1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Phytopathology
  4. Volume 60, 2022
  5. Article

Annual Review of Phytopathology

Volume 60, 2022

Going Viral: Virus-Based Biological Control Agents for Plant Protection

Abstract

The most economically important biotic stresses in crop production are caused by fungi, oomycetes, insects, viruses, and bacteria. Often chemical control is still the most commonly used method to manage them. However, the development of resistance in the different pathogens/pests, the putative damage on the natural ecosystem, the toxic residues in the field, and, thus, the contamination of the environment have stimulated the search for saferalternatives such as the use of biological control agents (BCAs). Among BCAs, viruses, a major driver for controlling host populations and evolution, are somewhat underused, mostly because of regulatory hurdles that make the cost of registration of such host-specific BCAs not affordable in comparison with the limited potential market. Here, we provide a comprehensive overview of the state of the art of virus-based BCAs against fungi, bacteria, viruses, and insects, with a specific focus on new approaches that rely on not only the direct biocidal virus component but also the complex ecological interactions between viruses and their hosts that do not necessarily result in direct damage to the host.

Keyword(s): bacteriophage, biocontrol, entomovirus, mycovirus, nanotechnology, virus
Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-021621-114208
2022-08-26
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/phyto/60/1/annurev-phyto-021621-114208.html?itemId=/content/journals/10.1146/annurev-phyto-021621-114208&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Abba S, Galetto L, Vallino M, Rossi M, Turina M et al. 2017. Genome sequence, prevalence and quantification of the first iflavirus identified in a phytoplasma insect vector. Arch. Virol. 162:799–809
     [Google Scholar]
  2. 2.
    Aguero J, Gomez-Aix C, Sempere RN, Garcia-Villalba J, Garcia-Nunez J et al. 2018. Stable and broad spectrum cross-protection against Pepino mosaic virus attained by mixed infection. Front. Plant Sci. 9:1810
     [Google Scholar]
  3. 3.
    Ahmad AA, Askora A, Kawasaki T, Fujie M, Yamada T. 2014. The filamentous phage XacF1 causes loss of virulence in Xanthomonas axonopodis pv. citri, the causative agent of citrus canker disease. Front. Microbiol. 5:321
     [Google Scholar]
  4. 4.
    Akremi I, Holtappels D, Brabra W, Jlidi M, Ibrahim AH et al. 2020. First report of filamentous phages isolated from Tunisian orchards to control Erwinia amylovora. Microorganisms 8:1762
     [Google Scholar]
  5. 5.
    Alejandro Solis-Sanchez G, Esmeralda Quinones-Aguilar E, Fraire-Velazquez S, Vega-Arreguin J, Rincon-Enriquez G 2020. Complete genome sequence of XaF13, a novel bacteriophage of Xanthomonas vesicatoria from Mexico. Microbiol. Resour. Announc. 9:e01371–19
     [Google Scholar]
  6. 6.
    Altinli M, Lequime S, Courcelle M, Francois S, Justy F et al. 2019. Evolution and phylogeography of Culex pipiens densovirus. Virus Evol 5:vez053
     [Google Scholar]
  7. 7.
    Amiri E, Herman JJ, Strand MK, Tarpy DR, Rueppell O. 2020. Egg transcriptome profile responds to maternal virus infection in honey bees, Apis mellifera. Infect. Genet. Evol. 85:104558
     [Google Scholar]
  8. 8.
    Anagnostakis SL. 1982. Biological control of Chestnut blight. Science 215:466–71
     [Google Scholar]
  9. 9.
    Arjona-Lopez JM, Telengech P, Jamal A, Hisano S, Kondo H et al. 2018. Novel, diverse RNA viruses from Mediterranean isolates of the phytopathogenic fungus, Rosellinia necatrix: insights into evolutionary biology of fungal viruses. Environ. Microbiol. 20:1464–83
     [Google Scholar]
  10. 10.
    Arpaia S, Birch ANE, Kiss J, van Loon JJA, Messean A et al. 2017. Assessing environmental impacts of genetically modified plants on non-target organisms: the relevance of in planta studies. Sci. Total Environ. 583:123–32
     [Google Scholar]
  11. 11.
    Asser-Kaiser S, Fritsch E, Undorf-Spahn K, Kienzle J, Eberle KE et al. 2007. Rapid emergence of baculovirus resistance in codling moth due to dominant, sex-linked inheritance. Science 317:1916–18
     [Google Scholar]
  12. 12.
    Asser-Kaiser S, Radtke P, El-Salamouny S, Winstanley D, Jehle JA. 2011. Baculovirus resistance in codling moth (Cydia pomonella L.) caused by early block of virus replication. Virology 410:360–67
     [Google Scholar]
  13. 13.
    Bai X, Correa VR, Toruno TY, Ammar E-D, Kamoun S, Hogenhout SA. 2009. AY-WB phytoplasma secretes a protein that targets plant cell nuclei. Mol. Plant-Microbe Interact. 22:18–30
     [Google Scholar]
  14. 14.
    Balogh B, Canteros BI, Stall KE, Jones JB. 2008. Control of citrus canker and citrus bacterial spot with bacteriophages. Plant Dis 92:1048–52
     [Google Scholar]
  15. 15.
    Balogh B, Jones JB, Momol MT, Olson SM, Obradovic A et al. 2003. Improved efficacy of newly formulated bacteriophages for management of bacterial spot on tomato. Plant Dis. 87:949–54
     [Google Scholar]
  16. 16.
    Beckage NE. 2008. Insect Immunology San Diego: Academic
  17. 17.
    Benaets K, Van Geystelen A, Cardoen D, De Smet L, de Graaf DC et al. 2017. Covert deformed wing virus infections have long-term deleterious effects on honeybee foraging and survival. Proc. R. Soc. B 284:20162149
     [Google Scholar]
  18. 18.
    Bian RL, Andika IB, Pang TX, Lian ZQ, Wei S et al. 2020. Facilitative and synergistic interactions between fungal and plant viruses. PNAS 117:3779–88
     [Google Scholar]
  19. 19.
    Boeckaerts D, Stock M, Criel B, Gerstmans H, De Baets B, Briers Y. 2021. Predicting bacteriophage hosts based on sequences of annotated receptor-binding proteins. Sci. Rep. 11:1467
     [Google Scholar]
  20. 20.
    Burrowes BH, Molineux IJ, Fralick JA. 2019. Directed in vitro evolution of therapeutic bacteriophages: the Appelmans Protocol. Viruses 11:241
     [Google Scholar]
  21. 21.
    Buttimer C, McAuliffe O, Ross RP, Hill C, O'Mahony J, Coffey A. 2017. Bacteriophages and bacterial plant diseases. Front. Microbiol. 8:34
     [Google Scholar]
  22. 22.
    Carballo A, Murillo R, Jakubowska A, Herrero S, Williams T, Caballero P. 2017. Co-infection with iflaviruses influences the insecticidal properties of Spodoptera exigua multiple nucleopolyhedrovirus occlusion bodies: implications for the production and biosecurity of baculovirus insecticides. PLOS ONE 12:e0177301
     [Google Scholar]
  23. 23.
    Chen B, Chen C-H, Bowman BH, Nuss DL. 1996. Phenotypic changes associated with wild-type and mutant hypovirus RNA transfection of plant pathogenic fungi phylogenetically related to Cryphonectria parasitica. Phytopathology 86:301–10
     [Google Scholar]
  24. 24.
    Chen BS, Choi GH, Nuss DL. 1993. Mitotic stability and nuclear inheritance of integrated viral cDNA in engineered hypovirulent strains of the chestnut blight fungus. EMBO J 12:2991–98
     [Google Scholar]
  25. 25.
    Chewachong GM, Miller SA, Blakeslee JJ, Francis DM, Morris TJ, Qu F. 2015. Generation of an attenuated, cross-protective Pepino mosaic virus variant through alignment-guided mutagenesis of the viral capsid protein. Phytopathology 105:126–34
     [Google Scholar]
  26. 26.
    Chiapello M, Bosco L, Ciuffo M, Ottati S, Salem N et al. 2021. Complexity and local specificity of the virome associated with tospovirus-transmitting thrips species. J. Virol. 95:21e0059721
     [Google Scholar]
  27. 27.
    Chiapello M, Rodriguez-Romero J, Ayllón MA, Turina M. 2020. Analysis of the virome associated to grapevine downy mildew lesions reveals new mycovirus lineages. Virus Evol 6:veaa058
     [Google Scholar]
  28. 28.
    Christiaens O, Whyard S, Velez AM, Smagghe G. 2020. Double-stranded RNA technology to control insect pests: current status and challenges. Front. Plant Sci. 11:451
     [Google Scholar]
  29. 29.
    Cody WB, Scholthof HB. 2019. Plant virus vectors 3.0: transitioning into synthetic genomics. Annu. Rev. Phytopathol. 57:211–30
     [Google Scholar]
  30. 30.
    Cotmore SF, Agbandje-McKenna M, Canuti M, Chiorini JA, Eis-Hubinger A-M et al. 2019. ICTV virus taxonomy profile: Parvoviridae. J. Gen. Virol. 100:367–68
     [Google Scholar]
  31. 31.
    Doemoetoer D, Becsagh P, Rakhely G, Schneider G, Kovacs T. 2012. Complete genomic sequence of Erwinia amylovora phage PhiEaH2. J. Virol. 86:10899
     [Google Scholar]
  32. 32.
    Dommes AB, Gross T, Herbert DB, Kivivirta KI, Becker A. 2019. Virus-induced gene silencing: empowering genetics in non-model organisms. J. Exp. Botany 70:757–70
     [Google Scholar]
  33. 33.
    Double ML, Nuss DL, Rittenour WR, Holaskova I, Short DPG et al. 2017. Long-term field study of transgenic hypovirulent strains of Cryphonectria parasitica in a forest setting. For. Pathol. 47:e12367
     [Google Scholar]
  34. 34.
    Eilenberg J, Hajek AE. 2019. Editorial overview: insect resistance and susceptibility to pathogens: a multi-faceted topic. Curr. Opin. Insect. Sci. 33:iii–v
     [Google Scholar]
  35. 35.
    Entwistle PF, Evans HF. 1985. Viral control. Comprehensive Insect Physiology. Biochemistry and Pharmacology, Vol. 12. Insect Control GA Kerkut, LI Gilbert 347–412 Oxford, UK: Pergamon Press
     [Google Scholar]
  36. 36.
    Eur. Food Saf. Auth 2015. Conclusion on the peer review of the pesticide risk assessment of the active substance Pepino mosaic virus strain CH2 isolate 1906. EFSA J. 13:3977
     [Google Scholar]
  37. 37.
    Fan J, Wennmann JT, Wang D, Jehle JA 2020. Novel diversity and virulence patterns found in new isolates of Cydia pomonella granulovirus from China. Appl. Environ. Microbiol. 86:e02000–19
     [Google Scholar]
  38. 38.
    Feng CC, Feng JH, Wang ZY, Pedersen C, Wang XQ et al. 2021. Identification of the viral determinant of hypovirulence and host range in Sclerotiniaceae of a genomovirus reconstructed from the plant metagenome. J. Virol. 95:e00264–21
     [Google Scholar]
  39. 39.
    Flaherty JE, Jones JB, Harbaugh BK, Somodi GC, Jackson LE. 2000. Control of bacterial spot on tomato in the greenhouse and field with H-mutant bacteriophages. HortScience 35:882–84
     [Google Scholar]
  40. 40.
    Folimonova SY. 2013. Developing an understanding of cross-protection by Citrus tristeza virus. Front. Microbiol. 4:76
     [Google Scholar]
  41. 41.
    Folimonova SY, Harper SJ, Leonard MT, Triplett EW, Shilts T. 2014. Superinfection exclusion by Citrus tristeza virus does not correlate with the production of viral small RNAs. Virology 468:462–71
     [Google Scholar]
  42. 42.
    Francois S, Filloux D, Roumagnac P, Bigot D, Gayral P et al. 2016. Discovery of parvovirus-related sequences in an unexpected broad range of animals. Sci. Rep. 6:30880
     [Google Scholar]
  43. 43.
    Francois S, Mutuel D, Duncan AB, Rodrigues LR, Danzelle C et al. 2019. A new prevalent densovirus discovered in Acari. Insight from metagenomics in viral communities associated with two-spotted mite (Tetranychus urticae) populations. Viruses 11:233
     [Google Scholar]
  44. 44.
    Frederiks C, Wesseler JHH. 2019. A comparison of the EU and US regulatory frameworks for the active substance registration of microbial biological control agents. Pest Manag. Sci. 75:87–103
     [Google Scholar]
  45. 45.
    Fuxa JR, Sun JZ, Weidner EH, LaMotte LR. 1999. Stressors and rearing diseases of Trichoplusia ni: evidence of vertical transmission of NPV and CPV. J. Invertebr. Pathol. 74:149–55
     [Google Scholar]
  46. 46.
    Gasmi L, Frattini A, Ogliastro M, Herrero S. 2019. Outcome of mixed DNA virus infections on Spodoptera exigua susceptibility to SeMNPV. J. Pest Sci. 92:885–93
     [Google Scholar]
  47. 47.
    Genty P, Mariau D. 1975. Utilisation d'un germe entomopathogene Bans la lutte contre Sibine fusca (Limacodidae). Oleagineux 30:349–54
     [Google Scholar]
  48. 48.
    Gerba CP. 1984. Applied and theoretical aspects of virus adsorption to surfaces. Adv. Appl. Microbiol. 30:133–68
     [Google Scholar]
  49. 49.
    Grant T-J, Costa AS. 1951. A mild strain of the tristeza virus of citrus. Phytopathology 41:114–22
     [Google Scholar]
  50. 50.
    Gu JB, Liu M, Deng YH, Peng HJ, Chen XG. 2011. Development of an efficient recombinant mosquito densovirus-mediated RNA interference system and its preliminary application in mosquito control. PLOS ONE 6:e21329
     [Google Scholar]
  51. 51.
    Hajek AE, van Frankenhuyzen K 2017. Use of entomopathogens against forest pests. Microbial Control of Insect and Mite Pests: From Theory to Practice LA Lacey 313–30 Cambridge, MA: Acad. Press
     [Google Scholar]
  52. 52.
    Hajeri S, Killiny N, El-Mohtar C, Dawson WO, Gowda S. 2014. Citrus tristeza virus-based RNAi in citrus plants induces gene silencing in Diaphorina citri, a phloem-sap sucking insect vector of citrus greening disease (Huanglongbing). J. Biotechnol. 176:42–49
     [Google Scholar]
  53. 53.
    Hanssen IM, Gutierrez-Aguirre I, Paeleman A, Goen K, Wittemans L et al. 2010. Cross-protection or enhanced symptom display in greenhouse tomato co-infected with different Pepino mosaic virus isolates. Plant Pathol 59:13–21
     [Google Scholar]
  54. 54.
    Hardy T, Bopp S, Egsmose M, Fontier H, Mohimont L et al. 2012. Risk assessment of plant protection products. EFSA J. 10:10s1010
     [Google Scholar]
  55. 55.
    Heiniger U, Rigling D. 1994. Biological control of chestnut blight in Europe. Annu. Rev. Phytopathol. 32:581–99
     [Google Scholar]
  56. 56.
    Holtappels D, Fortuna K, Lavigne R, Wagemans J. 2021. The future of phage biocontrol in integrated plant protection for sustainable crop production. Curr. Opin. Biotechnol. 68:60–71
     [Google Scholar]
  57. 57.
    Ibrahim YE, Saleh AA, Al-Saleh MA. 2017. Management of Asiatic citrus canker under field conditions in Saudi Arabia using bacteriophages and acibenzolar-S-methyl. Plant Dis 101:761–65
     [Google Scholar]
  58. 58.
    Joga MR, Zotti MJ, Smagghe G, Christiaens O. 2016. RNAi efficiency, systemic properties, and novel delivery methods for pest insect control: what we know so far. Front. Physiol. 7:553
     [Google Scholar]
  59. 59.
    Johnson RM, Rasgon JL. 2018. Densonucleosis viruses (‘densoviruses’) for mosquito and pathogen control. Curr. Opin. Insect. Sci. 28:90–97
     [Google Scholar]
  60. 60.
    Jourdan M, Jousset FX, Gervais M, Skory S, Bergoin M, Dumas B. 1990. Cloning of the genome of a densovirus and rescue of infectious virions from recombinant plasmid in the insect host Spodoptera littoralis. Virology 179:403–9
     [Google Scholar]
  61. 61.
    Jurvansuu J, Kashif M, Vaario L, Vainio E, Hantula J. 2014. Partitiviruses of a fungal forest pathogen have species-specific quantities of genome segments and transcripts. Virology 462:25–33
     [Google Scholar]
  62. 62.
    Kane M, Golovkina T. 2010. Common threads in persistent viral infections. J. Virol. 84:4116–23
     [Google Scholar]
  63. 63.
    Kanematsu S, Sasaki A, Onoue M, Oikawa Y, Ito T. 2010. Extending the fungal host range of a partitivirus and a mycoreovirus from Rosellinia necatrix by inoculation of protoplasts with virus particles. Phytopathology 100:922–30
     [Google Scholar]
  64. 64.
    Kerr CH, Wang QS, Keatings K, Khong A, Allan D et al. 2015. The 5′ untranslated region of a novel infectious molecular clone of the dicistrovirus Cricket paralysis virus modulates infection. J. Virol. 89:5919–34
     [Google Scholar]
  65. 65.
    Kraberger S, Stainton D, Dayaram A, Zawar-Reza P, Gomez C et al. 2013. Discovery of Sclerotinia sclerotiorum hypovirulence-associated virus-1 in urban river sediments of Heathcote and Styx rivers in Christchurch City, New Zealand. Microbiol. Resourc. Announc. 1:e00559–13
     [Google Scholar]
  66. 66.
    Kunte N, McGraw E, Bell S, Held D, Avila L-A. 2020. Prospects, challenges and current status of RNAi through insect feeding. Pest Manag. Sci. 76:26–41
     [Google Scholar]
  67. 67.
    Kwon H, Kim J, Lim H, Yu Y, Youn Y. 2018. Construction of a cDNA library of Aphis gossypii Glover for use in RNAi. Entomol. Res. 48:384–89
     [Google Scholar]
  68. 68.
    Lang JM, Gent DH, Schwartz HF. 2007. Management of Xanthomonas leaf blight of onion with bacteriophages and a plant activator. Plant Dis 91:871–78
     [Google Scholar]
  69. 69.
    Lee N-Y, Ko W-C, Hsueh P-R. 2019. Nanoparticles in the treatment of infections caused by multidrug-resistant organisms. Front. Pharmacol. 10:1153
     [Google Scholar]
  70. 70.
    Liu P, Li X, Gu J, Dong Y, Liu Y et al. 2016. Development of non-defective recombinant densovirus vectors for microRNA delivery in the invasive vector mosquito. Aedes albopictus. Sci. Rep. 6:20979
     [Google Scholar]
  71. 71.
    Liu S, Xie JT, Cheng JS, 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]
  72. 72.
    Liu YC, Linder-Basso D, Hillman BI, Kaneko S, Milgroom MG. 2003. Evidence for interspecies transmission of viruses in natural populations of filamentous fungi in the genus Cryphonectria. Mol. Ecol. 12:1619–28
     [Google Scholar]
  73. 73.
    Lood C, Boeckaerts D, Stock M, De Baets B, Lavigne R et al. 2022. Digital phagograms: predicting phage infectivity through a multilayer machine learning approach. Curr. Opin. Virol. 52:174–81
     [Google Scholar]
  74. 74.
    Lu H, Zhu J, Yu J, Chen X, Kang L, Cui F. 2020. A symbiotic virus facilitates aphid adaptation to host plants by suppressing jasmonic acid responses. Mol. Plant-Microbe Interact. 33:55–65
     [Google Scholar]
  75. 75.
    Macera L, Spezia PG, Medici C, Falasca F, Sciandra I et al. 2019. Low prevalence of Gemycircularvirus DNA in immunocompetent and immunocompromised subjects. New Microbiol 42:118–20
     [Google Scholar]
  76. 76.
    Mallmann W, Hemstreet C. 1924. Isolation of an inhibitory substance from plants. Agric. Res. 28:599–602
     [Google Scholar]
  77. 77.
    Martorell-Marugán J, Tabik S, Benhammou Y, del Val C, Zwir I et al. 2019. Deep learning in omics data analysis and precision medicine. Computational Biology H Husi , pp.37–53 Brisbane, Aust: Codon Publ.
     [Google Scholar]
  78. 78.
    McKinney HH. 1929. Mosaic diseases in the Canary Islands, West Africa, and Gibraltar. J. Agric. Res. 39:557–78
     [Google Scholar]
  79. 79.
    Meczker K, Doemoetoer D, Vass J, Rakhely G, Schneider G, Kovacs T. 2014. The genome of the Erwinia amylovora phage PhiEaH1 reveals greater diversity and broadens the applicability of phages for the treatment of fire blight. FEMS Microbiol. Lett. 350:25–27
     [Google Scholar]
  80. 80.
    Melzer MS, Ikeda SS, Boland GJ. 2002. Interspecific transmission of double-stranded RNA and hypovirulence from Sclerotinia sclerotiorum to S-minor. Phytopathology 92:780–84
     [Google Scholar]
  81. 81.
    Meynadier G. 1964. Virose d'un type inhabituel chez le Lepidoptere, Galleria mellonella L. Rev. Zool. Agric. Appl. 63:207–8
     [Google Scholar]
  82. 82.
    Meynadier G, Amargier A, Genty P. 1977. Une virose de type densonucleose chez le lepidoptere Sibine fusca Stoll. Oleagineux 32:357–61
     [Google Scholar]
  83. 83.
    Milgroom MG, Cortesi P. 2004. Biological control of chestnut blight with hypovirulence: a critical analysis. Annu. Rev. Phytopathol. 42:311–38
     [Google Scholar]
  84. 84.
    Minor PD. 2015. Live attenuated vaccines: historical successes and current challenges. Virology 479:379–92
     [Google Scholar]
  85. 85.
    Monsarrat P, Mariau D, Genty P. 1984. Densovirus en lutte biologique. Bull. Soc. Entomol. Fr. 89:816–21
     [Google Scholar]
  86. 86.
    Monteiro R, Pires D, Costa A, Azeredo J 2019. Phage therapy: going temperate?. Trends Microbiol 27:368–78
     [Google Scholar]
  87. 87.
    Moscardi F. 1999. Assessment of the application of baculoviruses for control of Lepidoptera. Annu. Rev. Entomol. 44:257–89
     [Google Scholar]
  88. 88.
    Myers JH, Cory JS. 2016. Ecology and evolution of pathogens in natural populations of Lepidoptera. Evol. Appl. 9:231–47
     [Google Scholar]
  89. 89.
    Nouri S, Salem N, Nigg JC, Falk BW. 2016. Diverse array of new viral sequences identified in worldwide populations of the Asian citrus psyllid (Diaphorina citri) using viral metagenomics. J. Virol. 90:2434–45
     [Google Scholar]
  90. 90.
    Nuss DL. 2005. Hypovirulence: mycoviruses at the fungal-plant interface. Nat. Rev. Microbiol. 3:632–42
     [Google Scholar]
  91. 91.
    Oh Y, Kim H, Kim SG. 2021. Virus-induced plant genome editing. Curr. Opin. Plant Biol. 60:101992
     [Google Scholar]
  92. 92.
    Ottati S, Chiapello M, Galetto L, Bosco D, Marzachi C, Abba S. 2020. New viral sequences identified in the flavescence dorée phytoplasma vector Scaphoideus titanus. Viruses 12:287
     [Google Scholar]
  93. 93.
    Otvos IS, Cunningham JC, Alfaro RI. 1987. Aerial application of nuclear polyhedrosis virus against Douglas-fir tussock moth, Orgyia pseudotsugata (Mcdunnough) (Lepidoptera, Lymantriidae): 2. Impact 1 year and 2 years after application. Can. Entomol. 119:707–15
     [Google Scholar]
  94. 94.
    Pearson MN, Beever RE, Boine B, Arthur K 2009. Mycoviruses of filamentous fungi and their relevance to plant pathology. Mol. Plant Pathol. 10:115–28
     [Google Scholar]
  95. 95.
    Pechinger K, Chooi KM, MacDiarmid RM, Harper SJ, Ziebell H. 2019. A new era for mild strain cross-protection. Viruses 11:670
     [Google Scholar]
  96. 96.
    Perrin A, Gosselin-Grenet A-S, Rossignol M, Ginibre C, Scheid B et al. 2020. Variation in the susceptibility of urban Aedes mosquitoes infected with a densovirus. Sci. Rep. 10:18654
     [Google Scholar]
  97. 97.
    Pirnay J-P. 2020. Phage therapy in the year 2035. Front. Microbiol. 11:1171
     [Google Scholar]
  98. 98.
    Podgwaite JD, Mazzone HM. 1986. Latency of insect viruses. Adv. Virus Res. 31:293–320
     [Google Scholar]
  99. 99.
    Prasad R, Gupta N, Kumar M, Kumar V, Wang S, Abd-Elsalam KA 2017. Nanomaterials act as plant defense mechanism. Nanotechnology R Prasad 253–69 Singapore: Springer
     [Google Scholar]
  100. 100.
    Prasad V, Srivastava S. 2016. Insect viruses. Ecofriendly Pest Management for Food Security Omkar 411–42 Cambridge, MA: Acad. Press
     [Google Scholar]
  101. 101.
    Pratama AA, van Elsas JD. 2018. The ‘neglected’ soil virome: potential role and impact. Trends Microbiol 26:649–62
     [Google Scholar]
  102. 102.
    Prospero S, Rigling D. 2016. Using molecular markers to assess the establishment and spread of a mycovirus applied as a biological control agent against chestnut blight. Biocontrol 61:313–23
     [Google Scholar]
  103. 103.
    Pyle JD, Scholthof KBG 2017. Biology and pathogenesis of satellite viruses. Viroids and Satellites A Hadidi, R Flores, J Randles, P Palukaitis 627–36 Cambridge, MA: Acad. Press
     [Google Scholar]
  104. 104.
    Ratcliff FG, MacFarlane SA, Baulcombe DC. 1999. Gene silencing without DNA: RNA-mediated cross-protection between viruses. Plant Cell 11:1207–15
     [Google Scholar]
  105. 105.
    Ren X, Hoiczyk E, Rasgon JL. 2008. Viral paratransgenesis in the malaria vector Anopheles gambiae. PLOS Pathog 4:e1000135
     [Google Scholar]
  106. 106.
    Rigling D, Prospero S. 2017. Cryphonectria parasitica, the causal agent of chestnut blight: invasion history, population biology and disease control. Mol. Plant Pathol. 19:7–20
     [Google Scholar]
  107. 107.
    Rivers CF, Longwort JF. 1972. Nonoccluded virus of Junonia coenia (Nymphalidae: Lepidoptera). J. Invertebr. Pathol. 20:369–70
     [Google Scholar]
  108. 108.
    Robin C, Lanz S, Soutrenon A, Rigling D. 2010. Dominance of natural over released biological control agents of the chestnut blight fungus Cryphonectria parasitica in south-eastern France is associated with fitness-related traits. Biological Control 53:55–61
     [Google Scholar]
  109. 109.
    Root C, Balbalian C, Bierman R, Geletka LM, Anagnostakis S et al. 2005. Multi-seasonal field release and spermatization trials of transgenic hypovirulent strains of Cryphonectria parasitica containing cDNA copies of hypovirus CHV1-EP713. Forest Pathol 35:277–97
     [Google Scholar]
  110. 110.
    Ruiz-Padilla A, Rodriguez-Romero J, Gomez-Cid I, Pacifico D, Ayllón MA. 2021. Novel mycoviruses discovered in the mycovirome of a necrotrophic fungus. mBio 12:e03705–20
     [Google Scholar]
  111. 111.
    Ryabov EV, Christmon K, Heerman MC, Posada-Florez F, Harrison RL et al. 2020. Development of a honey bee RNA virus vector based on the genome of a deformed wing virus. Viruses 12:4374
     [Google Scholar]
  112. 112.
    Schoebel CN, Prospero S, Gross A, Rigling D. 2018. Detection of a conspecific mycovirus in two closely related native and introduced fungal hosts and evidence for interspecific virus transmission. Viruses 10:628
     [Google Scholar]
  113. 113.
    Shen YB, Zhang R, Schwarz S, Wu CM, Shen JZ et al. 2020. Farm animals and aquaculture: significant reservoirs of mobile colistin resistance genes. Environ. Microbiol. 22:2469–84
     [Google Scholar]
  114. 114.
    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]
  115. 115.
    Shikano I, Ericsson JD, Cory JS, Myers JH 2010. Indirect plant-mediated effects on insect immunity and disease resistance in a tritrophic system. Basic Appl. Ecol. 11:15–22
     [Google Scholar]
  116. 116.
    Sikorski A, Massaro M, Kraberger S, Young LM, Smalley D et al. 2013. Novel myco-like DNA viruses discovered in the faecal matter of various animals. Virus Res 177:209–16
     [Google Scholar]
  117. 117.
    Simon AE, Roossinck MJ, Havelda Z. 2004. Plant virus satellite and defective interfering RNAs: new paradigms for a new century. Annu. Rev. Phytopathol. 42:415–37
     [Google Scholar]
  118. 118.
    Singh BN, Prateeksha, Upreti DK, Singh BR, Defoirdt T et al. 2017. Bactericidal, quorum quenching and anti-biofilm nanofactories: a new niche for nanotechnologists. Crit. Rev. Biotechnol. 37:525–40
     [Google Scholar]
  119. 119.
    Sosa-Gomez DR, Morgado FS, Correa RFT, Silva LA, Ardisson-Araujo DMP et al. 2020. Entomopathogenic viruses in the neotropics: current status and recently discovered species. Neotrop. Entomol. 49:315–31
     [Google Scholar]
  120. 120.
    Stauder CM, Nuss DL, Zhang D-X, Double ML, MacDonald WL et al. 2019. Enhanced hypovirus transmission by engineered super donor strains of the chestnut blight fungus, Cryphonectria parasitica, into a natural population of strains exhibiting diverse vegetative compatibility genotypes. Virology 528:1–6
     [Google Scholar]
  121. 121.
    Stefani E, Obradovic A, Gasic K, Altin I, Nagy IK, Kovacs T. 2021. Bacteriophage-mediated control of phytopathogenic xanthomonads: a promising green solution for the future. Microorganisms 9:1056
     [Google Scholar]
  122. 122.
    Stewart LMD, Hirst M, Ferber ML, Merryweather AT, Cayley PJ, Possee RD. 1991. Construction of an improved baculovirus insecticide containing an insect-specific toxin gene. Nature 352:85–88
     [Google Scholar]
  123. 123.
    Strange RN, Scott PR. 2005. Plant disease: a threat to global food security. Annu. Rev. Phytopathol. 43:83–116
     [Google Scholar]
  124. 124.
    Sullivan MB, Waterbury JB, Chisholm SW. 2003. Cyanophages infecting the oceanic cyanobacterium Prochlorococcus. Nature 424:1047–51
     [Google Scholar]
  125. 125.
    Summers MD. 2006. Milestones leading to the genetic engineering of baculoviruses as expression vector systems and viral pesticides. Insect Viruses Biotechnol. Appl. 68:3–73
     [Google Scholar]
  126. 126.
    Sun X. 2015. History and current status of development and use of viral insecticides in China. Viruses 7:306–19
     [Google Scholar]
  127. 127.
    Sundin GW, Wang N. 2018. Antibiotic resistance in plant-pathogenic bacteria. Annu. Rev. Phytopathol. 56:161–80
     [Google Scholar]
  128. 128.
    Suzuki N, Geletka LM, Nuss DL. 2000. Essential and dispensable virus-encoded replication elements revealed by efforts to develop hypoviruses as gene expression vectors. J. Virol. 74:7568–77
     [Google Scholar]
  129. 129.
    Svircev A, Roach D, Castle A. 2018. Framing the future with bacteriophages in agriculture. Viruses 10:218
     [Google Scholar]
  130. 130.
    Szoboszlay M, Tebbe CC. 2021. Hidden heterogeneity and co-occurrence networks of soil prokaryotic communities revealed at the scale of individual soil aggregates. MicrobiologyOpen 10:e1144
     [Google Scholar]
  131. 131.
    Tian B, Xie J, Fu Y, Cheng J, Li B et al. 2020. A cosmopolitan fungal pathogen of dicots adopts an endophytic lifestyle on cereal crops and protects them from major fungal diseases. ISME J 14:3120–35
     [Google Scholar]
  132. 132.
    Tijssen P, Penzes JJ, Yu Q, Pham HT, Bergoin M. 2016. Diversity of small, single-stranded DNA viruses of invertebrates and their chaotic evolutionary past. J. Invertebr. Pathol. 140:83–96
     [Google Scholar]
  133. 133.
    Turina M, Rostagno L. 2007. Virus-induced hypovirulence in Cryphonectria parasitica: still an unresolved conundrum. J. Plant Pathol. 89:165–78
     [Google Scholar]
  134. 134.
    Vainio EJ, Hakanpaa J, Dai Y-C, Hansen E, Korhonen K, Hantula J. 2011. Species of Heterobasidion host a diverse pool of partitiviruses with global distribution and interspecies transmission. Fungal Biol 115:1234–43
     [Google Scholar]
  135. 135.
    Vainio EJ, Hantula J 2018. Fungal viruses. Viruses of Microorganisms P Hyman, ST Abedon 193–209 Norfolk, UK: Caster Acad.
     [Google Scholar]
  136. 136.
    Vainio EJ, Pennanen T, Rajala T, Hantula J. 2017. Occurrence of similar mycoviruses in pathogenic, saprotrophic and mycorrhizal fungi inhabiting the same forest stand. FEMS Microbiol. Ecol. 93:fix003
     [Google Scholar]
  137. 137.
    van Lenteren JC, Bolckmans K, Kohl J, Ravensberg WJ, Urbaneja A. 2018. Biological control using invertebrates and microorganisms: plenty of new opportunities. Biocontrol 63:39–59
     [Google Scholar]
  138. 138.
    Walsh F, Duffy B. 2013. The culturable soil antibiotic resistome: a community of multi-drug resistant bacteria. PLOS ONE 8:e65567
     [Google Scholar]
  139. 139.
    Wang HL, Gonsalves D, Provvidenti R, Lecoq HL. 1991. Effectiveness of cross protection by a mild strain of zucchini yellow mosaic virus in cucumber, melon, and squash. Plant Dis 75:203–7
     [Google Scholar]
  140. 140.
    Wang X, Wei Z, Yang K, Wang J, Jousset A et al. 2019. Phage combination therapies for bacterial wilt disease in tomato. Nat. Biotechnol. 37:1513–20
     [Google Scholar]
  141. 141.
    Weitz JS, Poisot T, Meyer JR, Flores CO, Valverde S et al. 2013. Phage-bacteria infection networks. Trends Microbiol 21:82–91
     [Google Scholar]
  142. 142.
    Wuriyanghan H, Falk BW. 2013. RNA interference towards the potato psyllid, Bactericera cockerelli, is induced in plants infected with recombinant Tobacco mosaic virus (TMV). PLOS ONE 8:e66050
     [Google Scholar]
  143. 143.
    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]
  144. 144.
    Xu P, Liu Y, Graham RI, Wilson K, Wu K 2014. Densovirus is a mutualistic symbiont of a global crop pest (Helicoverpa armigera) and protects against a baculovirus and Bt biopesticide. PLOS Pathog 10:e1004490143
     [Google Scholar]
  145. 145.
    Yeh SD, Gonsalves D, Wang HL, Namba R, Chiu RJ. 1988. Control of papaya ringspot virus by cross protection. Plant Dis 72:375–80
     [Google Scholar]
  146. 146.
    Yu X, Li B, Fu Y, Jiang D, Ghabrial SA et al. 2010. A geminivirus-related DNA mycovirus that confers hypovirulence to a plant pathogenic fungus. PNAS 107:8387–92
     [Google Scholar]
  147. 147.
    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]
  148. 148.
    Zhang D-X, Nuss DL. 2016. Engineering super mycovirus donor strains of chestnut blight fungus by systematic disruption of multilocus vic genes. PNAS 113:2062–67
     [Google Scholar]
  149. 149.
    Zhang H, Xie J, Fu Y, Cheng J, Qu Z et al. 2020. A 2-kb mycovirus converts a pathogenic fungus into a beneficial endophyte for brassica protection and yield enhancement. Mol. Plant 13:1420–33
     [Google Scholar]
  150. 150.
    Zhang XF, Zhang SY, Guo Q, Sun R, Wei TY, Qu F. 2018. A new mechanistic model for viral cross protection and superinfection exclusion. Front. Plant Sci. 9:40
     [Google Scholar]
  151. 151.
    Zhou LL, Li XP, Kotta-Loizou I, Dong KL, Li SF et al. 2021. A mycovirus modulates the endophytic and pathogenic traits of a plant associated fungus. ISME J 15:1893–906
     [Google Scholar]
  152. 152.
    Ziebell H, Carr JP. 2010. Cross-protection: a century of mystery. Adv. Virus Res. 76:211–64
     [Google Scholar]
  153. 153.
    Ziebell H, MacDiarmid R. 2017. Prospects for engineering and improvement of cross-protective virus strains. Curr. Opin. Virol. 26:8–14
     [Google Scholar]
/content/journals/10.1146/annurev-phyto-021621-114208
Loading
Going Viral: Virus-Based Biological Control Agents for Plant Protection
Annual Review of Phytopathology 60, 21 (2022); https://doi.org/10.1146/annurev-phyto-021621-114208
/content/journals/10.1146/annurev-phyto-021621-114208
/content/journals/10.1146/annurev-phyto-021621-114208
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

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