1932

Abstract

The large genetic and structural divergences between plants and fungi may hinder the transmission of viruses between these two kingdoms to some extent. However, recent accumulating evidence from virus phylogenetic analyses and the discovery of naturally occurring virus cross-infection suggest the occurrence of past and current transmissions of viruses between plants and plant-associated fungi. Moreover, artificial virus inoculation experiments showed that diverse plant viruses can multiply in fungi and vice versa. Thus, virus cross-infection between plants and fungi may play an important role in the spread, emergence, and evolution of both plant and fungal viruses and facilitate the interaction between them. In this review, we summarize current knowledge related to cross-kingdom virus infection in plants and fungi and further discuss the relevance of this new virological topic in the context of understanding virus spread and transmission in nature as well as developing control strategies for crop plant diseases.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-111821-122539
2023-09-29
2024-07-15
Loading full text...

Full text loading...

/deliver/fulltext/virology/10/1/annurev-virology-111821-122539.html?itemId=/content/journals/10.1146/annurev-virology-111821-122539&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Van der Want J, Dijkstra J. 2006. A history of plant virology. Arch. Virol. 151:1467–98
    [Google Scholar]
  2. 2.
    Short SM, Staniewski MA, Chaban YV, Long AM, Wang D. 2020. Diversity of viruses infecting eukaryotic algae. Curr. Issues Mol. Biol. 39:29–62
    [Google Scholar]
  3. 3.
    Hull R. 2013. Plant Virology London: Academic. , 5th ed..
    [Google Scholar]
  4. 4.
    Roossinck MJ, Martin DP, Roumagnac P. 2015. Plant virus metagenomics: advances in virus discovery. Phytopathology 105:716–27
    [Google Scholar]
  5. 5.
    Hasiów-Jaroszewska B, Boezen D, Zwart MP. 2021. Metagenomic studies of viruses in weeds and wild plants: a powerful approach to characterise variable virus communities. Viruses 13:1939
    [Google Scholar]
  6. 6.
    Susi H, Filloux D, Frilander MJ, Roumagnac P, Laine A-L. 2019. Diverse and variable virus communities in wild plant populations revealed by metagenomic tools. PeerJ 7:e6140
    [Google Scholar]
  7. 7.
    Stobbe AH, Roossinck MJ. 2014. Plant virus metagenomics: what we know and why we need to know more. Front. Plant Sci. 5:150
    [Google Scholar]
  8. 8.
    Roossinck MJ. 2019. Viruses in the phytobiome. Curr. Opin. Virol. 37:72–76
    [Google Scholar]
  9. 9.
    Zhang Y-Z, Shi M, Holmes EC. 2018. Using metagenomics to characterize an expanding virosphere. Cell 172:1168–72
    [Google Scholar]
  10. 10.
    Hogenhout SA, Ammar E-D, Whitfield AE, Redinbaugh MG. 2008. Insect vector interactions with persistently transmitted viruses. Annu. Rev. Phytopathol. 46:327–59
    [Google Scholar]
  11. 11.
    Whitfield AE, Falk BW, Rotenberg D. 2015. Insect vector-mediated transmission of plant viruses. Virology 479:278–89
    [Google Scholar]
  12. 12.
    Whitfield AE, Huot OB, Martin KM, Kondo H, Dietzgen RG. 2018. Plant rhabdoviruses—their origins and vector interactions. Curr. Opin. Virol. 33:198–207
    [Google Scholar]
  13. 13.
    Andika IB, Kondo H, Sun L. 2016. Interplays between soil-borne plant viruses and RNA silencing-mediated antiviral defense in roots. Front. Microbiol. 7:1458
    [Google Scholar]
  14. 14.
    Bragard C, Caciagli P, Lemaire O, Lopez-Moya J, MacFarlane S et al. 2013. Status and prospects of plant virus control through interference with vector transmission. Annu. Rev. Phytopathol. 51:177–201
    [Google Scholar]
  15. 15.
    Campbell R. 1996. Fungal transmission of plant viruses. Annu. Rev. Phytopathol. 34:87–108
    [Google Scholar]
  16. 16.
    Galbraith DA, Fuller ZL, Ray AM, Brockmann A, Frazier M et al. 2018. Investigating the viral ecology of global bee communities with high-throughput metagenomics. Sci. Rep. 8:8879
    [Google Scholar]
  17. 17.
    He B, Li Z, Yang F, Zheng J, Feng Y et al. 2013. Virome profiling of bats from Myanmar by metagenomic analysis of tissue samples reveals more novel mammalian viruses. PLOS ONE 8:e61950
    [Google Scholar]
  18. 18.
    Ng TFF, Willner DL, Lim YW, Schmieder R, Chau B et al. 2011. Broad surveys of DNA viral diversity obtained through viral metagenomics of mosquitoes. PLOS ONE 6:e20579
    [Google Scholar]
  19. 19.
    Shi M, Lin X-D, Tian J-H, Chen L-J, Chen X et al. 2016. Redefining the invertebrate RNA virosphere. Nature 540:539–43
    [Google Scholar]
  20. 20.
    Dacheux L, Cervantes-Gonzalez M, Guigon G, Thiberge J-M, Vandenbogaert M et al. 2014. A preliminary study of viral metagenomics of French bat species in contact with humans: identification of new mammalian viruses. PLOS ONE 9:e87194
    [Google Scholar]
  21. 21.
    Ghabrial SA, Suzuki N. 2009. Viruses of plant pathogenic fungi. Annu. Rev. Phytopathol. 47:353–84
    [Google Scholar]
  22. 22.
    Ghabrial SA, Castón JR, Jiang D, Nibert ML, Suzuki N. 2015. 50-plus years of fungal viruses. Virology 479:356–68
    [Google Scholar]
  23. 23.
    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. 150:545–51
    [Google Scholar]
  24. 24.
    Wickner RB. 1996. Double-stranded RNA viruses of Saccharomyces cerevisiae. Microbiol. Rev. 60:250–65
    [Google Scholar]
  25. 25.
    Bostian KA, Hopper JE, Rogers DT, Tipper DJ. 1980. Translational analysis of the killer-associated virus-like particle dsRNA genome of S. cerevisiae: M dsRNA encodes toxin. Cell 19:403–14
    [Google Scholar]
  26. 26.
    Bevan E, Herring A, Mitchell DJ. 1973. Preliminary characterization of two species of dsRNA in yeast and their relationship to the “killer” character. Nature 245:81–86
    [Google Scholar]
  27. 27.
    Lampson G, Tytell A, Field A, Nemes M, Hilleman M. 1967. Inducers of interferon and host resistance. I. Double-stranded RNA from extracts of Penicillium funiculosum. PNAS 58:782–89
    [Google Scholar]
  28. 28.
    Jiang D, Ghabrial SA. 2004. Molecular characterization of Penicillium chrysogenum virus: reconsideration of the taxonomy of the genus Chrysovirus. J. Gen. Virol. 85:2111–21
    [Google Scholar]
  29. 29.
    Heiniger U, Rigling D. 1994. Biological control of chestnut blight in Europe. Annu. Rev. Phytopathol. 32:581–99
    [Google Scholar]
  30. 30.
    Shapira R, Choi GH, Nuss DL. 1991. Virus-like genetic organization and expression strategy for a double-stranded RNA genetic element associated with biological control of chestnut blight. EMBO J. 10:731–39
    [Google Scholar]
  31. 31.
    Xie J, Jiang D. 2014. New insights into mycoviruses and exploration for the biological control of crop fungal diseases. Annu. Rev. Phytopathol. 52:45–68
    [Google Scholar]
  32. 32.
    Choi GH, Nuss DL. 1992. Hypovirulence of chestnut blight fungus conferred by an infectious viral cDNA. Science 257:800–3
    [Google Scholar]
  33. 33.
    Kondo H, Botella L, Suzuki N. 2022. Mycovirus diversity and evolution revealed/inferred from recent studies. Annu. Rev. Phytopathol. 60:307–36
    [Google Scholar]
  34. 34.
    Thapa V, Roossinck MJ. 2019. Determinants of coinfection in the mycoviruses. Front. Cell. Infect. Microbiol. 9:169
    [Google Scholar]
  35. 35.
    Roossinck MJ. 2019. Evolutionary and ecological links between plant and fungal viruses. New Phytol. 221:86–92
    [Google Scholar]
  36. 36.
    Hillman BI, Annisa A, Suzuki N. 2018. Viruses of plant-interacting fungi. Adv. Virus Res. 100:99–116
    [Google Scholar]
  37. 37.
    Sun L, Kondo H, Andika IB 2021. Cross-kingdom virus infection. Encyclopedia of Virology D Bamford, M Zuckerman 443–44. Amsterdam: Elsevier. , 4th ed..
    [Google Scholar]
  38. 38.
    Cao X, Liu J, Pang J, Kondo H, Chi S et al. 2022. Common but nonpersistent acquisitions of plant viruses by plant-associated fungi. Viruses 14:2279
    [Google Scholar]
  39. 39.
    Andika IB, Wei S, Cao C, Salaipeth L, Kondo H, Sun L. 2017. Phytopathogenic fungus hosts a plant virus: a naturally occurring cross-kingdom viral infection. PNAS 114:12267–72
    [Google Scholar]
  40. 40.
    Forgia M, Navarro B, Daghino S, Cervera A, Gisel A et al. 2023. Hybrids of RNA viruses and viroid-like elements replicate in fungi. Nat. Commun. 14:2591
    [Google Scholar]
  41. 41.
    Dong K, Xu C, Kotta-Loizou I, Jiang J, Lv R et al. 2023. Novel viroid-like RNAs naturally infect a filamentous fungus. Adv. Sci. 10:2204308
    [Google Scholar]
  42. 42.
    Lee BD, Neri U, Roux S, Wolf YI, Camargo AP et al. 2023. Mining metatranscriptomes reveals a vast world of viroid-like circular RNAs. Cell 186:646–61
    [Google Scholar]
  43. 43.
    Roossinck MJ. 2010. Lifestyles of plant viruses. Philos. Trans. R. Soc. B 365:1899–905
    [Google Scholar]
  44. 44.
    Xie J, Wei D, Jiang D, Fu Y, Li G et al. 2006. Characterization of debilitation-associated mycovirus infecting the plant-pathogenic fungus Sclerotinia sclerotiorum. J. Gen. Virol. 87:241–49
    [Google Scholar]
  45. 45.
    Howitt RL, Beever RE, Pearson MN, Forster RL. 2001. Genome characterization of Botrytis virus F, a flexuous rod-shaped mycovirus resembling plant ‘potex-like’ viruses. J. Gen. Virol. 82:67–78
    [Google Scholar]
  46. 46.
    Howitt R, Beever R, Pearson M, Forster R. 2006. Genome characterization of a flexuous rod-shaped mycovirus, Botrytis virus X, reveals high amino acid identity to genes from plant ‘potex-like’ viruses. Arch. Virol. 151:563–79
    [Google Scholar]
  47. 47.
    Lin Y-H, Fujita M, Chiba S, Hyodo K, Andika IB et al. 2019. Two novel fungal negative-strand RNA viruses related to mymonaviruses and phenuiviruses in the shiitake mushroom (Lentinula edodes). Virology 533:125–36
    [Google Scholar]
  48. 48.
    Varsani A, Krupovic M. 2021. Family Genomoviridae: 2021 taxonomy update. Arch. Virol. 166:2911–26
    [Google Scholar]
  49. 49.
    Kazlauskas D, Varsani A, Koonin EV, Krupovic M. 2019. Multiple origins of prokaryotic and eukaryotic single-stranded DNA viruses from bacterial and archaeal plasmids. Nat. Commun. 10:3425
    [Google Scholar]
  50. 50.
    Lefeuvre P, Martin DP, Elena SF, Shepherd DN, Roumagnac P, Varsani A. 2019. Evolution and ecology of plant viruses. Nat. Rev. Microbiol. 17:632–44
    [Google Scholar]
  51. 51.
    Ryabov EV, Taliansky ME 2020. Umbraviruses (Calvusvirinae, Tombusviridae). Encyclopedia of Virology D Bamford, M Zuckerman 827–32. Amsterdam: Elsevier. , 4th ed..
    [Google Scholar]
  52. 52.
    Zhang R, Hisano S, Tani A, Kondo H, Kanematsu S, Suzuki N. 2016. A capsidless ssRNA virus hosted by an unrelated dsRNA virus. Nat. Microbiol. 1:15001
    [Google Scholar]
  53. 53.
    Jia J, Mu F, Fu Y, Cheng J, Lin Y et al. 2022. A capsidless virus is trans-encapsidated by a bisegmented botybirnavirus. J. Virol. 96:e00296–22
    [Google Scholar]
  54. 54.
    Sato Y, Hisano S, López-Herrera CJ, Kondo H, Suzuki N. 2022. Three-layered complex interactions among capsidless (+)ssRNA yadokariviruses, dsRNA viruses, and a fungus. mBio 13:e01685–22
    [Google Scholar]
  55. 55.
    Lucas WJ. 2006. Plant viral movement proteins: agents for cell-to-cell trafficking of viral genomes. Virology 344:169–84
    [Google Scholar]
  56. 56.
    Liu S, Xie J, Cheng J, Li B, Chen T et al. 2016. Fungal DNA virus infects a mycophagous insect and utilizes it as a transmission vector. PNAS 113:12803–8
    [Google Scholar]
  57. 57.
    Biella S, Smith ML, Aist JR, Cortesi P, Milgroom MG. 2002. Programmed cell death correlates with virus transmission in a filamentous fungus. Proc. R. Soc. B 269:2269–76
    [Google Scholar]
  58. 58.
    Wu S, Cheng J, Fu Y, Chen T, Jiang D et al. 2017. Virus-mediated suppression of host non-self recognition facilitates horizontal transmission of heterologous viruses. PLOS Pathog. 13:e1006234
    [Google Scholar]
  59. 59.
    Ding S-W. 2010. RNA-based antiviral immunity. Nat. Rev. Immunol. 10:632–44
    [Google Scholar]
  60. 60.
    Aliyari R, Ding SW. 2009. RNA-based viral immunity initiated by the Dicer family of host immune receptors. Immunol. Rev. 227:176–88
    [Google Scholar]
  61. 61.
    Segers GC, Zhang X, Deng F, Sun Q, Nuss DL. 2007. Evidence that RNA silencing functions as an antiviral defense mechanism in fungi. PNAS 104:12902–6
    [Google Scholar]
  62. 62.
    Neupane A, Feng C, Mochama PK, Saleem H, Lee Marzano S-Y. 2019. Roles of argonautes and dicers on Sclerotinia sclerotiorum antiviral RNA silencing. Front. Plant Sci. 10:976
    [Google Scholar]
  63. 63.
    Chiba S, Lin Y-H, Kondo H, Kanematsu S, Suzuki N. 2013. A novel victorivirus from a phytopathogenic fungus, Rosellinia necatrix, is infectious as particles and targeted by RNA silencing. J. Virol. 87:6727–38
    [Google Scholar]
  64. 64.
    Chiba S, Suzuki N. 2015. Highly activated RNA silencing via strong induction of dicer by one virus can interfere with the replication of an unrelated virus. PNAS 112:E4911–18
    [Google Scholar]
  65. 65.
    Mochama P, Jadhav P, Neupane A, Lee Marzano S-Y. 2018. Mycoviruses as triggers and targets of RNA silencing in white mold fungus Sclerotinia sclerotiorum. Viruses 10:214
    [Google Scholar]
  66. 66.
    Aulia A, Andika IB, Kondo H, Hillman BI, Suzuki N. 2019. A symptomless hypovirus, CHV4, facilitates stable infection of the chestnut blight fungus by a coinfecting reovirus likely through suppression of antiviral RNA silencing. Virology 533:99–107
    [Google Scholar]
  67. 67.
    Hammond T, Andrewski M, Roossinck M, Keller N. 2008. Aspergillus mycoviruses are targets and suppressors of RNA silencing. Eukaryot. Cell 7:350–57
    [Google Scholar]
  68. 68.
    Andika IB, Jamal A, Kondo H, Suzuki N. 2017. SAGA complex mediates the transcriptional up-regulation of antiviral RNA silencing. PNAS 114:E3499–506
    [Google Scholar]
  69. 69.
    Campo S, Gilbert KB, Carrington JC. 2016. Small RNA-based antiviral defense in the phytopathogenic fungus Colletotrichum higginsianum. PLOS Pathog. 12:e1005640
    [Google Scholar]
  70. 70.
    Aulia A, Hyodo K, Hisano S, Kondo H, Hillman BI, Suzuki N. 2021. Identification of an RNA silencing suppressor encoded by a symptomless fungal hypovirus, Cryphonectria hypovirus 4. Biology 10:100
    [Google Scholar]
  71. 71.
    Shimura H, Kim H, Matsuzawa A, Akino S, Masuta C. 2022. Coat protein of partitiviruses isolated from mycorrhizal fungi functions as an RNA silencing suppressor in plants and fungi. Sci. Rep. 12:7855
    [Google Scholar]
  72. 72.
    Yaegashi H, Yoshikawa N, Ito T, Kanematsu S. 2013. A mycoreovirus suppresses RNA silencing in the white root rot fungus, Rosellinia necatrix. Virology 444:409–16
    [Google Scholar]
  73. 73.
    Wang S, Zhang J, Nzabanita C, Zhang M, Nie J, Guo L. 2022. Fungal virus, FgHV1-encoded p20 suppresses RNA silencing through single-strand small RNA binding. J. Fungi 8:1171
    [Google Scholar]
  74. 74.
    Andika IB, Kondo H, Suzuki N. 2019. Dicer functions transcriptionally and posttranscriptionally in a multilayer antiviral defense. PNAS 116:2274–81
    [Google Scholar]
  75. 75.
    Nienhaus F. 1971. Tobacco mosaic virus strains extracted from conidia of powdery mildews. Virol. 46:504–5
    [Google Scholar]
  76. 76.
    Yarwood C, Hecht-Poinar E. 1973. Viruses from rusts and mildews. Phytopathology 63:1111–15
    [Google Scholar]
  77. 77.
    Janda M, Ahlquist P. 1993. RNA-dependent replication, transcription, and persistence of brome mosaic virus RNA replicons in S. cerevisiae. Cell 72:961–70
    [Google Scholar]
  78. 78.
    Pantaleo V, Rubino L, Russo M. 2003. Replication of Carnation Italian ringspot virus defective interfering RNA in Saccharomyces cerevisiae. J. Virol. 77:2116–23
    [Google Scholar]
  79. 79.
    Nagy PD. 2008. Yeast as a model host to explore plant virus-host interactions. Annu. Rev. Phytopathol. 46:217–42
    [Google Scholar]
  80. 80.
    Navarro B, Russo M, Pantaleo V, Rubino L. 2006. Cytological analysis of Saccharomyces cerevisiae cells supporting cymbidium ringspot virus defective interfering RNA replication. J. Gen. Virol. 87:705–14
    [Google Scholar]
  81. 81.
    Raghavan V, Malik PS, Choudhury NR, Mukherjee SK. 2004. The DNA-A component of a plant geminivirus (Indian mung bean yellow mosaic virus) replicates in budding yeast cells. J. Virol. 78:2405–13
    [Google Scholar]
  82. 82.
    Mascia T, Nigro F, Abdallah A, Ferrara M, De Stradis A et al. 2014. Gene silencing and gene expression in phytopathogenic fungi using a plant virus vector. PNAS 111:4291–96
    [Google Scholar]
  83. 83.
    Mascia T, Labarile R, Doohan F, Gallitelli D. 2019. Tobacco mosaic virus infection triggers an RNAi-based response in Phytophthora infestans. Sci. Rep. 9:2657
    [Google Scholar]
  84. 84.
    Mascia T, Vučurović A, Minutillo S, Nigro F, Labarile R et al. 2019. Infection of Colletotrichum acutatum and Phytophthora infestans by taxonomically different plant viruses. Eur. J. Plant Pathol. 153:1001–17
    [Google Scholar]
  85. 85.
    Bian R, Andika IB, Pang T, Lian Z, Wei S et al. 2020. Facilitative and synergistic interactions between fungal and plant viruses. PNAS 117:3779–88
    [Google Scholar]
  86. 86.
    Flores R, Gago-Zachert S, Serra P, Sanjuán R, Elena SF. 2014. Viroids: survivors from the RNA world?. Annu. Rev. Microbiol. 68:395–414
    [Google Scholar]
  87. 87.
    Moelling K, Broecker F. 2021. Viroids and the origin of life. Int. J. Mol. Sci. 22:3476
    [Google Scholar]
  88. 88.
    Di Serio F, Owens RA, Li S-F, Matoušek J, Pallás V et al. 2021. ICTV virus taxonomy profile: Pospiviroidae. J. Gen. Virol. 102:001543
    [Google Scholar]
  89. 89.
    Di Serio F, Li S-F, Matoušek J, Owens RA, Pallás V et al. 2018. ICTV virus taxonomy profile: Avsunviroidae. J. Gen. Virol. 99:611–12
    [Google Scholar]
  90. 90.
    Flores R, Hernández C, Martínez de Alba AE, Daròs J-A, Serio FD 2005. Viroids and viroid-host interactions. Annu. Rev. Phytopathol. 43:117–39
    [Google Scholar]
  91. 91.
    Kovalskaya N, Hammond RW. 2014. Molecular biology of viroid–host interactions and disease control strategies. Plant Sci. 228:48–60
    [Google Scholar]
  92. 92.
    Delan-Forino C, Maurel M-C, Torchet C. 2011. Replication of avocado sunblotch viroid in the yeast Saccharomyces cerevisiae. J. Virol. 85:3229–38
    [Google Scholar]
  93. 93.
    Latifi A, Bernard C, Da Silva L, Andéol Y, Elleuch A et al. 2016. Replication of avocado sunblotch viroid in the cyanobacterium Nostoc sp. PCC 7120. J. Plant Pathol. Microbiol. 7:4
    [Google Scholar]
  94. 94.
    Wei S, Bian R, Andika IB, Niu E, Liu Q et al. 2019. Symptomatic plant viroid infections in phytopathogenic fungi. PNAS 116:13042–50
    [Google Scholar]
  95. 95.
    Afanasenko O, Khiutti A, Mironenko N, Lashina N. 2022. Transmission of potato spindle tuber viroid between Phytophthora infestans and host plants. Vavilovskii Zhurnal Genet. Sel. 26:272–80
    [Google Scholar]
  96. 96.
    Wei S, Bian R, Andika IB, Niu E, Liu Q et al. 2020. Reply to Serra et al.: nucleotide substitutions in plant viroid genomes that multiply in phytopathogenic fungi. PNAS 117:10129–30
    [Google Scholar]
  97. 97.
    Tian M, Wei S, Bian R, Luo J, Khan HA et al. 2022. Natural cross-kingdom spread of apple scar skin viroid from apple trees to fungi. Cells 11:3686
    [Google Scholar]
  98. 98.
    Nakayashiki H, Kadotani N, Mayama S. 2006. Evolution and diversification of RNA silencing proteins in fungi. J. Mol. Evol. 63:127–35
    [Google Scholar]
  99. 99.
    Pang T, Peng J, Bian R, Liu Y, Zhang D et al. 2022. Similar characteristics of siRNAs of plant viruses which replicate in plant and fungal hosts. Biology 11:1672
    [Google Scholar]
  100. 100.
    Nerva L, Varese G, Falk B, Turina M. 2017. Mycoviruses of an endophytic fungus can replicate in plant cells: evolutionary implications. Sci. Rep. 7:1908
    [Google Scholar]
  101. 101.
    Wang Q, Zou Q, Dai Z, Hong N, Wang G, Wang L. 2022. Four novel mycoviruses from the hypovirulent Botrytis cinerea SZ-2-3y isolate from Paris polyphylla: molecular characterisation and mitoviral sequence transboundary entry into plants. Viruses 14:151
    [Google Scholar]
  102. 102.
    Deom CM, Schubert KR, Wolf S, Holt CA, Lucas WJ, Beachy RN. 1990. Molecular characterization and biological function of the movement protein of tobacco mosaic virus in transgenic plants. PNAS 87:3284–88
    [Google Scholar]
  103. 103.
    Sun L, Nuss DL, Suzuki N. 2006. Synergism between a mycoreovirus and a hypovirus mediated by the papain-like protease p29 of the prototypic hypovirus CHV1-EP713. J. Gen. Virol. 87:3703–14
    [Google Scholar]
  104. 104.
    Mascia T, Gallitelli D. 2016. Synergies and antagonisms in virus interactions. Plant Sci. 252:176–92
    [Google Scholar]
  105. 105.
    Kubota K, Tsuda S, Tamai A, Meshi T. 2003. Tomato mosaic virus replication protein suppresses virus-targeted posttranscriptional gene silencing. J. Virol. 77:11016–26
    [Google Scholar]
  106. 106.
    Kurihara Y, Inaba N, Kutsuna N, Takeda A, Tagami Y, Watanabe Y. 2007. Binding of tobamovirus replication protein with small RNA duplexes. J. Gen. Virol. 88:2347–52
    [Google Scholar]
  107. 107.
    Vogler H, Akbergenov R, Shivaprasad PV, Dang V, Fasler M et al. 2007. Modification of small RNAs associated with suppression of RNA silencing by tobamovirus replicase protein. J. Virol. 81:10379–88
    [Google Scholar]
  108. 108.
    Sun Q, Choi GH, Nuss DL. 2009. A single Argonaute gene is required for induction of RNA silencing antiviral defense and promotes viral RNA recombination. PNAS 106:17927–32
    [Google Scholar]
  109. 109.
    Nicolás FE, Ruiz-Vázquez RM. 2013. Functional diversity of RNAi-associated sRNAs in fungi. Int. J. Mol. Sci. 14:15348–60
    [Google Scholar]
  110. 110.
    Nicolás FE, Garre V 2017. RNA interference in fungi: retention and loss. The Fungal Kingdom J Heitman, BJ Howlett, PW Crous, EH Stukenbrock, TY James, NAR Gow 657–71. Washington, DC: Am. Soc. Microbiol.
    [Google Scholar]
  111. 111.
    Quintanilha-Peixoto G, Fonseca PLC, Raya FT, Marone MP, Bortolini DE et al. 2021. The sisal virome: uncovering the viral diversity of agave varieties reveals new and organ-specific viruses. Microorganisms 9:1704
    [Google Scholar]
  112. 112.
    Marzano S-YL, Domier LL. 2016. Novel mycoviruses discovered from metatranscriptomics survey of soybean phyllosphere phytobiomes. Virus Res. 213:332–42
    [Google Scholar]
  113. 113.
    Mifsud JC, Gallagher RV, Holmes EC, Geoghegan JL. 2022. Transcriptome mining expands knowledge of RNA viruses across the plant kingdom. J. Virol. 96:e00260–22
    [Google Scholar]
  114. 114.
    Glazebrook J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43:205–27
    [Google Scholar]
  115. 115.
    Barata-Antunes C, Alves R, Talaia G, Casal M, Gerós H et al. 2021. Endocytosis of nutrient transporters in fungi: the ART of connecting signaling and trafficking. Comput. Struct. Biotechnol. J. 19:1713–37
    [Google Scholar]
  116. 116.
    Lo Presti L, Lanver D, Schweizer G, Tanaka S, Liang L et al. 2015. Fungal effectors and plant susceptibility. Annu. Rev. Plant Biol. 66:513–45
    [Google Scholar]
  117. 117.
    Tariqjaveed M, Mateen A, Wang S, Qiu S, Zheng X et al. 2021. Versatile effectors of phytopathogenic fungi target host immunity. J. Integr. Plant Biol. 63:1856–73
    [Google Scholar]
  118. 118.
    Bradshaw MJ, Bartholomew HP, Fonseca JM, Gaskins VL, Prusky D, Jurick WM II. 2021. Delivering the goods: Fungal secretion modulates virulence during host–pathogen interactions. Fungal Biol. Rev. 36:76–86
    [Google Scholar]
  119. 119.
    Vincent D, Rafiqi M, Job D. 2020. The multiple facets of plant–fungal interactions revealed through plant and fungal secretomics. Front. Plant Sci. 10:1626
    [Google Scholar]
  120. 120.
    Doehlemann G, Hemetsberger C. 2013. Apoplastic immunity and its suppression by filamentous plant pathogens. New Phytol. 198:1001–16
    [Google Scholar]
  121. 121.
    Wang X, Chung KP, Lin W, Jiang L. 2018. Protein secretion in plants: conventional and unconventional pathways and new techniques. J. Exp. Bot. 69:21–37
    [Google Scholar]
  122. 122.
    Rabouille C. 2017. Pathways of unconventional protein secretion. Trends Cell Biol. 27:230–40
    [Google Scholar]
  123. 123.
    Shoji J, Kikuma T, Kitamoto K. 2014. Vesicle trafficking, organelle functions, and unconventional secretion in fungal physiology and pathogenicity. Curr. Opin. Microbiol. 20:1–9
    [Google Scholar]
  124. 124.
    Nemati M, Singh B, Mir RA, Nemati M, Babaei A et al. 2022. Plant-derived extracellular vesicles: a novel nanomedicine approach with advantages and challenges. Cell Commun. Signal. 20:69
    [Google Scholar]
  125. 125.
    Rizzo J, Rodrigues ML, Janbon G. 2020. Extracellular vesicles in fungi: past, present, and future perspectives. Front. Cell. Infect. Microbiol. 10:346
    [Google Scholar]
  126. 126.
    Van Niel G, d'Angelo G, Raposo G. 2018. Shedding light on the cell biology of extracellular vesicles. Nat. Rev. Mol. Cell Biol. 19:213–28
    [Google Scholar]
  127. 127.
    Samuel M, Bleackley M, Anderson M, Mathivanan S. 2015. Extracellular vesicles including exosomes in cross kingdom regulation: a viewpoint from plant-fungal interactions. Front. Plant Sci. 6:766
    [Google Scholar]
  128. 128.
    Rybak K, Robatzek S. 2019. Functions of extracellular vesicles in immunity and virulence. Plant Physiol. 179:1236–47
    [Google Scholar]
  129. 129.
    Rutter BD, Innes RW. 2018. Extracellular vesicles as key mediators of plant–microbe interactions. Curr. Opin. Plant Biol. 44:16–22
    [Google Scholar]
  130. 130.
    Uhse S, Djamei A. 2018. Effectors of plant-colonizing fungi and beyond. PLOS Pathog. 14:e1006992
    [Google Scholar]
  131. 131.
    Zhang S, Li C, Si J, Han Z, Chen D. 2022. Action mechanisms of effectors in plant-pathogen interaction. Int. J. Mol. Sci. 23:6758
    [Google Scholar]
  132. 132.
    Giraldo MC, Valent B. 2013. Filamentous plant pathogen effectors in action. Nat. Rev. Microbiol. 11:800–14
    [Google Scholar]
  133. 133.
    Petre B, Kamoun S. 2014. How do filamentous pathogens deliver effector proteins into plant cells?. PLOS Biol. 12:e1001801
    [Google Scholar]
  134. 134.
    Presti LL, Kahmann R. 2017. How filamentous plant pathogen effectors are translocated to host cells. Curr. Opin. Plant Biol. 38:19–24
    [Google Scholar]
  135. 135.
    Weiberg A, Wang M, Lin F-M, Zhao H, Zhang Z et al. 2013. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342:118–23
    [Google Scholar]
  136. 136.
    Hou Y, Zhai Y, Feng L, Zand Karimi H, Rutter BD et al. 2019. A Phytophthora effector suppresses trans-kingdom RNAi to promote disease susceptibility. Cell Host Microbe 25:153–65.e5
    [Google Scholar]
  137. 137.
    Hua C, Zhao J-H, Guo H-S. 2018. Trans-kingdom RNA silencing in plant–fungal pathogen interactions. Mol. Plant 11:235–44
    [Google Scholar]
  138. 138.
    Wang M, Weiberg A, Lin F-M, Thomma BP, Huang H-D, Jin H 2016. Bidirectional cross-kingdom RNAi and fungal uptake of external RNAs confer plant protection. Nat. Plants 2:16151
    [Google Scholar]
  139. 139.
    Cai Q, Qiao L, Wang M, He B, Lin F-M et al. 2018. Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes. Science 360:1126–29
    [Google Scholar]
  140. 140.
    Ruf A, Oberkofler L, Robatzek S, Weiberg A. 2022. Spotlight on plant RNA-containing extracellular vesicles. Curr. Opin. Plant Biol. 69:102272
    [Google Scholar]
  141. 141.
    He B, Cai Q, Qiao L, Huang C-Y, Wang S et al. 2021. RNA-binding proteins contribute to small RNA loading in plant extracellular vesicles. Nat. Plants 7:342–52
    [Google Scholar]
  142. 142.
    Zand Karimi H, Baldrich P, Rutter BD, Borniego L, Zajt KK et al. 2022. Arabidopsis apoplastic fluid contains sRNA- and circular RNA–protein complexes that are located outside extracellular vesicles. Plant Cell 34:1863–81
    [Google Scholar]
  143. 143.
    Liebana-Jordan M, Brotons B, Falcon-Perez JM, Gonzalez E. 2021. Extracellular vesicles in the fungi kingdom. Int. J. Mol. Sci. 22:7221
    [Google Scholar]
  144. 144.
    Qiao L, Lan C, Capriotti L, Ah-Fong A, Nino Sanchez J et al. 2021. Spray-induced gene silencing for disease control is dependent on the efficiency of pathogen RNA uptake. Plant Biotechnol. J. 19:1756–68
    [Google Scholar]
  145. 145.
    Laliberté J-F, Zheng H. 2014. Viral manipulation of plant host membranes. Annu. Rev. Virol. 1:237–59
    [Google Scholar]
  146. 146.
    Movahed N, Cabanillas DG, Wan J, Vali H, Laliberté J-F, Zheng H. 2019. Turnip mosaic virus components are released into the extracellular space by vesicles in infected leaves. Plant Physiol. 180:1375–88
    [Google Scholar]
  147. 147.
    Hu S, Yin Y, Chen B, Lin Q, Tian Y et al. 2021. Identification of viral particles in the apoplast of Nicotiana benthamiana leaves infected by potato virus X. Mol. Plant Pathol. 22:456–64
    [Google Scholar]
  148. 148.
    Yu X, Li B, Fu Y, Xie J, Cheng J et al. 2013. Extracellular transmission of a DNA mycovirus and its use as a natural fungicide. PNAS 110:1452–57
    [Google Scholar]
  149. 149.
    de Ronde D, Butterbach P, Kormelink R. 2014. Dominant resistance against plant viruses. Front. Plant Sci. 5:307
    [Google Scholar]
  150. 150.
    Hashimoto M, Neriya Y, Yamaji Y, Namba S. 2016. Recessive resistance to plant viruses: potential resistance genes beyond translation initiation factors. Front. Microbiol. 7:1695
    [Google Scholar]
  151. 151.
    Tatineni S, Hein GL. 2023. Plant viruses of agricultural importance: current and future perspectives of virus disease management strategies. Phytopathology 113:2117–41
    [Google Scholar]
  152. 152.
    Hadidi A, Sun L, Randles JW. 2022. Modes of viroid transmission. Cells 11:719
    [Google Scholar]
  153. 153.
    Barba M, Ilardi V, Pasquini G. 2015. Control of pome and stone fruit virus diseases. Adv. Virus Res. 91:47–83
    [Google Scholar]
/content/journals/10.1146/annurev-virology-111821-122539
Loading
/content/journals/10.1146/annurev-virology-111821-122539
Loading

Data & Media loading...

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error