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Endornaviruses: persistent dsRNA viruses with symbiotic properties in diverse eukaryotes

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Abstract

Endornaviruses are unique, persistent, double-stranded RNA (dsRNA) viruses with symbiotic properties that infect diverse eukaryotes, such as plants, fungi, and oomycetes. Endornaviruses contain a linear dsRNA genome of approximately 10 to 17 kbp in length and are classified in the family Endornaviridae, which consists of two genera, Alphaendornavirus and Betaendornavirus. The endornaviruses encode a single long open reading frame encoding approximately 3200 to 5800 amino acid residues of conserved viral RNA helicase and RNA-dependent RNA polymerase domains, and some endornaviruses contain a site-specific nick in the coding strand of their dsRNA genome. Acute plant viruses propagate rapidly and systemically, eventually killing the host plant, and are then transmitted horizontally. In contrast, plant endornaviruses have several common persistent (symbiotic) properties: a stable low copy number in the host plant, no obvious effect on the host plant, and efficient vertical transmission via gametes. Plant endornaviruses are likely maintained within host plants for hundreds of generations, so the host must stringently regulate their propagation. Whereas RNA silencing functions as a defense system against acute viruses in plants, it may be necessary for the persistent infection (symbiotic life cycle) of endornaviruses. This process includes the stringent regulation of low virus copy number (steady replication before every host cell division) and efficient vertical transmission of the virus to the next generation.

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References

  1. Dodds JA, Morris TJ, Jordan RL (1984) Plant viral double-stranded RNA. Annu Rev Phytopathol 22:151–168

    Article  CAS  Google Scholar 

  2. Boccardo G, Lisa V, Luisini E, Milne RG (1987) Cryptic plant viruses. Adv Virus Res 32:171–214

    Article  CAS  PubMed  Google Scholar 

  3. Brown GG, Finnegan PM (1989) RNA plasmids. Int Rev Cytol 117:1–56

    Article  CAS  PubMed  Google Scholar 

  4. Natsuaki T, Yamashita S, Doi Y, Yora K (1979) Ann Phytopath Soc Japan 45:313–320

  5. Valverde RA, Nameth S, Abdallha O, Al-Musa O, Desjardins P, Dodds JA (1990) Indigenous double-stranded RNA from pepper (Capsicum annuum). Plant Sci 67:195–201

    Article  CAS  Google Scholar 

  6. Fukuhara T, Moriyama H, Pak JK, Hyakutake T, Nitta T (1993) Enigmatic double-stranded RNA in Japonica rice. Plant Mol Biol 21:1121–1130

    Article  CAS  PubMed  Google Scholar 

  7. Ghabrial SA, Nibert ML, Maiss E, Lesker T, Baker TS, Tao YJ (2012) Family partitiviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy: ninth report of the International Committee on Taxonomy of Viruses. Elsevier, San Diego, pp 523–534

    Google Scholar 

  8. Fukuhara T, Gibbs MJ (2012) Family endornaviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy: ninth report of the International Committee on Taxonomy of Viruses. Elsevier, San Diego, pp 519–521

    Google Scholar 

  9. Wakarchuk DA, Hamilton RI (1985) Cellular double-stranded RNA in Phaseolus vulgaris. Plant Mol Biol 5:55–63

    Article  CAS  PubMed  Google Scholar 

  10. Zabalgogeazcoa IA, Gildow FE (1992) Double-stranded ribonucleic acid in ‘Barsoy’ barley. Plant Sci 83:187–194

    Article  CAS  Google Scholar 

  11. Wakarchuk DA, Hamilton RI (1990) Partial nucleotide sequence from enigmatic dsRNAs in Phaseolus vulgaris. Plant Mol Biol 14:637–639

    Article  CAS  PubMed  Google Scholar 

  12. Pfeiffer P (1998) Nucleotide sequence, genetic organization and expression strategy of the double-stranded RNA associated with the ‘447’ cytoplasmic male sterility in Vicia faba. J Gen Virol 79:2349–2358

    Article  CAS  PubMed  Google Scholar 

  13. Moriyama H, Nitta T, Fukuhara T (1995) Double-stranded RNA in rice: a novel RNA replicon in plants. Mol Gen Genet 248:364–369

    Article  CAS  PubMed  Google Scholar 

  14. Moriyama H, Horiuchi H, Koga R, Fukuhara T (1999) Molecular characterization of two endogenous double-stranded RNAs in rice and their inheritance by interspecific hybrids. J Biol Chem 274:6882–6888

    Article  CAS  PubMed  Google Scholar 

  15. Gibbs MJ, Koga K, Moriyama H, Pfeiffer P, Fukuhara T (2000) Phylogenetic analysis of some large double-stranded RNA replicons from plants suggests they evolved from a defective single-stranded RNA virus. J Gen Virol 81:227–233

    Article  CAS  PubMed  Google Scholar 

  16. Gibbs MJ, Pfeiffer P, Fukuhara T (2005) Genus Endornavirus. In: Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (eds) Virus taxonomy: Eighth report of the International Committee on Taxonomy of Viruses. Elsevier, San Diego, pp 603–605

    Google Scholar 

  17. Ghabrial S, Suzuki N (2009) Viruses of plant pathogenic fungi. Annu Rev Phytopathol 47:353–384

    Article  CAS  PubMed  Google Scholar 

  18. Dolja VV, Koonin EV (2012) Capsid-Less RNA Viruses. Wiley, Chichester. https://doi.org/10.1002/9780470015902.a0023269

  19. Khalifa ME, Pearson MN (2014) Molecular characterization of an endornavirus infecting the phytopathogen Sclerotinia sclerotiorum. Virus Res 189:303–309

    Article  CAS  PubMed  Google Scholar 

  20. Edwardson JR, Bond DA, Christie RG (1976) Cytoplasmic sterility factors in Vicia faba L. Genetics 82:443–449

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Grill LK, Garger SJ (1981) Identification and characterization of double-stranded RNA associated with cytoplasmic male sterility in Vicia faba. Proc Natl Acad Sci USA 78:7043–7046

    Article  CAS  PubMed  Google Scholar 

  22. Turpen T, Garger SJ, Grill LK (1988) On the mechanism of cytoplasmic male sterility in the 447 line of Vicia faba. Plant Mol Biol 10:489–497

    Article  CAS  PubMed  Google Scholar 

  23. Moriyama H, Horiuchi H, Nitta T, Fukuhara T (1999) Unusual inheritance of evolutionarily-related double-stranded RNAs in interspecific hybrid between rice plants Oryza sativa and Oryza rufipogon. Plant Mol Biol 39:1127–1136

    Article  CAS  PubMed  Google Scholar 

  24. Horiuchi H, Moriyama H, Fukuhara T (2003) Inheritance of Oryza sativa endornavirus in F1 and F2 hybrids between japonica and indica rice. Genes Genet Syst 78:229–234

    Article  CAS  PubMed  Google Scholar 

  25. Moriyama H, Kanaya K, Wang JZ, Nitta T, Fukuhara T (1996) Stringently and developmentally regulated levels of a cytoplasmic double-stranded RNA and its high-efficiency transmission via egg and pollen in rice. Plant Mol Biol 31:713–719

    Article  CAS  PubMed  Google Scholar 

  26. Zabalgogeazcoa IA, Cox-Fostre DC, Gildow FE (1993) Pedigree analysis of the transmission of a double-stranded RNA in barley cultivars. Plant Sci 91:45–53

    Article  CAS  Google Scholar 

  27. Candresse T, Marais A, Sorrentino R, Faure C, Theil S, Cadot V, Rolland M, Villemot J, Rabenstein F (2016) Complete genomic sequence of barley (Hordeum vulgare) endornavirus (HvEV) determined by next-generation sequencing. Arch Virol 161:741–743

    Article  CAS  PubMed  Google Scholar 

  28. Mackenzie SA, Pring DR, Bassett MJ (1988) Large double-stranded RNA molecules in Phaseolus vulgaris L. are not associated with cytoplasmic male sterility. Theor Appl Genet 76:59–63

    Article  CAS  PubMed  Google Scholar 

  29. Okada R, Yong CK, Valverde RA, Sabanadzovic S, Aoki N, Hotate S, Kiyota E, Moriyama H, Fukuhara T (2013) Molecular characterization of two evolutionally distinct endornaviruses co-infecting common bean (Phaseolus vulgaris). J Gen Virol 94:2191–2199

    Article  CAS  Google Scholar 

  30. Valverde RA, Fontenot JF (1991) Variation in double-stranded ribonucleic acid among pepper cultivars. J Am Soc Hort Sci 116:903–905

    Article  CAS  Google Scholar 

  31. Okada R, Kiyota E, Sabanadzovic S, Moriyama H, Fukuhara T, Saha P, Roossinck MJ, Severin A, Valverde RA (2011) Bell pepper endornavirus: molecular and biological properties and occurrence in the genus Capsicum. J Gen Virol 92:2664–2673

    Article  CAS  PubMed  Google Scholar 

  32. Lim S, Kim KH, Zhao F, Yoo RH, Igori D, Lee S-H, Moon JS (2015) Complete genome sequence of a novel endornavirus isolated from hot pepper. Arch Virol 160:3153–3156

    Article  CAS  PubMed  Google Scholar 

  33. Coutts RHA (2005) First report of an endornavirus in the Cucurbitaceae. Virus Genes 31:361–362

    Article  CAS  PubMed  Google Scholar 

  34. Sabanadzovic S, Wintermantel WM, Valverde RA, McCreight JD, Aboughanem-Sabanadzovic N (2016) Cucumis melo endornavirus: genome organization, host range and co-divergence with the host. Virus Res 214:49–58

    Article  CAS  PubMed  Google Scholar 

  35. Fukuhara T, Koga R, Aoki N, Yuki C, Yamamoto N, Oyama N, Udagawa T, Horiuchi H, Miyazaki S, Higashi Y, Takeshita M, Ikeda K, Arakawa M, Matsumoto N, Moriyama H (2006) The wide distribution of endornaviruses, large double-stranded RNA replicons with plasmid-like properties. Arch Virol 151:995–1002

    Article  CAS  PubMed  Google Scholar 

  36. Kwon S-J, Tan S, Vidalakis G (2014) Complete genome sequence and genome organization of an endornavirus from bottle gourd (Lagenaria siceraria) in California U. S. A. Virus Genes 49:163–168

    Article  CAS  PubMed  Google Scholar 

  37. Peng X, Pan H, Muhammad A, An H, Fang S, Li W, Zhang S (2018) Complete genome sequence of a new strain of Lagenaria siceraria endornavirus from China. Arch Virol 163:805–808

    Article  CAS  PubMed  Google Scholar 

  38. Villanueva F, Sabanadzovic S, Valverde RA, Navas-Castillo J (2012) Complete genome sequence of a double-stranded RNA virus from avocado. J Virol 86:1282–1283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Khankhum S, Valverde RA (2018) Physiological traits of endornavirus-infected and endornavirus-free common bean (Phaseolus vulgaris) cv Black Turtle Soup. Arch Virol 163:1051–1056

    Article  CAS  PubMed  Google Scholar 

  40. Nuss DL, Koltin Y (1990) Significance of dsRNA genetic elements in plant pathogenic fungi. Annu Rev Phytopathol 28:37–58

    Article  CAS  PubMed  Google Scholar 

  41. Ghabrial SA (1994) New developments in fungal virology. Adv Virus Res 43:303–388

    Article  CAS  PubMed  Google Scholar 

  42. Ghabrial SA, Castón JR, Jiang D, Nibert ML, Suzuki N (2015) 50-plus years of fungal viruses. Virology 479–480:356–368

    Article  CAS  PubMed  Google Scholar 

  43. Osaki H, Nakamura H, Sasaki A, Matsumoto N, Yoshida K (2006) An endornavirus from a hypovirulent strain of the violet root rot fungus, Helicobasidium mompa. Virus Res 118:143–149

    Article  CAS  PubMed  Google Scholar 

  44. Hacker CV, Brasier CM, Buck KW (2005) A double-stranded RNA from a Phytophthora species is related to the plant endornaviruses and contains a putative UDP glycosyltransferase gene. J Gen Virol 86:1561–1570

    Article  CAS  PubMed  Google Scholar 

  45. Liu H, Fu Y, Xie J, Cheng J, Ghabrial SA, Li G, Yi X, Jiang D (2012) Discovery of novel dsRNA viral sequences by in silico cloning and implications for viral diversity, host range and evolution. PLoS ONE 7:e42147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Wylie SJ, Adams M, Chalam C, Kreuze J, López-Moya JJ, Ohshima K, Praveen S, Rabenstein F, Stenger D, Wang A, Zerbini FM, ICTV Report Consortium (2017) ICTV Virus Taxonomy Profile: Potyviridae. J Gen Virol 98:352–354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Pfeiffer P, Jung JL, Heitzler J, Keith G (1993) Unusual structure of the double-stranded RNA associated with the ‘447’ cytoplasmic male sterility in Vicia faba. J Gen Virol 74:1167–1173

    Article  CAS  PubMed  Google Scholar 

  48. Fukuhara T, Moriyama H, Nitta T (1995) The unusual structure of a novel RNA replicon in rice. J Biol Chem 270:18147–18149

    Article  CAS  PubMed  Google Scholar 

  49. Lefebvre A, Scalla R, Pfeiffer P (1990) The double-stranded RNA associated with the `447′ cytoplasmic male sterility in Vicia faba is packaged together with its replicase in cytoplasmic membranous vesicles. Plant Mol Biol 14:477–490

    Article  CAS  PubMed  Google Scholar 

  50. Horiuchi H, Udagawa T, Koga K, Moriyama H, Fukuhara T (2001) RNA-dependent RNA polymerase activity associated with endogenous double-stranded RNA in rice. Plant Cell Physiol 42:197–203

    Article  CAS  PubMed  Google Scholar 

  51. Napoli C, Lemieux C, Jorgensen R (1990) Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2:279–289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–811

    Article  CAS  Google Scholar 

  53. Romano N, Macino G (1992) Quelling: transient inactivation of gene expression in Neurospora crassa by transformation with homologous sequences. Mol Microbiol 6:3343–3353

    Article  CAS  PubMed  Google Scholar 

  54. Baulcombe D (2004) RNA silencing in plants. Nature 431:356–363

    Article  CAS  PubMed  Google Scholar 

  55. Lindbo JA, Dougherty WG (2005) Plant pathology and RNAi: a brief history. Annu Rev Phytopathol 43:191–204

    Article  CAS  PubMed  Google Scholar 

  56. Henderson IR, Zhang X, Lu C, Johnson L, Meyers BC, Green PJ et al (2006) Dissecting Arabidopsis thaliana DICER function in small RNA processing, gene silencing and DNA methylation patterning. Nat Genet 38:721–725

    Article  CAS  PubMed  Google Scholar 

  57. Fukudome A, Fukuhara T (2017) Plant Dicer-like proteins: double-stranded RNA-cleaving enzymes for small RNA biogenesis. J Plant Res 130:33–44

    Article  CAS  PubMed  Google Scholar 

  58. Fagard M, Boutet S, Morel JB, Bellini C, Vaucheret H (2000) AGO1, QDE-2, and RDE-1 are related proteins required for post-transcriptional gene silencing in plants, quelling in fungi, and RNA interference in animals. Proc Natl Acad Sci USA 97:11650–11654

    Article  CAS  PubMed  Google Scholar 

  59. Baumberger N, Baulcombe DC (2005) Arabidopsis ARGONAUTE1 is an RNA Slicer that selectively recruits microRNAs and short interfering RNAs. Proc Natl Acad Sci USA 102:11928–11933

    Article  CAS  PubMed  Google Scholar 

  60. Bouche N, Lauressergues D, Gasciolli V, Vaucheret H (2006) An antagonistic function for Arabidopsis DCL2 in development and a new function for DCL4 in generating viral siRNAs. EMBO J 25:3347–3356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Donaire L, Wang Y, Gonzalez-Ibeas D, Mayer KF, Aranda MA, Llave C (2009) Deep-sequencing of plant viral small RNAs reveals effective and widespread targeting of viral genomes. Virology 392:203–214

    Article  CAS  PubMed  Google Scholar 

  62. Nagano H, Fukudome A, Hiraguri A, Moriyama H, Fukuhara T (2014) Distinct substrate specificities of Arabidopsis DCL3 and DCL4. Nucleic Acids Res 42:1845–1856

    Article  CAS  PubMed  Google Scholar 

  63. Wang XB, Jovel J, Udomporn P, Wang Y, Wu Q, Li WX, Gasciolli V, Vaucheret H, Ding SW (2011) The 21-nucleotide, but not 22-nucleotide, viral secondary small interfering RNAs direct potent antiviral defense by two cooperative argonautes in Arabidopsis thaliana. Plant Cell 23:1625–1638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Garcia-Ruiz H, Carbonell A, Hoyer JS, Fahlgren N, Gilbert KB, Takeda A, Giampetruzzi A, Garcia Ruiz MT, McGinn MG, Lowery N, Martinez Baladejo MT, Carrington JC (2015) Roles and programming of Arabidopsis ARGONAUTE proteins during Turnip mosaic virus infection. PLoS Pathog 11:e1004755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Kasschau KD, Carrington JC (1998) A counterdefensive strategy of plant viruses: suppression of posttranscriptional gene silencing. Cell 95:461–470

    Article  CAS  PubMed  Google Scholar 

  66. Roth BM, Pruss GJ, Vance VB (2004) Plant viral suppressors of RNA silencing. Virus Res 102:97–108

    Article  CAS  PubMed  Google Scholar 

  67. Csorba T, Kontra L, Burgyán J (2015) Viral silencing suppressors: tools forged to fine-tune host-pathogen coexistence. Virology 479–480:85–103

    Article  CAS  PubMed  Google Scholar 

  68. Urayama S, Moriyama H, Aoki N, Nakazawa Y, Okada R, Kiyota E, Miki D, Shimamoto K, Fukuhara T (2010) Knock-down of OsDCL2 in rice negatively affects maintenance of the endogenous dsRNA virus, Oryza sativa endornavirus. Plant Cell Physiol 51:58–67

    Article  CAS  PubMed  Google Scholar 

  69. Sela N, Luria N, Dombrovsky A (2012) Genome assembly of bell pepper endornavirus from small RNA. J Virol 86:7721

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Nordenstedt N, Marcenaro D, Chilagane D, Mwaipopo B, Rajamäki ML, Nchimbi-Msolla S, Njau PJR, Mbanzibwa DR, Valkonen JPT (2017) Pathogenic seedborne viruses are rare but Phaseolus vulgaris endornaviruses are common in bean varieties grown in Nicaragua and Tanzania. PLoS ONE 12:e0178242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Manche L, Green SR, Schmedt C, Mathews MB (1992) Interactions between double-stranded RNA regulators and the protein kinase DAI. Mol Cell Biol 12:5238–5248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Stark GR, Kerr IM, Williams BR, Silverman RH, Schreiber RD (1998) How cells respond to interferons. Annu Rev Biochem 67:227–264

    Article  CAS  Google Scholar 

  73. Okada R, Kiyota E, Moriyama H, Fukuhara T, Valverde RA (2014) A new endornavirus species infecting Malabar spinach (Basella alba L.). Arch Virol 159:807–809

    Article  CAS  PubMed  Google Scholar 

  74. Okada R, Kiyota K, Moriyama H, Fukuhara T, Valverde RA (2017) Molecular and biological properties of an endornavirus infecting winged bean (Psophocarpus tetragonolobus). Virus Genes 53:141–145

    Article  CAS  PubMed  Google Scholar 

  75. Debat HJ, Grabiale M, Aguilera PM, Bubillo R, Zapata PD, Marti DA, Ducasse DA (2014) The complete genome of a putative endornavirus identified in yerba mate (Ilex paraguariensis St. Hil.). Virus Genes 49:348–350

    Article  CAS  PubMed  Google Scholar 

  76. Du Z, Lin W, Qiu P, Liu X, Guo L, Wu K, Zhang S, Wu Z (2016) Complete sequence of a double-stranded RNA from the phytopathogenic fungus Erysiphe cichoracearum that might represent a novel endornavirus. Arch Virol 161:2343–2346

    Article  CAS  PubMed  Google Scholar 

  77. Espach Y, Maree HJ, Burger JT (2012) Complete genome of a novel endornavirus assembled from next-generation sequence data. J Virol 86:13142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Li W, Zhang T, Sun H, Deng Y, Zhang A, Chen H, Wang K (2014) Complete genome sequence of a novel endornavirus in the wheat sharp eyespot pathogen Rhizoctonia cerealis. Arch Virol 159:1213–1216

    Article  CAS  PubMed  Google Scholar 

  79. Shang HH, Zhong J, Zhang RJ, Chen CY, Gao BD, Zhu HJ (2015) Genome sequence of a novel endornavirus from the phytopathogenic fungus Alternaria brassicicola. Arch Virol 160:1827–1830

    Article  CAS  PubMed  Google Scholar 

  80. Hao F, Zhou Z, Wu M, Li G (2017) Molecular characterization of a novel endornavirus from the phytopathogenic fungus Botritis cinerea. Arch Virol 162:313–316

    Article  CAS  PubMed  Google Scholar 

  81. Tuomivirta TT, Kaitera J, Hantula J (2009) A novel putative virus of Gremmeniella abietina type B (Ascomycota: Helotiaceae) has a composite genome with endornavirus affinities. J Gen Virol 90:2299–2305

    Article  CAS  PubMed  Google Scholar 

  82. Stielow B, Klenk HP, Menzel W (2011) Complete genome sequence of the first endornavirus from the ascocarp of the ectomycorrhizal fungus Tuber aestivum Vittad. Arch Virol 156:343–345

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The author thanks Ms. Midori Tabara (Tokyo University of Agriculture and Technology) for her critical reading of the manuscript. This work was supported by the Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan (Grants-in-Aid for Scientific Research on Innovative Areas [Nos. 16H06435, 16H06429 and 16H21723] to T.F.).

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Fukuhara, T. Endornaviruses: persistent dsRNA viruses with symbiotic properties in diverse eukaryotes. Virus Genes 55, 165–173 (2019). https://doi.org/10.1007/s11262-019-01635-5

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