Skip to main content
SpringerLink
Log in
Book cover

Biocommunication of Fungi pp 71–83Cite as

Genes from Double-Stranded RNA Viruses in the Nuclear Genomes of Fungi

  • Chapter
  • First Online:

Abstract

The sequencing of large numbers of eukaryotic genomes has demonstrated the widespread occurrence of viral genes in nuclear (and mitochondrial) genomes. Essentially all the families of RNA viruses are represented, and we have coined the term NIRV (non-retroviral integrated RNA virus) for these sequences. Some 3% of sequenced eukaryotic genomes have NIRVs and the fungi are well represented with both complete and partial copies of RNA viral genes. The fungal NIRVs are the best characterized and demonstrate that, with the most widespread fungal viruses, the dsRNA totiviruses and partitiviruses, which generally exist as stable persistent infections in their hosts, gene transfers between host and virus have taken place in both directions. Selection has preserved those events with adaptive value: hosts with NIRVs have become immune to infection with the cognate virus and viruses with cellular toxin genes provide an advantage to their hosts by killing cells without the virus.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Abel PP, Nelson RS, De B, Hoffmann N, Rogers SG, Fraley RT, Beachy RN (1986) Delay of disease development in transgenic plants that express the tobacco mosaic virus coat protein gene. Science 232:738–743

    Article  PubMed  CAS  Google Scholar 

  • Ballinger MJ, Bruenn JA, Taylor DJ (2012) Evolution and expression of sigma virus-like genes in Drosophila after integration by an LTR retroelement (submitted)

    Google Scholar 

  • Belyi VA, Levine AJ, Skalka AM (2010) Unexpected inheritance: multiple integrations of ancient bornavirus and ebolavirus/marburgvirus sequences in vertebrate genomes. PLoS Pathog 6:e1001030

    Article  PubMed  Google Scholar 

  • Bivalkar-Mehla S, Vakharia J, Mehla R, Abreha M, Kanwar JR, Tikoo A, Chauhan A (2011) Viral RNA silencing suppressors (RSS): novel strategy of viruses to ablate the host RNA interference (RNAi) defense system. Virus Res 155:1–9

    Article  PubMed  CAS  Google Scholar 

  • Blower TR, Salmond GP, Luisi BF (2011) Balancing at survival’s edge: the structure and adaptive benefits of prokaryotic toxin-antitoxin partners. Curr Opin Struct Biol 21:109–118

    Article  PubMed  CAS  Google Scholar 

  • Boone C, Bussey H, Greene D, Thomas DY, Vernet T (1986) Yeast killer toxin: site-directed mutations implicate the precursor protein as the immunity component. Cell 46:105–113

    Article  PubMed  CAS  Google Scholar 

  • Bostian KA, Elliott Q, Bussey H, Burn V, Smith A, Tipper DJ (1984) Sequence of the preprotoxin dsRNA gene of type 1 killer yeast: multiple processing events produce a two-component toxin. Cell 36:741–751

    Article  PubMed  CAS  Google Scholar 

  • Breinig F, Sendzik T, Eisfeld K, Schmitt MJ (2006) Dissecting toxin immunity in virus-infected killer yeast uncovers an intrinsic strategy of self-protection. Proc Natl Acad Sci USA 103:3810–3815

    Article  PubMed  CAS  Google Scholar 

  • Bruenn JA (1986) The killer systems of Saccharomyces cerevisiae and other yeasts. In: Buck K (ed) Fungal virology. CRC Press, Boca Raton, pp 85–108

    Google Scholar 

  • Bruenn JA (1999) The Ustilago maydis viruses. In: Granoff A, Webster RG (eds) Encyclopedia of virology. Academic, London, pp 1812–1817

    Chapter  Google Scholar 

  • Bruenn JA (2000) Viruses of fungi and protozoans: is everyone sick? In: Hurst CJ (ed) Viral ecology. Academic, New York, pp 297–317

    Chapter  Google Scholar 

  • Bruenn J (2008) The Ustilago maydis viruses. In: Mahy BWJ, Regenmortel Mv (eds) Encyclopedia of virology. Elsevier, Amsterdam, pp 214–219

    Chapter  Google Scholar 

  • Bruenn J, Taylor DJ (2012) Co-adaption of viruses and their fungal hosts. (in preparation)

    Google Scholar 

  • Chiba S, Kondo H, Tani A, Saisho D, Sakamoto W, Kanematsu S, Suzuki N (2011) Widespread endogenization of genome sequences of non-retroviral RNA viruses into plant genomes. PLoS Pathog 7:e1002146

    Article  PubMed  CAS  Google Scholar 

  • Crochu S, Cook S, Attoui H, Charrel RN, De Chesse R, Belhouchet M, Lemasson JJ, de Micco P, de Lamballerie X (2004) Sequences of flavivirus-related RNA viruses persist in DNA form integrated in the genome of Aedes spp. mosquitoes. J Gen Virol 85:1971–1980

    Article  PubMed  CAS  Google Scholar 

  • Czech B, Hannon GJ (2011) Small RNA sorting: matchmaking for argonautes. Nat Rev Genet 12:19–31

    Article  PubMed  CAS  Google Scholar 

  • Diamond G, Beckloff N, Weinberg A, Kisich KO (2009) The roles of antimicrobial peptides in innate host defense. Curr Pharm Des 15:2377–2392

    Article  PubMed  CAS  Google Scholar 

  • Dignard D, Whiteway M, Germain D, Tessier D, Thomas DY (1991) Expression in yeast of a cDNA copy of the K2 killer toxin gene. Mol Gen Genet 227:127–136

    Article  PubMed  CAS  Google Scholar 

  • Drinnenberg IA, Fink GR, Bartel DP (2011) Compatibility with killer explains the rise of RNAi-deficient fungi. Science 333:1592

    Article  PubMed  CAS  Google Scholar 

  • Frank AC, Wolfe KH (2009) Evolutionary capture of viral and plasmid DNA by yeast nuclear chromosomes. Eukaryot Cell 8:1521–1531

    Article  PubMed  CAS  Google Scholar 

  • Fujimura T, Esteban R, Esteban LM, Wickner RB (1990) Portable encapsidation signal of the L-A double-stranded RNA virus of S. cerevisiae. Cell 62:819–828

    Article  PubMed  CAS  Google Scholar 

  • Geuking MB, Weber J, Dewannieux M, Gorelik E, Heidmann T, Hengartner H, Zinkernagel RM, Hangartner L (2009) Recombination of retrotransposon and exogenous RNA virus results in nonretroviral cDNA integration. Science 323:393–396

    Article  PubMed  CAS  Google Scholar 

  • Gilbert C, Schaack S, Pace JK 2nd, Brindley PJ, Feschotte C (2010) A role for host-parasite interactions in the horizontal transfer of transposons across phyla. Nature 464:1347–1350

    Article  PubMed  CAS  Google Scholar 

  • Hammond TM, Andrewski MD, Roossinck MJ, Keller NP (2008) Aspergillus mycoviruses are targets and suppressors of RNA silencing. Eukaryot Cell 7:350–357

    Article  PubMed  CAS  Google Scholar 

  • Hoffmann JA (2003) The immune response of Drosophila. Nature 426:33–38

    Article  PubMed  CAS  Google Scholar 

  • Holmes EC (2009) The emergence and evolution of RNA viruses, vol 1. Oxford University Press, Oxford

    Google Scholar 

  • Horie M, Honda T, Suzuki Y, Kobayashi Y, Daito T, Oshida T, Ikuta K, Jern P, Gojobori T, Coffin JM et al (2010) Endogenous non-retroviral RNA virus elements in mammalian genomes. Nature 463:84–87

    Article  PubMed  CAS  Google Scholar 

  • Katzourakis A, Gifford RJ (2010) Endogenous viral elements in animal genomes. PLoS Genet 6:e1001191

    Article  PubMed  Google Scholar 

  • Koonin EV (2010) Taming of the shrewd: novel eukaryotic genes from RNA viruses. BMC Biol 8:2

    Article  PubMed  Google Scholar 

  • Li N, Erman M, Pangborn W, Duax WL, Park C-M, Bruenn JA, Ghosh D (1999) Structure of Ustilago maydis killer toxin KP6 a-subunit: a multimeric assembly with a central pore. J Biol Chem 274:20425–20431

    Article  PubMed  CAS  Google Scholar 

  • Liu H, Fu Y, Jiang D, Li G, Xie J, Cheng J, Peng Y, Ghabrial SA, Yi X (2010) Widespread horizontal gene transfer from double-stranded RNA viruses to eukaryotic nuclear genomes. J Virol 84:11876–11887

    Article  PubMed  CAS  Google Scholar 

  • Lolle S, Skipper N, Bussey H, Thomas DY (1984) The expression of cDNA clones of yeast M1 double-stranded RNA in yeast confers both killer and immunity phenotypes. EMBO J 3:1383–1387

    PubMed  CAS  Google Scholar 

  • Mayor C, Brudno M, Schwartz JR, Poliakov A, Rubin EM, Frazer KA, Pachter LS, Dubchak I (2000) VISTA: visualizing global DNA sequence alignments of arbitrary length. Bioinformatics 16:1046–1047

    Article  PubMed  CAS  Google Scholar 

  • Moran NA, Jarvik T (2010) Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science 328:624–627

    Article  PubMed  CAS  Google Scholar 

  • Palffy R, Gardlik R, Behuliak M, Kadasi L, Turna J, Celec P (2009) On the physiology and pathophysiology of antimicrobial peptides. Mol Med 15:51–59

    PubMed  CAS  Google Scholar 

  • Park C-M, Banerjee N, Koltin Y, Bruenn JA (1996) The Ustilago maydis virally encoded KP1 killer toxin. Mol Microbiol 20:957–963

    Article  PubMed  CAS  Google Scholar 

  • Peery T, Shabat-Brand T, Steinlauf R, Koltin Y, Bruenn J (1987) The virus encoded toxin of Ustilago maydis – two polypeptides are essential for activity. Mol Cell Biol 7:470–477

    PubMed  CAS  Google Scholar 

  • Reimann-Philipp U (1998) Mechanisms of resistance. Expression of coat protein. Methods Mol Biol 81:521–532

    PubMed  CAS  Google Scholar 

  • Ribas JC, Fujimura T, Wickner RB (1994) Essential RNA binding and packaging domains of the Gag-Pol fusion protein of the L-A double-stranded RNA virus of Saccharomyces cerevisiae. J Biol Chem 269:28420–28428

    PubMed  CAS  Google Scholar 

  • Rodriguez-Cousino N, Maqueda M, Ambrona J, Zamora E, Esteban R, Ramirez M (2011) A new wine Saccharomyces cerevisiae killer toxin (Klus), encoded by a double-stranded RNA virus, with broad antifungal activity is evolutionarily related to a chromosomal host gene. Appl Environ Microbiol 77:1822–1832

    Article  PubMed  CAS  Google Scholar 

  • Russell PJ, Bennett AM, Love Z, Baggott DM (1997) Cloning, sequencing and expression of a full-length cDNA copy of the M1 double-stranded RNA virus from the yeast, Saccharomyces cerevisiae. Yeast 13:829–836

    Article  PubMed  CAS  Google Scholar 

  • Russell AB, Hood RD, Bui NK, LeRoux M, Vollmer W, Mougous JD (2011) Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475:343–347

    Article  PubMed  CAS  Google Scholar 

  • Schmitt MJ, Breinig F (2002) The viral killer system in yeast: from molecular biology to application. FEMS Microbiol Rev 26:257–276

    Article  PubMed  CAS  Google Scholar 

  • Schmitt MJ, Breinig F (2006) Yeast viral killer toxins: lethality and self-protection. Nat Rev Microbiol 4:212–221

    Article  PubMed  CAS  Google Scholar 

  • Schmitt MJ, Neuhausen F (1994) Killer toxin-secreting double-stranded RNA mycoviruses in the yeasts Hanseniaspora uvarum and Zygosaccharomyces bailii. J Virol 68:1765–1772

    PubMed  CAS  Google Scholar 

  • Schmitt MJ, Tipper DJ (1990) K28, a unique double-stranded RNA killer virus of Saccharomyces cerevisiae. Mol Cell Biol 10:4807–4815

    PubMed  CAS  Google Scholar 

  • Schmitt MJ, Tipper DJ (1995) Sequence of the M28 dsRNA: preprotoxin is processed to an alpha/beta heterodimeric protein toxin. Virology 213:341–351

    Article  PubMed  CAS  Google Scholar 

  • Schmitt MJ, Poravou O, Trenz K, Rehfeldt K (1997) Unique double-stranded RNAs responsible for the anti-Candida activity of the yeast Hanseniaspora uvarum. J Virol 71:8852–8855

    PubMed  CAS  Google Scholar 

  • Shen Y, Bruenn JA (1993) RNA Structural requirements for RNA binding in a double-stranded RNA virus. Virology 195:481–491

    Article  PubMed  CAS  Google Scholar 

  • Smith HA, Swaney SL, Parks TD, Wernsman EA, Dougherty WG (1994) Transgenic plant virus resistance mediated by untranslatable sense RNAs: expression, regulation, and fate of nonessential RNAs. Plant Cell 6:1441–1453

    PubMed  CAS  Google Scholar 

  • Sommer SS, Wickner RB (1982) Co-curing of plasmids affecting killer double-stranded RNAs of Saccharomyces cerevisiae: [HOK], [NEX], and the abundance of L are related and further evidence that M1 requires L. J Bacteriol 150:545–551

    PubMed  CAS  Google Scholar 

  • Steinlauf R, Peery T, Koltin Y, Bruenn J (1988) The Ustilago maydis virus encoded toxin – effect of KP6 on cells and spheroplasts. Exp Mycol 12:264–274

    Article  CAS  Google Scholar 

  • Sturley SL, Elliot Q, Levitre J, Tipper DJ, Bostian KA (1986) Mapping of functional domains within the Saccharomyces cerevisiae type 1 killer preprotoxin. EMBO J 5:3381–3389

    PubMed  CAS  Google Scholar 

  • Tao J, Ginsberg I, Banerjee N, Koltin Y, Held W, Bruenn JA (1990) The Ustilago maydis KP6 killer toxin: structure, expression in Saccharomyces cerevisiae and relationship to other cellular toxins. Mol Cell Biol 10:1373–1381

    PubMed  CAS  Google Scholar 

  • Taylor DJ, Bruenn J (2009) The evolution of novel fungal genes from non-retroviral RNA viruses. BMC Biol 7:88

    Article  PubMed  Google Scholar 

  • Taylor DJ, Leach RW, Bruenn J (2010) Filoviruses are ancient and integrated into mammalian genomes. BMC Evol Biol 10:193–202

    Article  PubMed  Google Scholar 

  • Tipper DJ, Schmitt MJ (1991) Yeast dsRNA viruses: replication and killer phenotypes. Mol Microbiol 5:2331–2338

    Article  PubMed  CAS  Google Scholar 

  • Valle RP, Wickner RB (1993) Elimination of L-A double-stranded RNA virus of Saccharomyces cerevisiae by expression of gag and gag-pol from L-A cDNA clone. J Virol 67:2764–2771

    PubMed  CAS  Google Scholar 

  • Weiler F, Schmitt MJ (2003) Zygocin, a secreted antifungal toxin of the yeast Zygosaccharomyces bailii, and its effect on sensitive fungal cells. FEMS Yeast Res 3:69–76

    PubMed  CAS  Google Scholar 

  • Weiler F, Rehfeldt K, Bautz F, Schmitt MJ (2002) The Zygosaccharomyces bailii antifungal virus toxin zygocin: cloning and expression in a heterologous fungal host. Mol Microbiol 46:1095–1105

    Article  PubMed  CAS  Google Scholar 

  • Wickner RB (1979) The killer double-stranded RNA plasmids of yeast. Plasmid 2:303–322

    Article  PubMed  CAS  Google Scholar 

  • Wickner RB (1983) Killer systems in Saccharomyces cerevisiae: three distinct modes of exclusion of M2 double-stranded RNA by three species of double-stranded RNA, M1, L-A-E, and L-A-HN. Mol Cell Biol 3:654–661

    PubMed  CAS  Google Scholar 

  • Wickner RB (1996) Double-stranded RNA viruses of Saccharomyces cerevisiae. Microbiol Rev 60:250–265

    PubMed  CAS  Google Scholar 

  • Wickner RB, Fujimura T, Esteban R (1986) Overview of double-stranded RNA replication in Saccharomyces cerevisiae. Basic Life Sci 40:149–163

    PubMed  CAS  Google Scholar 

  • Wloch-Salamon DM, Gerla D, Hoekstra RF, de Visser JA (2008) Effect of dispersal and nutrient availability on the competitive ability of toxin-producing yeast. Proc Biol Sci 275:535–541

    Article  PubMed  Google Scholar 

  • Yao W, Bruenn JA (1995) Interference with replication of two double-stranded RNA viruses by production of N-terminal fragments of capsid polypeptides. Virology 214:215–221

    Article  PubMed  CAS  Google Scholar 

  • Yao W, Muqtadir K, Bruenn JA (1995) Packaging in a yeast double-stranded RNA virus. J Virol 69:1917–1919

    PubMed  CAS  Google Scholar 

  • Yao W-S, Adelman K, Bruenn JA (1997) In vitro selection of packaging sites in a double-stranded RNA virus. J Virol 71:2157–2162

    PubMed  CAS  Google Scholar 

  • Yie Y, Zhao F, Zhao SZ, Liu YZ, Liu YL, Tien P (1992) High resistance to cucumber mosaic virus conferred by satellite RNA and coat protein in transgenic commercial tobacco cultivar G-140. Mol Plant Microbe Interact 5:460–465

    Article  PubMed  CAS  Google Scholar 

  • Yoshida S, Maruyama S, Nozaki H, Shirasu K (2010) Horizontal gene transfer by the parasitic plant Striga hermonthica. Science 328:1128

    Article  PubMed  CAS  Google Scholar 

  • Zhu H, Bussey H (1991) Mutational analysis of the functional domains of yeast k1 killer toxin. Mol Cell Biol 11:175–181

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biological Sciences, The State University of New York at Buffalo, Buffalo, NY, 14260, USA

    Jeremy Bruenn

Authors
  1. Jeremy Bruenn
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jeremy Bruenn .

Editor information

Editors and Affiliations

  1. Telos - Philosophische Praxis, Vogelsangstr. 18c, Bürmoos, 5111, Austria

    Günther Witzany

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Bruenn, J. (2012). Genes from Double-Stranded RNA Viruses in the Nuclear Genomes of Fungi. In: Witzany, G. (eds) Biocommunication of Fungi. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-4264-2_5

Download citation

Publish with us

Policies and ethics

Search

Navigation