SUMMARY. Currently, there are about six and a half thousand species of viruses known in the world, among which more than one and a half thousand are phytoviruses. Most plant viruses are capable of causing epiphytoties, which lead to decreased yields, reduced product quality, and sometimes put valuable commertial varieties or even entire plant species at risk of extinction. The glo-bal spread of viruses leads to the need to strengthen phytosanitary and quarantine restrictions, which re-quires additional financial costs. Understanding of the viral biology and the principles of their propagation is a key factor in the formation of strategies and methods of combating these pathogens. Among the newest ap-proaches are the genetic engineering technologies. Their use made it possible to create a number of plant varieties with increased resistance to viruses. However, the problem of creating virus-resistant plants still remains one of the most urgent, since with time viruses acquire the ability to bypass defense mechanisms and there is a need to obtain new resistant varieties. There are several main approaches for obtaining of transgenic plants with increased resistance to viruses. They are based on: RNA interference, resistance associated with viral capsid proteins, RNA-satellites, antisense RNAs, replicases, RNA-dependent RNA polymerase, the ac-tion of ribonucleases, ribosome-inactivating proteins, hammerhead ribozymes, miRNAs, plant antibodies, ets. One of the approaches to creating of virus-resistant plants is the use of ribonucleases genes. The genes encoding ribonucleases have different natural origin and belong to a wide range of hosts: bacteria, fungi, plants, animals. In particular, extracellular ribonucleases are able to cut non-specifically molecules of viral RNA in apoplast, that allows to create plants with increased resistance to various phytoviruses. This review is focused on the study of various genetic engineering approaches and the prospects of their use for the creation of virus-resistant plants. Emphasis is placed on the study of heterologous ribonuclease genes influence.
Keywords:

Full text and supplemented materials
Free full text: PDFReferences
Akbar, S., Wei, Y., and Zhang, M., RNA Interference: promising approach to combat plant viruses, Int. J. Mol. Sci., 2022, vol. 23, no. 10, p. 5312. https://doi.org/10.3390/ijms23105312
Akhter, M., Nakahara, K.S., and Masuta, C., Resistance induction based on the understanding of molecular interactions between plant viruses and host plants, Virol. J., 2021, vol. 18, p. 176. https://doi.org/10.1186/s12985-021-01647-4
Alam, I., Sharmin, S.A., Naher, M., et al., Elimination and detection of viruses in meristem-derived plantlets of sweet potato as a low-cost option toward commercialization, 3 Biotech, 2013, vol. 3, no. 2, pp. 153–164. https://doi.org/10.1007/s13205-012-0080-6
Ali, S., Ganai, B.A., Kamili, A.N., et al., Pathogenesis-related proteins and peptides as promising tools for engineering plants with multiple stress tolerance, Microbiol. Res., 2018, vols. 212–213, pp. 29–37. https://doi.org/10.1016/j.micres.2018.04.008
Andersen, E.J. and Ali, S., Byamukama, E., et al., Disease resistance mechanisms in plants, Genes (Basel), 2018, vol. 9, no. 7, p. 339. https://doi.org/10.3390/genes9070339
Ausubel, F.M., Are innate immune signaling pathways in plants and animals conserved?, Nat. Immunol., 2005, vol. 6, pp. 973–979. https://doi.org/10.1038/ni1253
Bald, J.G., Cytological evidence for the production of plant virus ribonucleic acid in the nucleus, Virology, 1964, vol. 22, no. 3, pp. 377–387. https://doi.org/10.1016/0042-6822(64)90028-5
Balint-Kurti, P., The plant hypersensitive response: concepts, control and consequences, Mol. Plant Pathol., 2019, vol. 20, pp. 1163–1178. https://doi.org/10.1111/mpp.12821
Bariola, P.A., MacIntosh, G.C., and Green, P.J., Regulation of S-like ribonuclease levels in Arabidopsis. Antisense inhibition of RNS1 or RNS2 elevates anthocyanin accumulation, Plant Physiol., 1999, vol. 119, no. 1, pp. 331–342. https://doi.org/10.1104%2Fpp.119.1.331
Beachy, R.N., Mechanisms and applications of pathogen-derived resistance in transgenic plants, Curr. Opin. Biotechnol., 1997, vol. 8, no. 2, pp. 215–220. https://doi.org/10.1016/S0958-1669(97)80105-XSi
Bevan, M.W., Flavell, R.B., and Chilton, M.D., A chimaeric antibiotic resistance gene as a selectable marker for plant cell transformation, Nature, 1983, vol. 304, no. 5922, pp. 184–187.
Bhattacharyya, D., Gnanasekaran, P., Kumar, R.K., et al., A geminivirus betasatellite damages the structural and functional integrity of chloroplasts leading to symptom formation and inhibition of photosynthesis, J. Exp Bot., 2015, vol. 66, no. 19, pp. 5881–5895. https://doi.org/10.1093/jxb/erv299
Bradamante, G., Mittelsten Scheid, O., and Incarbone, M., Under siege: virus control in plant meristems and progeny, Plant Cell, 2021, vol. 33, no. 8, pp. 2523–2537. https://doi.org/10.1093/plcell/koab140
Cao, X., Lu, Y., Di, D., et al., Enhanced virus resistance in transgenic maize expressing a dsRNA-specific endoribonuclease gene from E. coli, PLoS One, 2013, vol. 8, no. 10, pp. 1228–1232. https://doi.org/10.1371/journal.pone.0060829
Citores, L., Iglesias, R., and Ferreras, J.M., Antiviral activity of ribosome-inactivating proteins, Toxins, 2021, vol. 13, no. 2, p. 80. https://doi.org/10.3390/toxins13020080
Conti, G., Rodriguez, M.C., Manacorda, C.A., and Asurmendi, S., Transgenic expression of Tobacco mosaic virus capsid and movement proteins modulate plant basal defense and biotic stress responses in Nicotiana tabacum, Mol. Plant Microb. Interact., 2012, vol. 25, no. 10, pp. 1370–1384. https://doi.org/10.1094/MPMI-03-12-0075-R
Cosson, P., Schurdi-Levraud, V., Le, Q.H., et al., The RTM resistance to potyviruses in Arabidopsis thaliana: natural variation of the RTM genes and evidence for the implication of additional genes, PLoS One, 2012, vol. 7, no. 6, p. e39169. https://doi.org/10.1371/journal.pone.0039169
Deshpande, R.A. and Shankar, V., Ribonucleases from T2 family, Crit. Rev. Microbiol., 2002, vol. 28, no. 2, pp. 79–122. https://doi.org/10.1080/1040-840291046704
Ding, L.N., Li, Y.T., Wu, Y.Z., et al., Plant disease resistance-related signaling pathways: recent progress and future prospects, Int. J. Mol. Sci., 2022, vol. 23, no. 24, p. 16200. https://doi.org/10.3390/ijms232416200
Dodds, P.N. and Rathjen, J.P., Plant immunity: towards an integrated view of plant-pathogen interactions, Nat. Rev. Genet., 2010, vol. 11, pp. 539–548. https://doi.org/10.1038/nrg2812
Eleftherianos, I., Tafesh-Edwards, G., and Mohamed, A., Pathogen infection routes and host innate immunity: Lessons from insects, Immunol. Lett., 2022, vol. 247, pp. 46–51. https://doi.org/10.1016/j.imlet.2022.05.006
Flores, R., Highly abundant small interfering RNAs derived from a satellite RNA contribute to symptom attenuation by binding helper virus-encoded RNA silencing suppressors, Front. Plant Sci., 2016, vol. 7, p. 692 https://doi.org/10.3389/fpls.2016.00692
Gergerich, R.C. and Dolja V.V., Introduction to plant viruses, the invisible foe, Plant Health Instr., 2006. https://doi.org/10.1094/PHI-I-2006-0414-01
Golemboski, D.B., Lomonossoff, G.P., and Zaitlin, M., Plants transformed with a Tobacco mosaic virus nonstructural gene sequence are resistant to the virus, Proc. Natl. Acad. Sci. U. S. A., 1990, vol. 87, no. 16, pp. 6311–6315. https://doi.org/10.1073/pnas.87.16.6311
Grech-Baran, M., Witek, K., Szajko, K., et al., Extreme resistance to Potato virus Y in potato carrying the Ry sto gene is mediated by a TIR-NLR immune receptor, Plant Biotechnol. J., 2020, vol. 18, no. 3. https://doi.org/10.1111/pbi.13230
Green, P.J., The ribonucleases of higher plants, Ann. Rev. Plant Biol., 1994, vol. 45, no. 1, pp. 421–445. https://www.annualreviews.org/doi/pdf/10.1146/annurev.pp.45.060194.002225
Grout, B.W.W., Meristem-tip culture for propagation and virus elimination, in Methods In Molecular Biology, vol. 111: Plant cell culture protocols, Hall, R.D., Ed., Humana Press, 1999. https://doi.org/10.1385/1-59259-583-9:115
Gupta, N., Reddy, K., and Bhattacharyya, D., Plant responses to geminivirus infection: guardians of the plant immunity, Virol. J., 2021, vol. 18, no. 1, p. 143. https://doi.org/10.1186/s12985-021-01612-1
Hohn, T., Richert-Pöggeler, K.R., Staginnus, C., et al., Evolution of integrated plant viruses, Plant Virus Evol., 2008, pp. 53–81. https://doi.org/10.1007/978-3-540-75763-4_4
Hollings, M., Disease control through virus-free stock, Ann. Rev. Phytopathol., 1965, vol. 3, no. 1, pp. 367–396. https://www.annualreviews.org/doi/pdf/10.1146/annurev.py.03.090165.002055
Holmes, F.O., Inheritance of resistance to tobacco mosaic disease in tobacco, Phytopathology, 1938, vol. 28, no. 8, pp. 553–561. https://www.apsnet.org/edcenter/apsnetfeatures/Documents/2008/Holmes1938.pdf.
Huttner, E., Tucker, W., Vermeulen, A., et al., Ribozyme genes protecting transgenic melon plants against potyviruses, Curr. Issues Mol. Biol., 2001, vol. 3, no. 2, pp. 27–34. https://doi.org/10.21775/cimb.003.027
Jafarzade, M., Ramezani, M., Hedayati, F., et al., Antibody-mediated resistance to rhizomania disease in sugar beet hairy roots, Plant Pathol. J., 2019, vol. 35, no. 6, pp. 692–697. https://doi.org/10.5423/PPJ.OA.04.2018.0073
Jewehan, A., Salem, N., Tóth, Z., et al., Screening of Solanum (sections Lycopersicon and Juglandifolia) germplasm for reactions to the tomato brown rugose fruit virus (ToBRFV), J. Plant Dis. Prot., 2022, vol. 129, pp. 117–123. https://doi.org/10.1007/s41348-021-00535-x
Jiang, T. and Tao, Z., Unraveling the mechanisms of virus-induced symptom development in plants, Plants, 2023, vol. 12, no. 15, p. 2830. https://doi.org/10.3390/plants12152830
Johnson, A.M.A., Gopal, D.V.R.S., and Sudhakar, C., GM Crops for plant virus resistance: a review, in Genetically Modified Crops, 2020, pp. 257–337. https://doi.org/10.1007/978-981-15-5932-7_11
Kachroo, P., Yoshioka, K., Shah, J., et al., Resistance to turnip crinkle virus in Arabidopsis is regulated by two host genes and is salicylic acid dependent but NPR1, ethylene, and jasmonate independent, Plant Cell, 2000, vol. 12, pp. 677–690. https://doi.org/10.1105/tpc.12.5.677
Kochetov, A. and Shumny, V., Transgenic plants as genetic models for studying functions of plant genes, Russ. J. Genet.: Appl. Res., 2017, vol. 7, no. 4, pp. 421–427. https://doi.org/10.1134/S2079059717040050
Kumar, R. and Kanwar, S.S., Biotechnological production and applications of ribonucleases, in Bio-Technological Production of Bioactive Compounds, Verma, M.L. and Chandel, A.K., Eds., Elsevier, 2020, pp. 363–389. https://doi.org/10.1016/B978-0-444-64323-0.00012-6
Kumar, P., Chandra, S., and Sangeeta Srivastava, V.C., RGAs approach in identification of disease resistance genes and their deployment in crops improvement, Int. J. Appl. Agric. Res., 2017. https://www.ripublication.com/ijaar17/ijaarv12n2_08.pdf.
Kyrychenko, A.M. and Kovalenko, O.G., Basic engineering strategies for virus-resistant plants, Cytol. Genet., 2018, vol. 52, pp. 213–221. https://doi.org/10.3103/S0095452718030076
Lanfermeijer, F.C., Jiang, G., Ferwerda, M.A., et al., The durable resistance gene Tm-2 2 from tomato confers resistance against ToMV in tobacco and preserves its viral specificity, Plant Sci., 2004, vol. 167, no. 4, pp. 687–692. https://doi.org/10.1016/j.plantsci.2004.04.027
Langenberg, W., Zhang, L., Court, D., et al., Transgenic tobacco plants expressing the bacterial mc gene resist virus infection, Mol. Breed., 1997, vol. 3, pp. 391–399. https://doi.org/10.1023/A:1009697507261
Lapidot, M., Gafny, R., Ding, B., et al., A dysfunctional movement protein of Tobacco mosaic virus that partially modifies the plasmodesmata and limits virus spread in transgenic plants, Plant J., 1993, vol. 4, pp. 959–970. https://onlinelibrary.wiley.com/doi/pdf/10. 1046/j.1365-313X.1993.04060959.x
Lefeuvre, P., Martin, D., Elena, S.F., et al., Evolution and ecology of plant viruses, Nat. Rev. Microbiol., 2019, vol. 17, pp. 632–644. https://doi.org/10.1038/s41579-019-0232-3
Li, F. and Wang, A., RNA-targeted antiviral immunity: more than just RNA silencing, Trends Microbiol., 2019, vol. 27, no. 9, pp. 792–805. https://doi.org/10.1016/j.tim.2019.05.007
Lindbo, J. and Falk, W., The impact of “coat protein-mediated virus resistance” in applied plant pathology and basic research, Phytopathology, 2017, vol. 107, no. 6, pp. 624–634. https://doi.org/10.1094/PHYTO-12-16-0442-RVW
Lino, Y., Sugimoto, A., and Yamamoto, M., S. pombe pac1 +, whose overexpression inhibits sexual development, encodes a ribonuclease III-like RNase, EMBO, 1991, vol. 10, pp. 221–226. https://doi.org/10.1002/j.1460-2075.1991.tb07939.x
Liu, S., Chen, M., Li, R., et al., Identification of positive and negative regulators of antiviral RNA interference in Arabidopsis thaliana, Nat. Commun., 2022, vol. 13, no. 1, p. 2994 https://doi.org/10.1038/s41467-022-30771-0
MacIntosh, G.C. and Castandet, B., Organellar and secretory ribonucleases: major players in plant RNA homeostasis, Plant Physiol., 2020, vol. 183, no. 4, pp. 1438–1452. https://doi.org/10.1104/pp.20.00076
Mandadi, K.K. and Scholthof, K.B., Plant immune responses against viruses: how does a virus cause disease?, Plant Cell, 2013, vol. 5, pp. 1489–1505. https://doi.org/10.1105/tpc.113.111658
Manjunatha, L., Rajashekara, H., Uppala, L.S., et al., Mechanisms of microbial plant protection and control of plant viruses, Plants, 2022, vol. 11, no. 24, p. 3449. https://doi.org/10.3390/plants11243449
Marathe, R., Anandalakshmi, R., Liu, Y., and Dinesh-Kumar, S.P., The tobacco mosaic virus resistance gene, N, Mol. Plant Pathol., 2002, vol. 3, no. 3, pp. 167–172. https://doi.org/10.1046/j.1364-3703.2002.00110.x
Mengist, A.A. and Tenkegna, T.A., The role of miRNA in plant-virus interaction: a review, Mol. Biol. Rep., 2021, vol. 48, pp. 2853–2861. https://doi.org/10.1007/s11033-021-06290-4
Milosevic, S., Simonovic, A., Cingel, A., et al., Introduction of dsRNA-specific ribonuclease pac1 into Impatiens walleriana provides resistance to Tomato spotted wilt virus, Sci. Hortic., 2013, vol. 164, no. 17, pp. 499–506. https://doi.org/10.1016/j.scienta.2013.10.015
Monteiro, F. and Nishimura, M.T., Structural, functional, and genomic diversity of plant NLR proteins: an evolved resource for rational engineering of plant immunity, Ann. Rev. Phytopathol., 2018, vol. 56, pp. 243–267. https://doi.org/10.1146/annurev-phyto-080417-045817
Mushegian, A.R., Are there 1031 virus particles on Earth, or more, or fewer?, J. Bacteriol., 2020, vol. 202, no. 9, p. e00052-20. https://doi.org/10.1128/jb.00052-20
Musidlak, O., Nawrot, R., and Goździcka-Józefiak, A., Which plant proteins are involved in antiviral defense? Review on in vivo and in vitro activities of selected plant proteins against viruses, Int. J. Mol. Sci., 2017, vol. 18, no. 11, p. 2300. https://doi.org/10.3390/ijms18112300
Nejidat, A. and Beachy, R.N., Decreased levels of TMV coat protein in transgenic tobacco plants at elevated temperatures reduce resistance to TMV infection, Virology, 1989, vol. 73, no. 2, pp. 531–538. https://doi.org/10.1016/0042-6822(89)90565-5
Ogawa, T., Toguri, T., Kudoh, H., et al., Double-stranded RNA-specific ribonuclease confers tolerance against Chrysanthemum stunt viroid and Tomato spotted wilt virus in transgenic chrysanthemum plants, Breed. Sci., 2005a, vol. 55, no. 1, pp. 49–55. https://doi.org/10.1270/jsbbs.55.49
Ogawa, T., Toguri, T., Kudoh, H., et al., Transgenic potato expressing a double-stranded RNA-specific ribonucleases is resistant to Potato spindle tuber viroid, Breed. Sci., 2005b, vol. 15, no. 12, pp. 1290–1294. https://doi.org/10.1038/nbt1197-1290
Okada, K., Kato, T., Oikawa, T., et al., A genetic analysis of the resistance in barley to soil-borne wheat mosaic virus, Breed. Sci., 2020, vol. 70, no. 5, pp. 617–622. https://doi.org/10.1270/jsbbs.20071
Ovcharenko, O.O. and Rudas, V.A., Modern approaches to genetic engineering in the Orchidaceae family, Cytol. Genet., 2023, vol. 57, no. 2, pp. 142–156. https://doi.org/10.3103/S0095452723020093
Ovcharenko, O., Potrokhov, A., Sosnovska, D., et al., Increased virus resistance in transgenic petunia with heterologous ZRNaseII gene, JJBS, 2023, vol. 16, no. 4, pp. 587–592 https://doi.org/10.54319/jjbs/160403
Park, C.-J., Kim, K.-J., Shin, R., et al., Pathogenesis-related protein 10 isolated from hot pepper functions as a ribonuclease in an antiviral pathway, Plant J., 2003, vol. 37, no. 2, pp. 186–198. https://doi.org/10.1046/j.1365-313x.2003.01951.x
Parrella, G., Ruffel, S., Moretti, A., et al., Recessive resistance genes against potyviruses are localized in colinear genomic regions of the tomato (Lycopersicon spp.) and pepper (Capsicum spp.) genomes, Theor. Appl. Genet., 2002, vol. 105, pp. 855–861. https://doi.org/10.1007/s00122-002-1005-2
Perez, K., Yeam, I., Kang, B.C., et al., Tobacco etch virus infectivity in Capsicum spp. is determined by a maximum of three amino acids in the viral virulence determinant VPg, Mol. Plant-Microbe Interact., 2012, vol. 25, no. 12, pp. 1562–1573. https://doi.org/10.1094/MPMI-04-12-0091-R
Potrokhov, A., Sosnovska, D., Ovcharenko, O., et al., Increased ribonuclease activity in Solanum tuberosum L. transformed with heterologous genes of apoplastic ribonucleases as a putative approach for production of virus resistant plants, Turk. J. Biol., 2021, vol. 45, no. 1, pp. 79–87. https://doi.org/10.3906/biy-2007-87
Potrokhov, A., Sosnovskaya, D., and Ovcharenko, O., Antioxidant activity of petunias with the heterologous ribonuclease ZRNase II gene infected with tobacco mosaic virus, Innovative Biosyst. Bioeng., 2022, vol. 6, no. 1, pp. 40–45. https://doi.org/10.20535/ibb.2022.6.1.254464
Prasad, A., Sett, S., and Prasad, M., Plant-virus-abiotic stress interactions: A complex interplay, Environ. Exp. Bot., 2022, vol. 199, p. 104869. https://doi.org/10.1016/j.envexpbot.2022.104869
Prins, M., Laimer, M., Noris, E., et al., Strategies for antiviral resistance in transgenic plants, Mol. Plant Pathol., 2008, vol. 9, pp. 73–83. https://doi.org/10.1111/j.1364-3703.2007.00447.x
Pumplin, N. and Voinnet, O., RNA silencing suppression by plant pathogens: defence, counter-defence and counter-counter-defence, Nat. Rev. Microbiol., 2013, vol. 11, no. 11, pp. 745–760. https://doi.org/10.1038/nrmicro3120
Raines, R., Ribonuclease A, Chem Rev., 1998, vol. 98, no. 3, pp. 1045–1066. https://doi.org/10.1021/cr960427h
Rashid, A.H.A. and Lateef, D.D., Novel techniques for gene delivery into plants and its applications for disease resistance in crops, Am. J. Plant Sci., 2016, vol. 7, no. 1, pp. 181–193. https://doi.org/10.4236/ajps.2016.71019
Richard, M.M.S., Knip, M., Aalders, T., et al., Unlike many disease resistances, Rx1-mediated immunity to Potato virus X is not compromised at elevated temperatures, Front. Genet., 2020, vol. 11, p. 417. https://doi.org/10.3389/fgene.2020.00417
Rodríguez-Negrete, E.A., Carrillo-Tripp, J., and Rivera-Bustamante, R.F., RNA silencing against geminivirus: complementary action of posttranscriptional gene silencing and transcriptional gene silencing in host recovery, J. Virol., 2009, vol. 83, no. 3, pp. 1332–1340. https://doi.org/10.1128/JVI.01474-08
Ronde de D., Butterbach, P., and Kormelink, R., Dominant resistance against plant viruses, Front. Plant Sci., 2014, vol. 5, p. 307. https://doi.org/10.3389/fpls.2014.00307
Rubio, M., Martínez-Gómez, P., and Dicenta, F., Apricot breeding for multiple resistance to Plum pox virus and Apple chlorotic leaf spot virus, Sci. Hortic., 2023, vol. 309, p. 111706. https://doi.org/10.1016/j.scienta.2022.111706
Ruffel, S., Dussault, M.H., Palloix, A., et al., A natural recessive resistance gene against Potato virus Y in pepper corresponds to the eukaryotic initiation factor 4E (eIF4E), Plant J., 2002, vol. 32, no. 6, pp. 1067–1075. https://doi.org/10.1046/j.1365-313X.2002.01499.x
Ruffel, S., Gallois, J.L., Lesage, M.L., and Caranta, C., The recessive potyvirus resistance gene pot-1 is the tomato orthologue of the pepper pvr2-eIF4E gene, Mol. Genet. Genomics, 2005, vol. 274, pp. 346–353. https://doi.org/10.1007/s00438-005-0003-x
Saez, C., Flores-Leon, A., Montero-Pau, J., et al., RNA-Seq transcriptome analysis provides candidate genes for resistance to Tomato leaf curl New Delhi virus in melon, Front. Plant Sci., 2022, vol. 8, no. 12, p. 798858. https://doi.org/10.3389/fpls.2021.798858
Safarnejad, M.R, Jouzani, G.S., Tabatabaie, M., et al., Antibody-mediated resistance against plant pathogens, Biotechnol. Adv., 2011, vol. 29, pp. 961–971. https://doi.org/10.1016/j.biotechadv.2011.08.011
Salgotra, R.K. and Stewart, C.N., Functional markers for precision plant breeding, Int. J. Mol. Sci., 2020, vol. 21, no. 13, p. 4792. https://doi.org/10.3390/ijms21134792
Sangaev, S., Trifonova, E., Titov, S., et al., Effective expression of the gene encoding an extracellular ribonuclease of Zinnia elegans in the SR1 Nicotiana tabacum plants, Russ. J. Genet., 2007, vol. 43, no. 7, pp. 831–833. https://doi.org/10.1134/S1022795407070186
Sangaev, S., Kochetov, A., Ibragimova, S.S., et al., Physiological role of extracellular ribonucleases of higher plants, Russ. J. Genet.: Appl. Res., 2011, vol. 1, no. 1, pp. 44–50. https://doi.org/10.1134/S2079059711010060
Sano, T., Nagayama, A., Ogawa, T., et al., Transgenic potato expressing a double-stranded RNA-specific ribonucleases is resistant to potato spindle tuber viroid, Nat. Biotechnol., 1997, vol. 15, no. 12, pp. 1290–1294. https://doi.org/10.1038/nbt1197-1290
Scaria, V., Hariharan, M., Maiti, S., et al., Host-virus interaction: a new role for microRNAs, Retrovirology, 2006, vol. 3, p. 68. https://doi.org/10.1186/1742-4690-3-68
Sehrish, A., Wei, Y., and Zhang, M.-Q., RNA interference: promising approach to combat plant viruses, Int. J. Mol. Sci., 2022, vol. 23, no. 10, p. 5312. https://doi.org/10.3390/ijms23105312
Sekine, K., Kawakami, S., Hase, S., et al., High level expression of a virus resistance gene, RCY1, confers extreme resistance to Cucumber mosaic virus in Arabidopsis thaliana, Mol. Plant Microb. Interact., 2008, no. 11, pp. 1398–1407. https://doi.org/10.1094/MPMI-21-11-1398
Seo, Y.S., Rojas, M.R., Lee, J.Y., et al., A viral resistance gene from common bean functions across plant families and is up-regulated in a non-virus-specific manner, Proc. Natl. Acad. Sci. U. S. A., 2006, vol. 103, no. 32, pp. 11856–11861. https://doi.org/10.1073/pnas.0604815103
Shaikhaldein, H.O., Hoffmann, B., Alaraidh, I.A., et al., Evaluation of extreme resistance genes of Potato virus X (Rx1 and Rx2) in different potato genotypes, J. Plant Dis. Prot., 2018, vol. 125, pp. 251–257. https://doi.org/10.1007/s41348-018-0148-6
Sheat, S. and Winter, S., Developing broad-spectrum resistance in cassava against viruses causing the cassava mosaic and the cassava brown streak diseases, Front. Plant Sci., 2023, vol. 14, p. 1042701. https://doi.org/10.3389/fpls.2023.1042701
Shen, W.-X., Au, P.C.K., Shi, B.-J., et al., Satellite RNAs interfere with the function of viral RNA silencing suppressors, Front. Plant Sci., 2015, vol. 6, p. 281. https://doi.org/10.3389/fpls.2015.00281
Siar, S.V., Beligan, G.A., Sajise, A.J.C., et al., Papaya ringspot virus resistance in Carica papaya via introgression from Vasconcellea quercifolia, Euphytica, 2011, vol. 181, pp. 159–168. https://doi.org/10.1007/s10681-011-0388-z
Sindarovska, Y.R., Guzyk, O.I., Yuzvenko, L.V., et al., Ribonuclease activity of buckwheat plant (Fagopyrum esculentum) cultivars with different sensitivities to buckwheat burn virus, Ukr. Biochem. J., 2014, vol. 86, no. 3, pp. 33–40. https://doi.org/10.15407/ubj86.03.033
Sindelarova, M. and Sindelar, L., Isolation of pathogenesis-related proteins from TMV-infected tobacco and their influence on infectivity of TMV, Plant Prot. Sci., 2018, vol. 41, no. 2, pp. 52–57. https://doi.org/10.17221/2747-PPS
Singh, A., Taneja, J., Dasgupta I., Mukherjee S.K. Development of plants resistant to tomato geminiviruses using artificial trans-acting small interfering RNA, Mol. Plant Pathol., 2015, vol. 16, pp. 724–734. https://doi.org/10.1111/mpp.12229
Sugawara, T., Trifonova, E., Kochetov, A., and Kanayama, Y., Expression of an extracellular ribonuclease gene increases resistance to Cucumber mosaic virus in tobacco, BMC Plant Biol., 2016, vol. 16, no. 3, p. 246. https://doi.org/10.1186/s12870-016-0928-8
Takken, F.L.W., Albrecht, M., and Tameling, W.I.L., Resistance proteins: molecular switches of plant defence, Curr. Opin. Plant Biol., 2006, vol. 9, pp. 383–390. https://doi.org/10.1016/j.pbi.2006.05.009
Taninaka, Y., Nakahara, K.S., and Hagiwara-Komoda, Y., Intracellular proliferation of Clover yellow vein virus is unaffected by the recessive resistance gene cyv1 of Pisum sativum, Microbiol. Immunol., 2020, vol. 64, no. 1, pp. 76–82. https://doi.org/10.1111/1348-0421.12755
Tatineni, S. and Hein, G.L., Plant viruses of agricultural importance: current and future perspectives of virus disease management strategies, Phytopathology, 2023, vol. 113, no. 2, pp. 117–141. https://doi.org/10.1094/PHYTO-05-22-0167-RVW
Teixeira, R.M., Ferreira, M.A., Raimundo, G.A.S., and Fontes, E.P.B., Geminiviral triggers and suppressors of plant antiviral immunity, Microorganisms, 2021, vol. 9, no. 4, p. 775. https://doi.org/10.3390/microorganisms9040775
Trifonova, E., Sapotsky, M., Komarova, M., et al., Protection of transgenic tobacco plants expressing bovine pancreatic ribonuclease against Tobacco mosaic virus, Plant Cell Rep., 2007, vol. 26, no. 7, pp. 1121–1126. https://doi.org/10.1007/s00299-006-0298-z
Trifonova, E., Romanova, A., Sangaev, S., et al., Inducible expression of the gene of Zinnia elegans coding for extracellular ribonuclease in Nicotiana tabacum plants, Biol. Plant., 2012, vol. 56, pp. 571–574. https://doi.org/10.1007/s10535-011-0206-4
Varma, A., Integrated management of plant viral diseases, Ciba Foundation Symposium, Chichester: John Wiley & Sons, 1993, vol. 177, pp. 140–157. https://doi.org/10.1002/9780470514474.ch9
Verchot, J., Plant virus infection and the ubiquitin proteasome machinery: arms race along the endoplasmic reticulum, Viruses, 2016, vol. 8, no. 11, p. 314. https://doi.org/10.3390/v8110314
Verma, K.K., Song, X.P., Budeguer, F., et al., Genetic engineering: an efficient approach to mitigating biotic and abiotic stresses in sugarcane cultivation, Plant Signaling Behav., 2022, vol. 17, no. 1, p. 2108253. https://doi.org/10.1080/15592324.2022.2108253
Vicente, M., De Fazio, G., Menezes, M.E., and Golgher, R.R., Inhibition of plant viruses by human gamma interferon, J. Phytopathol., 1987, vol. 119, pp. 25–31. https://doi.org/10.1111/j.1439-0434.1987.tb04380.x
Wang, X., Kong, L., Zhi, P., and Chang, C., Update on cuticular wax biosynthesis and its roles in plant disease resistance, Int. J. Mol. Sci., 2020, vol. 21, no. 15, p. 5514. https://doi.org/10.3390/ijms21155514
Wang, M.R., Hamborg, Z., Blystad, D.R., and Wang, Q.C., Combining thermotherapy with meristem culture for improved eradication of onion yellow dwarf virus and shallot latent virus from infected in vitro-cultured shallot shoots, Ann. Appl. Biol., 2021, vol. 178, no. 3, pp. 442–449. https://doi.org/10.1111/aab.12646
Wang, W., Wang, J., Feng, X., et al., Breeding of virus-resistant transgenic sugarcane by the integration of the Pac1 gene, Front. Sustainable Food Syst., 2022, vol. 6, p. 925839. https://doi.org/10.3389/fsufs.2022.925839
Watanabe, T., Ogawa, H., Takahashi, I., et al., Resistance against multiple plant viruses in plants mediated by a double stranded-RNA specific ribonuclease, FEBS Lett., 1995, vol. 372, nos. 2–3, pp. 165–168. https://doi.org/10.1016/0014-5793(95)00901-K
Xie, Z., Fan, B., Chen, C., and Chen, Z., An important role of an inducible RNA-dependent RNA polymerase in plant antiviral defense, Proc. Natl. Acad. Sci. U. S. A., 2001, vol. 98, no. 11, pp. 6516–6521. https://doi.org/10.1073/pnas.111440998
Yang, Z. and Li, Y., Dissection of RNAi-based antiviral immunity in plants, Curr. Opin. Virol., 2018, vol. 32, pp. 88–99. https://doi.org/10.1016/j.coviro.2018.08.003
Yang, X., Niu, L., Zhang, W., et al. Increased multiple virus resistance in transgenic soybean overexpressing the double-strand RNA-specific ribonuclease gene PAC1, Transgenic Res., 2019, vol. 28, pp. 129–140. https://doi.org/10.1007/s11248-018-0108-8
Ye, Z.-H. and Droste, D.L., Isolation and characterization of cDNAs encoding xylogenesis-associated and wounding-induced ribonucleases in Zinnia elegans, Plant Mol. Biol., 1996, vol. 30, pp. 697–709. https://doi.org/10.1007/BF00019005
Younis, A., Siddique, M.I., Kim, C.K., and Lim, K.B., RNA Interference (RNAi) induced gene silencing: a promising approach of Hi-tech plant breeding, Int. J. Biol. Sci., 2014, vol. 10, no. 10, pp. 1150–1158. https://doi.org/10.7150/ijbs.10452
Zand Karimi, H. and Innes, R.W., Molecular mechanisms underlying host-induced gene silencing, Plant Cell, 2022, vol. 34, no. 9, pp. 3183–3199. https://doi.org/10.1093/plcell/koac165
Zhang, L., French, R., Langenberg, W., and Mitra, A., Accumulation of Barley stripe mosaic virus is significantly reduced in transgenic wheat plants expressing a bacterial ribonuclease, Transgenic Res., 2001, vol. 10, no. 1, pp. 13–19. https://doi.org/10.1023/a:1008931706679
Zhirnov, I.V., Trifonova, E.A., Romanova, A.V., et al., Induced expression of Serratia marcescens ribonuclease III gene in transgenic Nicotiana tabacum L. cv. SR1 tobacco plants, Russ. J. Genet., 2016, vol. 52, no. 11, pp. 1137–1141. https://doi.org/10.1134/S102279541611017X
Zhu, S., Jeong, R.-D., Lim, G.-H., et al., Double-stranded RNA-binding protein 4 is required for resistance signaling against viral and bacterial pathogens, Cell Rep., 2013, vol. 4, no. 6, pp. 1168–1184. https://doi.org/10.1016/j.celrep.2013.08.018
Zhu, M., Jiang, L., Bai, B., et al., The intracellular immune receptor sw-5b confers broad-spectrum resistance to tospoviruses through recognition of a conserved 21-amino acid viral effector epitope, Plant Cell, 2017, vol. 29, no. 9, pp. 2214–223. https://doi.org/10.1105/tpc.17.00180