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Genetic Diversity and Evolution

Identification of Diverse Mycoviruses through Metatranscriptomics Characterization of the Viromes of Five Major Fungal Plant Pathogens

Shin-Yi Lee Marzano, Berlin D. Nelson, Olutoyosi Ajayi-Oyetunde, Carl A. Bradley, Teresa J. Hughes, Glen L. Hartman, Darin M. Eastburn, Leslie L. Domier
A. Simon, Editor
Shin-Yi Lee Marzano
aDepartment of Crop Sciences, University of Illinois, Urbana, Illinois, USA
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Berlin D. Nelson
bDepartment of Plant Pathology, North Dakota State University, Fargo, North Dakota, USA
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Olutoyosi Ajayi-Oyetunde
aDepartment of Crop Sciences, University of Illinois, Urbana, Illinois, USA
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Carl A. Bradley
aDepartment of Crop Sciences, University of Illinois, Urbana, Illinois, USA
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Teresa J. Hughes
cMonsanto Company, Chesterfield, Missouri, USA
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Glen L. Hartman
aDepartment of Crop Sciences, University of Illinois, Urbana, Illinois, USA
dUnited States Department of Agriculture, Agricultural Research Service, Urbana, Illinois, USA
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Darin M. Eastburn
aDepartment of Crop Sciences, University of Illinois, Urbana, Illinois, USA
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Leslie L. Domier
aDepartment of Crop Sciences, University of Illinois, Urbana, Illinois, USA
dUnited States Department of Agriculture, Agricultural Research Service, Urbana, Illinois, USA
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A. Simon
University of Maryland
Roles: Editor
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DOI: 10.1128/JVI.00357-16
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ABSTRACT

Mycoviruses can have a marked effect on natural fungal communities and influence plant health and productivity. However, a comprehensive picture of mycoviral diversity is still lacking. To characterize the viromes of five widely dispersed plant-pathogenic fungi, Colletotrichum truncatum, Macrophomina phaseolina, Diaporthe longicolla, Rhizoctonia solani, and Sclerotinia sclerotiorum, a high-throughput sequencing-based metatranscriptomic approach was used to detect viral sequences. Total RNA and double-stranded RNA (dsRNA) from mycelia and RNA from samples enriched for virus particles were sequenced. Sequence data were assembled de novo, and contigs with predicted amino acid sequence similarities to viruses in the nonredundant protein database were selected. The analysis identified 72 partial or complete genome segments representing 66 previously undescribed mycoviruses. Using primers specific for each viral contig, at least one fungal isolate was identified that contained each virus. The novel mycoviruses showed affinity with 15 distinct lineages: Barnaviridae, Benyviridae, Chrysoviridae, Endornaviridae, Fusariviridae, Hypoviridae, Mononegavirales, Narnaviridae, Ophioviridae, Ourmiavirus, Partitiviridae, Tombusviridae, Totiviridae, Tymoviridae, and Virgaviridae. More than half of the viral sequences were predicted to be members of the Mitovirus genus in the family Narnaviridae, which replicate within mitochondria. Five viral sequences showed strong affinity with three families (Benyviridae, Ophioviridae, and Virgaviridae) that previously contained no mycovirus species. The genomic information provides insight into the diversity and taxonomy of mycoviruses and coevolution of mycoviruses and their fungal hosts.

IMPORTANCE Plant-pathogenic fungi reduce crop yields, which affects food security worldwide. Plant host resistance is considered a sustainable disease management option but may often be incomplete or lacking for some crops to certain fungal pathogens or strains. In addition, the rising issues of fungicide resistance demand alternative strategies to reduce the negative impacts of fungal pathogens. Those fungus-infecting viruses (mycoviruses) that attenuate fungal virulence may be welcome additions for mitigation of plant diseases. By high-throughput sequencing of the RNAs from 275 isolates of five fungal plant pathogens, 66 previously undescribed mycoviruses were identified. In addition to identifying new potential biological control agents, these results expand the grand view of the diversity of mycoviruses and provide possible insights into the importance of intracellular and extracellular transmission in fungus-virus coevolution.

FOOTNOTES

    • Received 2 March 2016.
    • Accepted 11 May 2016.
    • Accepted manuscript posted online 18 May 2016.
  • Address correspondence to Shin-Yi Lee Marzano, shinyi.marzano{at}sdstate.edu, or Leslie L. Domier, leslie.domier{at}ars.usda.gov.
  • ↵* Present address: Shin-Yi Lee Marzano, Department of Biology and Microbiology, Department of Plant Science, South Dakota State University, Brookings, South Dakota, USA; Carl A. Bradley, Department of Plant Pathology, University of Kentucky Research and Education Center, Princeton, Kentucky, USA.

  • Citation Marzano S-YL, Nelson BD, Ajayi-Oyetunde O, Bradley CA, Hughes TJ, Hartman GL, Eastburn DM, Domier LL. 2016. Identification of diverse mycoviruses through metatranscriptomics characterization of the viromes of five major fungal plant pathogens. J Virol 90:6846–6863. doi:10.1128/JVI.00357-16.

  • Supplemental material for this article may be found at http://dx.doi.org/10.1128/JVI.00357-16.

  • Copyright © 2016, American Society for Microbiology. All Rights Reserved.
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Identification of Diverse Mycoviruses through Metatranscriptomics Characterization of the Viromes of Five Major Fungal Plant Pathogens
Shin-Yi Lee Marzano, Berlin D. Nelson, Olutoyosi Ajayi-Oyetunde, Carl A. Bradley, Teresa J. Hughes, Glen L. Hartman, Darin M. Eastburn, Leslie L. Domier
Journal of Virology Jul 2016, 90 (15) 6846-6863; DOI: 10.1128/JVI.00357-16

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Identification of Diverse Mycoviruses through Metatranscriptomics Characterization of the Viromes of Five Major Fungal Plant Pathogens
Shin-Yi Lee Marzano, Berlin D. Nelson, Olutoyosi Ajayi-Oyetunde, Carl A. Bradley, Teresa J. Hughes, Glen L. Hartman, Darin M. Eastburn, Leslie L. Domier
Journal of Virology Jul 2016, 90 (15) 6846-6863; DOI: 10.1128/JVI.00357-16
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