Types of Relationships between Viruses and Their Hosts: Parasitism, Commensalism and Mutualism
DOI:
https://doi.org/10.24925/turjaf.v14i7.5078-5088.8651Keywords:
Virus-host interactions, Symbiosis, Metagenomics, Cryptic virus, SymbiogenesisAbstract
For many years, studies on viruses have primarily focused on understanding the etiology and pathogenesis of specific diseases. As a result, most of the viruses identified to date are known be pathogenic to their hosts. However, recent advancements in metagenomic techniques have shown that not all viruses are harmful; some may have commensal or mutualistic relationships with their hosts. In particular, studies on virus-host interactions indicated that some mutualistic viruses may contribute positively to their hosts by enhancing their development, strengthening their immune systems, and thus increasing resistance to both biotic and abiotic stress conditions. Certain types of viruses, such as cryptic viruses, are examples of commensalism because they can reside within host cells without causing any noticeable harmful effects. Some viruses may shift between various types of symbiotic relationships as they evolve along with their hosts. Currently, in relation to viruses, a definition of “symbiotic members of life” has been recognized. This review explores the symbiotic relationships between viruses and their hosts, categorizing them into parasitism, commensalism, and mutualism.
References
Abe, H., Tomitaka, Y., Shimoda, T., Seo, S., Sakurai, T., Kugimiya, S., Tsuda, S., & Kobayashi, M. (2011). Antagonistic Plant Defense System Regulated by Phytohormones Assists Interactions Among Vector Insect, Thrips and a Tospovirus. Plant and Cell Physiology, 53(1), 204-212. https://doi.org/10.1093/pcp/pcr173
Aguk, J. A., Karanja, N., Schulte-Geldermann, E., Bruns, C., Kinyua, Z., & Parker, M. (2018). Control of bacterial wilt (Ralstonia solanacearum) in potato (Solanum tuberosum) using rhizobacteria and arbuscular mycorrhiza fungi. African Journal of Food, Agriculture, Nutrition and Development, 18(2), 13371–13387. https://doi.org/10.4314/ajfand.v18i2
Al-Hamdani, S., Stoelting, A., & Morsy, M. (2014). Infuence of symbiosis between fungus, virus, and tomato plant in combating heat stress. Journal of Alabama Academy of Science, 85,150–160. https://doi.org/10.4236/ajps.2015.610163
Anonim, (2008). Zirai Mücadele Teknik Talimatları, Cilt: 4. T.C. Tarım ve Orman Bakanlığı, Tarımsal Araştırmalar ve Politikalar Genel Müdürlüğü. Ankara, 332 s.
Atiq, M., Zulfiqar, H., Rajput, N.A., Sahi, S.T., Abbas, W., Ahmad, S., Sultan, A., Usman, M., Jabbar, A., Ghaffar, A., Aimen, T., Wasi-Ud, D. (2022). Bacterial wilt of cucumber: An emerging threat to cucumber production in Pakistan. Plant Cell Biotechnology and Molecular Biology, 23 (23-24):54–65. https://doi.org/10.56557/pcbmb/2022/v23i23-247717.
Barr, J. J., Auro, R., Furlan, M., Whiteson, K. L., Erb, M. L., Pogliano, J., Stotland, A., Wolkowicz, R., Cutting, A. S., Doran, K. S., Salamon, P., Youle, M., & Rohwer, F. (2013). Bacteriophage adhering to mucus provide a non-host-derived immunity. Proceedings of the National Academy of Sciences of the United States of America, 110(26), 10771e10776. http://doi.org/10.1073/pnas.1305923110.
Begum, N., Qin, C., Ahanger, M. A., Raza, S., Khan, M. I., Ashraf, M., Ahmed, N., & Zhang, L. (2019). Role of Arbuscular Mycorrhizal Fungi in Plant Growth Regulation: Implications in Abiotic Stress Tolerance. Frontiers in Plant Science, 10, 1068. https://doi.org/10.3389/fpls.2019.01068
Belliure, B., Janssen, A., Maris, P. C., Peters, D., & Sabelis, M. W. (2004). Herbivore arthropods benefit from vectoring plant viruses. Ecology Letters, 8(1),70–79. https://doi.10.1111/j.1461-0248.2004.00699.x
Belshaw, R., Pereira, V., Katzourakis, A., Talbot, G., Paces, J., Burt, A., & Tristem, M. (2004). Long-term reinfection of the human genome by endogenous retroviruses. Proceedings of the National Academy of Sciences, 101(14), 4894–4899. https://doi.org/10.1073/pnas.0307800101
Bézier, A., Annaheim, M., Herbinière, J., Wetterwald, C., Gyapay, G., Bernard-Samain, S., Wincker, P., Roditi, I., Heller, M., Belghazi, M., Pfister-Wilhem, R., Periquet, G., Dupuy, C., Huguet, E., Volkoff, A. N., Lanzrein, B., & Drezen, J. M. (2009). Polydnaviruses of braconid wasps derive from an ancestral nudivirus. Science (New York, N.Y.), 323(5916), 926e930. https://doi.org/10.1126/science.1166788
Blinov, V. M., Zverev, V. V., Krasnov, G. S., Filatov, F. P., & Shargunov, A. V. (2017). Viral component of the human genome. Molecular Biology, 51(2), 205–215. https://doi.org/10.1134/s0026893317020066
Boccardo, G., Lisa, V., Luisoni, E., & Milne, R. (1987). Cryptic plant viruses. Advances in Virus Research, 33, 171 –214. https://doi.org/10.1016/S0065-3527(08)60477-7
Brown, P.O. (1997). Integration. (Eds: J.M. Coffin, S.H. Hughes, H.E. Varmus). Retroviruses. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press. https://www.ncbi.nlm.nih.gov/books/NBK19392/
Chatzivassiliou, E. K., Nagata, T., Katis, N. I., & Peters, D. (1999). Transmission of tomato spotted wilt tospovirus by Thrips tabaci populations originating from leek. Plant Pathology, 48, 700–706. https://doi.org/10.1046/j.1365-3059.1999.00414.x
Chinnaiah, S., Gautam, S., Herron, B., Workneh, F., Rush, C. M., & Gadhave, K. R. (2023). Novel strains of a pandemic plant virus, tomato spotted wilt orthotospovirus, increase vector fitness and modulate virus transmission in a resistant host. Frontiers in Microbiology, 14, 1257724. https://doi.10.3389/fmicb.2023.1257724
Chuong, E. B. (2018). The placenta goes viral: Retroviruses control gene expression in pregnancy. PLoS Biology, 16(10), e3000028. https://doi.org/10.1371/journal.pbio.3000028
Crawford, D.H. (2011). ‘What are viruses?’. (D.H. Crawford, Ed), Viruses: A Very Short Introduction, 1st edn, Very Short Introduction Series, Volume: 276. Oxford University Press, p.156 https://doi.org/10.1093/actrade/9780199574858.003.000
Dheilly, N. M., Maure, F., Ravallec, M., Galinier, R., Doyon, J., Duval, D., Leger, L., Volkoff, A. N., Misse, D., Nidelet, S., Demolombe, V., Brodeur, J., Gourbal, B., Thomas, F., & Mitta, G. (2015). Who is the puppet master? Replication of a parasitic wasp-associated virus correlates with host behaviour manipulation. Proceedings of the Royal Society B: Biological Sciences, 282(1803), 20142773–20142773. https://doi.org/10.1098/rspb.2014.2773
Dilmen, H. (2025). Identification of the Parasitoid Wasp Dinocampus coccinellae (Schrank) (Hymenoptera: Braconidae) in Pistachio Orchards Using DNA Barcoding. Turkish Journal of Agricultural and Natural Sciences, 12 (2), 276–284. https://doi.org/10.30910/turkjans.1531632
Dunlap, K. A., Palmarini, M., Varela, M., Burghardt, R. C., Hayashi, K., Farmer, J. L., & Spencer, T. E. (2006). Endogenous retroviruses regulate periimplantation placental growth and differentiation. Proceedings of the National Academy of Sciences of the United States of America, 103(39),14390e14395. https://doi.org/10.1073/pnas.0603836103
Dupressoir, A., Vernochet, C., Bawa, O., Harper, F., Pierron, G., Opolon, P., & Heidmann, T. (2009). Syncytin-A knockout mice demonstrate the critical role in placentation of a fusogenic, endogenous retrovirus-derived, envelope gene. Proceedings of the National Academy of Sciences of the United States of America, 106(29), 12127e12132. https://doi.org/10.1073/pnas.0902925106.
Espagne, E., Dupuy, C., Huguet, E., Cattolico, L., Provost, B., Martins, N., Poirié, M., Periquet, G., & Drezen, J. M. (2004). Genome sequence of a polydnavirus: insights into symbiotic virus evolution. Science (New York, N.Y.), 306(5694), 286e289. https://doi.org/10.1126/science.1103066
Ghosh, A., Das, A., Vijayanandaraj, S., & Mandal, B. (2015). Cardamom bushy dwarf virus infection in large cardamom alters plant selection preference, life stages, and fecundity of aphid vector, Micromyzus kalimpongensis (Hemiptera: Aphididae). Environmental Entomology, 45, 178–184. https://doi.org/10.1093/ee/nvv161
Gilbert, K. B., Holcomb, E. E., Allscheid, R. L., & Carrington, J. C. (2019). Hiding in plain sight: New virus genomes discovered via a systematic analysis of fungal public transcriptomes. PLoS One, 14(7), e0219207. https://doi.org/10.1371/journal.pone.0219207
González, R., Butković, A., Escaray, F. J., Martínez-Latorre, J., Melero, I., Pérez-Parets, E., Gómez-Cadenas, A., Carrasco, P., & Elena, S. F. (2021). Plant virus evolution under strong drought conditions results in a transition from parasitism to mutualism, Proceedings of the National Academy of Sciences of the United States of America, 118(6), e2020990118. https://doi.org/10.1073/pnas.2020990118
Guo, T. X., Xuan, J., Zhang, J., & Zhou, J. Y. (2023). The mutually beneficial relationship between ants and aphids discussed from the perspectives of biology and biochemistry, Molecular Entomology, 14(1), 1-8. https://doi: 10.5376/me.2023.14.0001
Guy, P. L., & Gerard, P. J. (2016). White clover cryptic virus-1 in New Zealand and eastern Australia. Annals of Applied Biology, 168(2), 225-231. https://doi.org/10.1111/aab.12258
Herniou, E. A., Huguet, E., Thézé, J., Bézier, A., Periquet, G., & Drezen, J. M. (2013). When parasitic wasps hijacked viruses: genomic and functional evolution of polydnaviruses. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 368(1626), 20130051. https://doi.org/10.1098/rstb.2013.0051
Hasiów-Jaroszewska, B., Boezen, D,, Zwart, M.P. (2021). Metagenomic studies of viruses in weeds and wild plants: A powerful approach to characterise variable virus communities. Viruses, 13(10):1939. https://doi.org/10.3390/v13101939
Jagdale, S. S., & Joshi, R. S. (2018). Enemies with benefits: mutualistic interactions of viruses with lower eukaryotes. Archives of Virology, 163, 821–830. https://doi.org/10.1007/s00705-017-3686-5
Kernbauer, E., Ding, Y., & Cadwell, K. (2014). An enteric virus can replace the beneficial function of commensal bacteria. Nature, 516(7529), 94–98. https://doi.org/10.1038/nature13960
Khankhum, S., & Valverde, R. A. (2018). Physiological traits of endornavirus-infected and endornavirus-free common bean (Phaseolus vulgaris) cv Black Turtle Soup. Archives of Virology, 163(4), 1051-1056. https://doi.org/10.1007/s00705-018-3702-4
Konuş, M., & Uğurlu Karaağaç, S. (2014). Adana’da Pamukta Yeşilkurt [Helicoverpa armigera (Hübner)]’un İnsektisitlere Karşı Dayanıklılık Oranlarının Belirlenmesi. Anadolu Tarım Bilim. Dergisi, 29(2),106-112. https://doi.org/10.7161/anajas.2014.29.2.106-112
Koyama, S., & Majerus, M. E. (2008). Interactions between the parasitoid wasp Dinocampus coccinellae and two species of coccinellid from Japan and Britain. BioControl, 53(1), 253-264. https://doi.org/10.1007/978-1-4020-6939-0_17
Kumari, R., Bhardwaj, P., Singh, L., Zaidi, A.A., Hallan, V. (2013). Biological and molecular characterization of cucumber mosaic virus Subgroup II isolate causing severe mosaic in cucumber. Indian Journal of Virology, 24(1):27-34. https://doi.org/10.1007/s13337-012-0125-9
Leng, C., Mengyan, H., Yongmei, X., & Chen, J. (2024). 1 Perspective and challenges of mycorrhizal symbiosis in orchid medicinal plants. Chinese Herbal Medicines, 6(2), 172-179. https://doi.org/10.1016/j.chmed.2024.03.001
Leung, T. L., & Poulin, R. (2008). Parasitism, commensalism, and mutualism: exploring the many shades of symbioses. Vie et Milieu/Life & Environment, 58 (2), 107-115.
Lu, H., Zhu, J., Yu, J., Chen, X., Kang, L., & Cui, F. (2019). A Symbiotic Virus Facilitates Aphid Adaptation to Host Plants by Suppressing Jasmonic Acid Responses, Molecular Plant-Microbe Interactions, 33(1), 55-65. https://doi.10.1094/MPMI-01-19-0016-R
Maris, P. C., Joosten, N. N., Goldbach, R. W., & Peters, D. (2004). Tomato spotted wilt virus infection improves host suitability for its vector Frankliniella occidentalis. Phytopathology, 94, 706–711. https://doi.10.1094/PHYTO.2004.94.7.706
Márquez, L. M., Redman, R. S., Rodriguez, R. J., & Roossinck, M. J. (2007). A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance. Science, 315, 513–515. https://doi.org/10.1126/science.1136237
Miest, T. S., & Cattaneo, R. (2014). New viruses for cancer therapy: meeting clinical needs. Nature Reviews Microbiology, 12(1), 23–34. https://doi.org/10.1038/nrmicro3140
Morales-Vargas, A. T., López-Ramírez, V., Álvarez-Mejía, C., & Vázquez-Martínez, J. (2024). Endophytic fungi for crops adaptation to abiotic stresses. Microorganisms, 12, 1357. https://doi.org/10.3390/microorganisms12071357
Moreno, A., & Fereres, A. (2012). Virus diseases in lettuce in the Mediterranean Basin. G. Loebenstein & H. Lecoq (Eds.), Viruses and virus diseases of vegetables in the Mediterranean Basin Advances in Virus Research, Vol. 84, pp. 247–288. Academic Press.https://doi.org/10.1016/b978-0-12-394314-9.00007-5
Nibert, M. L., Ghabrial, S. A., Maiss, E., Lesker, T., Vainio, E. J., Jiang, D., & Suzuki, N. (2014). Taxonomic reorganization of family Partitiviridae and other recent progress in partitivirus research. Virus Research, 188, 128-141. https://doi.org/10.1016/j.virusres.2014.04.007
Nilon, A., Robinson, K., Pappu, H. R., & Mitter, N. (2021). Current status and potential of RNA interference for the management of tomato spotted wilt virus and thrips vectors. Pathogens, 10(3), 320. https://doi.org/10.3390/pathogens10030320
Novgorodova T.A. (2004). Simbioticheskie vzaimootnosheniia murav'ev i tleĭ [Symbiotic relationships between ants and aphids]. Zhurnal Obshchei Biologii, 65(2),153-166 (Rusca). [Abstract: İngilizce]
Ogada, P. A., Maiss, E., & Poehling, H. M. (2013). Influence of tomato spotted wilt virus on performance and behaviour of western flower thrips (Frankliniella occidentalis). Journal of Applied Entomology, 137, 488–498. https://doi.10.1111/jen.12023
Oliver, K. M., & Higashi, C. H. V. (2019). Variations on a protective theme: Hamiltonella defensa infections in aphids variably impact parasitoid success. Current Opinion in Insect Science, 32, 1-7. https://doi.org/10.1016/j.cois.2018.08.009
Oliver, K. M., Degnan, P. H., Hunter, M. S., & Moran, N. A. (2009). Bacteriophages encode factors required for protection in a symbiotic mutualism. Science (New York, N.Y.), 325(5943), 992-994. https://doi.org/10.1126/science.1174463
Pappu, H. R., Jones, R. A. C., & Jain, R. K. (2009). Global status of tospovirus epidemics in diverse cropping systems: successes achieved and challenges ahead. Virus Research, 141, 219–236. https://doi10.1016/j.virusres.2009.01.009
Parato, K. A., Senger, D., Forsyth, P. A., & Bell, J. C. (2005). Recent progress in the battle between oncolytic viruses and tumours. Nature Reviews Cancer, 5(12), 965–976. https://doi.org/10.1038/nrc1750
Pazarlar, S., & Şimşek, E. (2024). The endophytic fungus Serendipita indica colonization protects chickpea plants against Fusarium wilt disease. Ege Üniversitesi. Ziraat Fakültesi Dergisi, 61(4), 449-459, https://doi.org/10.20289/zfdergi.1461733
Pradeu, T. (2016). Mutualistic viruses and the heteronomy of life. Studies in History and Philosophy of Biological and Biomedical Sciences, 59, 80-88. https://doi.org/10.1016/j.shpsc.2016.02.007
Prasch, C.M & Sonnewald, U. (2013). Simultaneous application of heat, drought, and virus to Arabidopsis plants reveals significant shifts in signaling networks. Plant Physiology, 162, 1849–1866. https://doi. 0.1104/pp.113.221044
Prell, J., White, J. P., Bourdes, A., Bunnewell, S., Bongaerts, R. J., & Poole, P. S. (2009). Legumes regulate Rhizobium bacteroid development and persistence by the supply of branched-chain amino acids. Proceedings of the National Academy of Sciences, 106 (30), 12477-12482. https://doi.org/10.1073/pnas.0903653106
Priscáková, P., Svoboda, M., Feketová, Z., Hutník, J., Repiská, V., Gbelcová, H. & Gergely, L. (2023). Syncytin-1, syncytin-2 and suppressyn in human health and disease. Journal of Molecular Medicine, 101(12):1527-1542. https://doi.10.1007/s00109-023-02385-6
Provorov, N. A. (2018). Symbiogenesis as Evolution of Open Genetic Systems. Russian Journal of Genetics, 54(8), 888–896. https://doi.org/10.1134/S1022795418080100
Relman, D. A. (2008). 'Til death do us part': coming to terms with symbiotic relationships. Forward. Nature Reviews Microbiology, 6(10),721-4. https://doi.org/10.1038/nrmicro1990
Roossinck, M. J. & Bazan, E.R. (2017). Symbiosis: Viruses as Intimate Partners. The Annual Review of Virology, 4, 123-139. https://doi.org/10.1146/annurev-virology-110615-042323
Roossinck, M. J. (2008). Symbiosis, mutualism and symbiogenesis. In Plant Virus Evolution (pp. 157-164). Springer Berlin Heidelberg. https://doi.org/10.1007/978-3-540-75763-4_9
Roossinck, M. J. (2011). The good viruses: viral mutualistic symbioses. Nature Reviews Microbiology, 9, 99–108. https://doi.org/10.1038/nrmicro2491
Roossinck, M. J. (2015). Plants, viruses and the environment: ecology and mutualism. Virology, 479, 271–277. https://doi.org/10.1016/j.virol.2015.03.041
Roossinck, M. J., Martin, D. P. & Roumagnac, P. (2015). Plant Virus Metagenomics: Advances in Virus Discovery. Phytopathology, 105(6): 716-727. https://doi.org/10.1094/PHYTO-12-14-0356-RVW
Sarı, M., Karanfil, A., & Korkmaz, S. (2024). Determination of Zucchini Yellow Mosaic Virus and Watermelon Mosaic Virus Infections in Cucurbit Production Areas of Çanakkale Province from Türkiye. Turkish Journal of Agriculture-Food Science and Technology, 12(1): 2097-2103. https://doi.org/10.24925/turjaf.v12is1.2097-2103.7114
Sastry, K. S., & Zitter, T. A. (2014). Management of virus and viroid diseases of crops in the tropics. Plant Virus and Viroid Diseases in The Tropics: Epidemiology and Management, K.S. Sastry, T.A. Zitter (EDs), Vol. 2 (pp. 149-480). Dordrecht: Springer Netherlands. https://doi.org/10.1007/978-94-007-7820-7_2
Scholthof, K. B., Adkins, S., Czosnek, H., Palukaitis, P., Jacquot, E., Hohn, T., Hohn, B., Saunders, K., Candresse, T., Ahlquist, P., Hemenway, C., & Foster, G. D. (2011). Top 10 plant viruses in molecular plant pathology. Molecular Plant Pathology, 12(9), 938-954. https://doi:10.1111/j.1364-3703.2011.00752.x
Shamsudin, N. A., Sathiya Seelan, J. S., Gansau, J. A., & Rusdi, N. A. (2024). A review: Molecular identification of orchid mycorrhiza. Advances in Horticultural Science, 38(1), 97–116. https://doi.org/10.36253/ahsc-14952
Shapiro, L. R., Salvaudon, L., Mauck, K. E., Pulido, H., De Moraes, C. M., Stephenson, A. G., & Mescher, M. C. (2013). Disease Interactions in a Shared Host Plant: Effects of Pre-Existing Viral Infection on Cucurbit Plant Defense Responses and Resistance to Bacterial Wilt Disease. PLoS ONE, 8(10), e77393. https://doi.org/10.1371/journal.pone.0077393
Shrestha, A., Srinivasan, R., Riley, D. G., & Culbreath, A. K. (2012). Direct and indirect effects of a thrips-transmitted Tospovirus on the preference and fitness of its vector, Frankliniella fusca. Entomologia Experimentalis et Applicata, 145, 260–271. https://doi.10.1111/eea.12011
Stumpf, C. F. & Kennedy, G.G. (2005). Effects of tomato spotted wilt virus (TSWV) isolates, host plants, and temperature on survival, size, and development time of Frankliniella fusca. Entomologia Experimentalis et Applicata, 114, 215–225. https://doi.10.1111/j.1570-7458.2005.00251.x
Takahashi, H., Xu, N., Kanayama, Y., Tabara, M., Takeda, A., Fukuhara, T., & Miyashita, S. (2025). Latent infection of Vigna unguiculata with seed-borne bean common mosaic virus modulates plant growth and may contribute to mutualistic symbiosis between the virus host plant. Frontiers in Microbiology, 16, 1524787. https://doi.10.3389/fmicb.2025.152478
Tatineni, S. & Hein, G.L. (2023). Plant Viruses of Agricultural Importance: Current and Future Perspectives of Virus Disease Management Strategies. Phytopathology, 113(2), 117-141. https://doi.10.1094/PHYTO-05-22-0167-RVW
Tillmann, H. L., Heiken, H., Knapik-Botor, A., Heringlake, S., Ockenga, J., & Wilber, J. C. (2001). Infection with GB Virus C and Reduced Mortality among HIV-Infected Patients. New England Journal of Medicine, 345(10), 715–724. https://doi.org/10.1056/NEJMoa010398
Ullman, D. E., Sherwood, J. L., & German, T. L. (1997). Thrips as vectors of plant pathogens. T. Lewis (Eds.), Thrips as Crop Pests (pp. 539–565). CAB International.
Van den Heuvel, J. F., Hummelen, H., Verbeek, M., Dullemans, A. M., & van der Wilk, F. (1997). Characteristics of acyrthosiphon pisum virus, a newly identified virus infecting the pea aphid. Journal of Invertebrate Pathology, 70(3), 169-76. https://doi.10.1006/jipa.1997.4691
Van der Heijden, M. G. A., Martin, F. M., Selosse, M. A., & Sanders, I. R. (2015). Mycorrhizal ecology and evolution: The past, the present, and the future. New Phytologist, 205(4), 1406-1423. https://doi.org/10.1111/nph.13288
Wan, Y., Hussain, S., Merchant, A., Xu, B., Xie, W., Wang, S., Zhang, Y., Zhou, X., & Wu, Q. (2020). Tomato spotted wilt orthotospovirus influences the reproduction of its insect vector, western flower thrips, Frankliniella occidentalis, to facilitate transmission. Pest Management Science, 76, 2406–2414. https://doi.10.1002/ps.5779
Walker P.J., Siddell, S.G., Lefkowitz, E.J., Mushegian, A.R., Adriaenssens, E.M., Alfenas-Zerbini, P., Davison, A.J., Dempsey, D.M., Dutilh, B.E., García, M.L., Harrach, B., Harrison, R.L., Hendrickson, R.C., Junglen, S., Knowles, N.J., Krupovic, M., Kuh, J.H., Lambert, A.J., Łobocka, M., Nibert, M.L., Oksanen, H.M., Orton, R.J., Robertson, D.L., Rubino, L., Sabanadzovic, S., Simmonds, P., Smith, D.B., Suzuki, N., Van Dooerslaer, K., Vandamme, A.M., Varsani, A., Zerbini, F.M. (2021). Changes to virus taxonomy and to the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses (2021). Archives of Virology, 166(9), 2633–2648. https://doi.org/10.1007/s00705-021-05156-1
Weldon, S. R., & Oliver, K. M. (2016). Diverse Bacteriophage Roles in an Aphid-Bacterial Defensive Mutualism. In: Hurst, C. (Eds.) The Mechanistic Benefits of Microbial Symbionts. Advances in Environmental Microbiology, 2, 173-206. Springer, Cham. https://doi.org/10.1007/978-3-319-28068-4_7
Weng, W., Yan, J., Zhou, M., Yao, X., Gao, A., Ma, C., Cheng, J., & Ruan, J. (2022). Roles of Arbuscular mycorrhizal Fungi as a Biocontrol Agent in the Control of Plant Diseases. Microorganisms, 10(7), 1266. https://doi.org/10.3390/microorganisms10071266
Whitfield, A. E., Ullman, D. E., & German, T. L. (2005). Tospovirus-thrips interactions. Annual Review of Phytopathology, 43, 459–489. https://doi.10.1146/annurev.phyto.43.040204.140017
Xu, P., Chen, F., Mannas, J. P., Feldman, T., Sumner, L. W., & Roossinck, M. J. (2008). Virus infection improves drought tolerance. New Phytologist, 180, 911– 921. https://doi.org/10.1111/j.1469-8137.2008.02627.x
Xu, P., Liu, Y., Graham, R. I., 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 Pathogens, 10: e1004490. https://doi.org/10.1371/journal.ppat.1004490
Yang, L., Qiu, L. M., Fang, Q., Stanley, D. W., & Ye, G. Y. (2021). Cellular and humoral immune interactions between Drosophila and its parasitoids. Insect Science, 28(5), 1208-1227. https://doi.org/10.1111/1744-7917.12863
Yücel, S., & Genç, H. (2018). Çanakkale İli Domates Ekim Alanlarındaki Yeşil Kurt, Helicoverpa armigera Hübner (Lepidoptera:Noctuidae)’nın Yayılışı ve Bulaşıklık Durumunun Belirlenmesi. Çanakkale Onsekiz Mart Üniversitesi Ziraat Fakültesi Dergisi, 6 (Özel Sayı), 115–122. https://doi.org/10.33202/comuagri.503914
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