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

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.

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3];  [4];  [5];  [2];  [2];  [6];  [2];  [7];  [8];  [9];  [10];  [8];  [8];  [8];  [8];  [8];  [4];  [4] more »;  [10];  [9]; ORCiD logo [9];  [11];  [4];  [5];  [4];  [12];  [8];  [3];  [13]; ORCiD logo [2] « less
  1. Univ. of Sopron (Hungary); Swiss Federal Research Inst. WSL, Birmensdorf (Hungary)
  2. Hungarian Academy of Sciences, Szeged (Hungary)
  3. Technische Universität München, Freising (Germany)
  4. Univ. Maynooth County, Kildare (Ireland)
  5. Seqomics Ltd. Mórahalom (Hungary)
  6. Univ. of Vienna (Austria)
  7. The Ohio State Univ., Columbus, OH (United States)
  8. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  9. Univ. of Szeged (Hungary)
  10. Swiss Federal Research Inst. WSL, Birmensdorf (Hungary)
  11. Univ. of Zurich (Switzerland)
  12. Univ. of Toronto, ON (Canada)
  13. Univ. of Sopron (Hungary); Helmholtz Zentrum München (Germany)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC); Univ. of California, Oakland, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1543759
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Nature Ecology and Evolution
Additional Journal Information:
Journal Volume: 1; Journal Issue: 12; Journal ID: ISSN 2397-334X
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

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, and Nagy, László G. Genome expansion and lineage-specific genetic innovations in the forest pathogenic fungi Armillaria. United States: N. p., 2017. Web. doi:10.1038/s41559-017-0347-8.
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. Genome expansion and lineage-specific genetic innovations in the forest pathogenic fungi Armillaria. United States. doi:10.1038/s41559-017-0347-8.
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, and Nagy, László G. Mon . "Genome expansion and lineage-specific genetic innovations in the forest pathogenic fungi Armillaria". United States. doi:10.1038/s41559-017-0347-8. https://www.osti.gov/servlets/purl/1543759.
@article{osti_1543759,
title = {Genome expansion and lineage-specific genetic innovations in the forest pathogenic fungi Armillaria},
author = {Sipos, György and Prasanna, Arun N. and Walter, Mathias C. and O’Connor, Eoin and Bálint, Balázs and Krizsán, Krisztina and Kiss, Brigitta and Hess, Jaqueline and Varga, Torda and Slot, Jason and Riley, Robert and Bóka, Bettina and Rigling, Daniel and Barry, Kerrie and Lee, Juna and Mihaltcheva, Sirma and LaButti, Kurt and Lipzen, Anna and Waldron, Rose and Moloney, Nicola M. and Sperisen, Christoph and Kredics, László and Vágvölgyi, Csaba and Patrignani, Andrea and Fitzpatrick, David and Nagy, István and Doyle, Sean and Anderson, James B. and Grigoriev, Igor V. and Güldener, Ulrich and Münsterkötter, Martin and Nagy, László G.},
abstractNote = {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.},
doi = {10.1038/s41559-017-0347-8},
journal = {Nature Ecology and Evolution},
number = 12,
volume = 1,
place = {United States},
year = {2017},
month = {10}
}

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