopron, Swiss Federal Research Institute WSL
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  fullname: Hess, Jaqueline
  organization: Department of Botany and Biodiversity Research, University of Vienna
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  organization: Synthetic and Systems Biology Unit, Biological Research Center, Hungarian Academy of Sciences
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  organization: Department of Plant Pathology, Ohio State University
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  organization: Joint Genome Institute US Department of Energy (DOE)
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  organization: Department of Biology, University Maynooth County
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/29085064$$D View this record in MEDLINE/PubMed
https://www.osti.gov/servlets/purl/1543759$$D View this record in Osti.gov
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Snippet Armillaria species are both devastating forest pathogens and some of the largest terrestrial organisms on Earth. They forage for hosts and achieve immense...
Armillaria species are both devastating forest pathogens and some of the largest terrestrial organisms on Earth. They forage for hosts and achieve immense...
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StartPage 1931
SubjectTerms 631/136
631/181/2474
631/208/212
BASIC BIOLOGICAL SCIENCES
Biological and Physical Anthropology
Biomedical and Life Sciences
Decay fungi
Developmental stages
Dispersal
Dispersion
Ecology
Evolutionary Biology
Fruit bodies
Fungi
Gene expression
Gene sequencing
Genes
Genomes
Life Sciences
Lignocellulose
Morphogenesis
Mycelia
Paleontology
Pathogenicity
Pathogens
Plant diseases
Proteomics
Rhizomorphs
Ribonucleic acid
RNA
Root rot
Species
Toolkits
Zoology
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Title Genome expansion and lineage-specific genetic innovations in the forest pathogenic fungi Armillaria
URI https://link.springer.com/article/10.1038/s41559-017-0347-8
https://www.ncbi.nlm.nih.gov/pubmed/29085064
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