Цитологія і генетика 2023, том 57, № 6, 82-109
Cytology and Genetics 2023, том 57, № 6, 587–610, doi: https://www.doi.org/https://doi.org/10.3103/S0095452723060026

Використання технології РНК-інтерференції для поліпшення господарсько-корисних ознак злакових культур

Дубровна О.В., Михальська С.І., Комісаренко А.Г.

  • Інститут фізіології рослин і генетики НАН України, вул. Васильківська 31/17, Київ, 03022, Україна

РНК-інтерференція (РНКі) являє собою новий потенційний інструмент для селекції рослин шляхом впровадження невеликих некодуючих послідовностей РНК із можливістю глушіння експресії генів специфічним для послідовності способом. Здатність до зниження експресії певного гена забезпечує можливість набуття нової характеристики шляхом елімінації або накопичення певних ознак рослин, що приводить до біохімічних або фенотипових змін, яких не мають вихідні рослини. У даному огляді літератури описано досягнутий за останні десятиріччя прогрес у застосуванні РНКі для створення злакових культур з поліпшеними господарсько-цінними ознаками. Коротко представлені основні етапи механізму глушіння генів, опосередкованого короткими інтерферуючими РНК (кіРНК), особливості їхнього біогенезу, спосіб дії та розповсюдження. Узагальнено численні приклади розробки різних біотехнологічних підходів до поліпшення злаків з використанням трансформації генів та екзогенних дволанцюгових молекул РНК (длРНК). Висвітлено можливості застосування технології РНКі для зміни агрономічних ознак рослин, підвищення харчової цінності та якості зерна, зменшення кількості токсичних сполук та алергенів. Значна увага приділена практичним  результатам різноманітного застосування РНКі для  підвищення стійкості зернових культур до біотичних стресових чинників, зокрема таких як віруси, бактерії, гриби, комахи-шкідники, нематоди. Наводяться приклади використання РНКі, опосередкованої кіРНК, для покращення резистентності зернових до абіотичних стресів, зокрема посухи та засолення.

Ключові слова: злакові культури, РНК-інтерференція, трансгенні рослини, агрономічні ознаки, якість зерна, стійкість до абіотичних та біотичних стресі

Цитологія і генетика
2023, том 57, № 6, 82-109

Current Issue
Cytology and Genetics
2023, том 57, № 6, 587–610,
doi: https://doi.org/10.3103/S0095452723060026

Повний текст та додаткові матеріали

Цитована література

Abdellatef, E., Will, T., Koch, A., et al., Silencing the expression of the salivary sheath protein causes transgenerational feeding suppression in the aphid Sitobion avenae, Plant Biotechnol. J., 2015, vol. 13, no. 6, pp. 849–857. https://doi.org/10.1111/pbi.12322

Abdellatef, E., Kamal, N.M., and Tsujimoto, H., Tuning beforehand: A foresight on RNA interference (RNAi) and in vitro-derived dsRNAs to enhance crop resilience to biotic and abiotic stresses, Int. J. Mol. Sci., 2021, vol. 22, p. 7687. https://doi.org/10.3390/ijms22147687

Ahmed, M.M.S., Bian, S., Wang, M., et al., RNAi-mediated resistance to rice black-streaked dwarf virus in transgenic rice, Transgenic Res., 2017, vol. 26, no. 2, pp. 197–207. https://doi.org/10.1007/s11248-016-9999-4

Akbar, S., Tahir, M., Wang, M.B., and Liu, Q., Expression analysis of hairpin RNA carrying Sugarcane mosaic virus (SCMV) derived sequences and transgenic resistance development in a model rice plant, Biomed. Res. Int., 2017, p. 1646140. https://doi.org/10.1155/2017/1646140

Akbar, S., 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

Ali, N., Datta, N., and Datta, K., RNA interference in designing transgenic crops GM, Crops, 2010, vol. 1, no. 4, pp. 207–213. https://doi.org/10.4161/gmcr.1.4.13344

Ali, N., Paul, S., Gayen, D., Sarkar, S.N., and Datta, K., Development of low phytate rice by RNAi mediated seed-specific silencing of inositol 1,3,4,5,6-pentakisphosphate 2-kinase gene (IPK1), PLoS One, 2013à, vol. 8, no. 7, p. e68161. https://doi.org/10.1371/journal.pone.0068161

Ali, N., Paul, S., Gayen, D., et al., RNAi mediated down regulation of myo-inositol-3-phosphate synthase to generate low phytate rice, Rice, 2013b, vol. 6, p. 12. https://doi.org/10.1186/1939-8433-6-12

Altenbach, S.B., Tanaka, C.K., and Allen, P.V., Quantitative proteomic analysis of wheat grain proteins reveals differential effects of silencing of omega-5 gliadin genes in transgenic lines, J. Cereal Sci., 2014à, vol. 59, pp. 118–125. https://doi.org/10.1016/j.jcs.2013.11.008

Altenbach, S.B., Tanaka, C.K., and Seabourn, B.W., Silencing of omega-5 gliadins in transgenic wheat eliminates a major source of environmental variability and improves dough mixing properties of flour BMC, Plant Biol., 2014b, vol. 14, p. 393. https://doi.org/10.1186/s12870-014-0393-1

Ansari, A., Wang, C., Wang, J., et al., Engineered dwarf male-sterile rice: a promising genetic tool for facilitating recurrent selection in rice, Front. Plant Sci., 2017, vol. 8, pp. 21–32. https://doi.org/10.3389/fpls.2017.02132

Bai, X., Huang, X., Tian, S., et al., RNAi-mediated stable silencing of TaCSN5 confers broad-spectrum resistance to Puccinia striiformis f. sp tritici, Mol. Plant Pathol., 2021, vol. 22, pp. 410–421. https://doi.org/10.1111/mpp.13034

Barro, F., Iehisa, J.C., Giménez, M.J., et al., Targeting of prolamins by RNAi in bread wheat: effectiveness of seven silencing-fragment combinations for obtaining lines devoid of coeliac disease epitopes from highly immunogenic gliadins, Plant Biotechnol. J., 2016, vol. 14, pp. 986–996. https://doi.org/10.1111/pbi.12455

Baulcombe, D., How Virus resistance provided a mechanistic foundation for RNA silencing, Plant Cell, 2019, vol. 31, pp. 1395–1396. https://doi.org/10.1105/tpc.19.00348

Baum, J.A. and Roberts, J.K., Progress towards RNAi-mediated insect pest management, Adv. Insect Physiol., 2014, vol. 47, pp. 250–295. https://doi.org/10.1016/B978-0-12-800197-4.00005-1

Baum, J.A., Bogaert, T., Clinton, W., et al., Control of coleopteran insect pests through RNA interference, Nat. Biotechnol., 2007, vol. 25, no. 11, pp. 1322–1326. https://doi.org/10.1038/nbt1359

Bharathi, J., Anandan, R., Benjamin, L., Muneer, S., and Prakash, M., Recent trends and advances of RNA interference (RNAi) to improve agricultural crops and enhance their resilience to biotic and abiotic stresses, Plant Physiol. Biochem., 2023, vol. 194, pp. 600–618. https://doi.org/10.1016/j.plaphy.2022.11.035

Bilir, Ö., Göl, D., Hong, Y., et al., Small RNA-based plant protection against diseases, Front. Plant Sci., 2022, vol. 13, p. 951097. https://doi.org/10.3389/fpls.2022.951097

Blyuss, K.B., Fatehi, F., Tsygankova, V.A., et al., RNAi-based biocontrol of wheat nematodes using natural poly-component biostimulants, Front. Plant Sci., 2019, vol. 10, p. 483. https://doi.org/10.3389/fpls.2019.00483

Bolognesi, R., Ramaseshadri, P., Anderson, J., et al., Characterizing the mechanism of action of doublestranded RNA activity against western corn rootworm (Diabrotica virgifera virgifera LeConte), PLoS One, 2012, vol. 7, p. e47534. https://doi.org/10.1371/journal.pone.0047534

Canto-Pastor, A., Santos, B.A., Valli, A.A., et al., Enhanced resistance to bacterial and oomycete pathogens by short tandem target mimic RNAs in tomato, Proc. Natl. Acad. Sci. U. S. A., 2019, vol. 116, no. 7, pp. 2755–2760. https://doi.org/10.1073/pnas.1814380116

Chen, C.L., Liu, S.S., Liu, Q., et al., An ANNEXIN-like protein from the cereal cyst nematode Heterodera avenae suppresses plant defense, PLoS One, 2015, vol. 10, p. e0122256. https://doi.org/10.1371/journal.pone.0122256

Chen, W., Kastner, C., Nowara, D., et al., Host-induced silencing of Fusarium culmorum genes protects wheat from infection, J. Exp. Bot., 2016, vol. 67, no. 17, pp. 4979–4991. https://doi.org/10.1093/jxb/erw263

Cheng, W., Song, X.S., Li, H.P., et al., Host-induced gene silencing of an essential chitin synthase gene confers durable resistance to Fusarium head blight and seedling blight in wheat, Plant Biotechnol. J., 2015, vol. 13, no. 9, pp. 1335–1345. https://doi.org/10.1111/pbi.12352

Cruz, L.F., Rupp, J.L.S., Trick, H.N., and Fellers, J.P., Stable resistance to Wheat streak mosaic virus in wheat mediated by RNAi, In Vitro Cell. Dev. Biol. - Plant, 2014, vol. 50, no. 6, pp. 665–672. https://doi.org/10.1007/s11627-014-9634-0

Da Silva, L.S., Taylor, J., and Taylor, J.R.N., Transgenic sorghum with altered kafirin synthesis: kafirin solubility, polymerization and protein digestion, J. Agric. Food Chem., 2011, vol. 59, pp. 9265–9270. https://doi.org/10.1021/jf201878p

Dalakouras, A., Wassenegger, M., Dadami, E., et al., Genetically modified organism-free RNA interference: exogenous application of RNA molecules in plants, Plant Physiol., 2020, vol. 182, pp. 38–50. https://doi.org/10.1104/pp.19.00570

de Framond, A., Rich, P.J., McMillan, J., and Ejeta, G., Effects on Striga parastitism of transgenic maize armed with RNAi constructs targeting essential S. asitica genes, in Integrating New Technologies for Striga Control: Towards Ending the Witch-Hunt, Singapore: World Scientific Publishing Company, 2007, vols. 185–196. https://doi.org/10.1142/9789812771506_0014

Dubrovna, O.V., Stasik, O.O., Priadkina, G.O., et al., Resistance of genetically modified wheat plants, containing a double-stranded RNA suppressor of the proline dehydrogenase gene, to soil moisture deficiency, Agric. Sci. Pract., 2020, vol. 7, no. 2, pp. 24–34. https://doi.org/10.15407/agrisp7.02.024

Dubrovna, O.V., Priadkina, G.O., Mykhalska, S.I., and Komisarenko, A.G., Drought-tolerance of transgenic winter wheat with partial suppression of the proline dehydrogenase gene, Regulat. Mech. Biosyst., 2022, vol. 13, no. 4, pp. 385–392. https://doi.org/10.15421/022251

Dutta, T.K., Banakar, P., and Rao, U., The status of RNAi-based transgenic research in plant nematology, Front. Microbiol., 2015, vol. 5, pp. 760. https://doi.org/10.3389/fmicb.2014.00760

Dutta, T.K., Papolu, P.R., Singh, D., et al., Expression interference of a number of Heterodera avenae conserved genes perturbs nematode parasitic success in Triticum aestivum, Plant Sci., 2020, vol. 301, p. 110670. https://doi.org/10.1016/j.plantsci.2020.110670

El’konin, L.A., Domanina, I.V., and Ital’yanskaya, Yu.V., Genetic engineering as a tool for modification of seed storage proteins and improvement of nutritional value of cereal grain, Agric. Biol., 2016, vol. 51, no. 1, pp. 17–30. https://doi.org/10.15389/agrobiology.2016.1.17eng

Fahim, M., Ayala-Navarrete, L., Millar, A.A., and Larkin, P.J., Hairpin RNA derived from viral NIa gene confers immunity to wheat streak mosaic virus in fection in transgenic wheat plants, Plant Biotechnol. J., 2010, vol. 8, pp. 821–834. https://doi.org/10.1111/j.1467-7652.2010.00513.x

Feldmann, K.A., Steroid regulation improves crop yield, Nat. Biotechnol., 2006, vol. 24, pp. 46–47. https://doi.org/10.1038/nbt0106-46

Feng, Z., Yuan, M., Zou, J., et al., Development of marker-free rice with stable and high resistance to rice black-streaked dwarf virus disease through RNA interference, Plant Biotechnol. J., 2021, vol. 19, pp. 212–214. https://doi.org/10.1111/pbi.13459

Fire, A.S., Xu, M.K., Montgomery, S.A., et al., Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans, Nature, 1998, vol. 391, no. 6669, pp. 806–811. https://doi.org/10.1038/35888

Fletcher, S.J., Reeves, P.T., Hoang, B.T., and Mitter, N.A., Perspective on RNAi-based biopesticides, Front. Plant Sci., 2020, vol. 11, p. 51. https://doi.org/10.3389/fpls.2020.00051

Frizzi, A., Huang, S., Gilbertson, L., et al., Modifying lysine biosynthesis and catabolism in corn with a single bifunctional expression/silencing transgene cassette, Plant Biotechnol. J., 2008, vol. 6, no. 1, pp. 13–21. https://doi.org/10.1111/j.1467-7652.2007.00290.x

Gantasala, N.P., Kumar, M., Banakar, P., Thakur, P.K., and Rao, U., Functional validation of genes in cereal cyst nematode, Heterodera avenae, using siRNA gene silencing, in Nematodes of Small Grain Cereals: Current Status and Research, Dababat, A., Muminjanov, H., and Smiley, R.W., Eds., Ankara: FAO, 2015, pp. 353–356.

Gasparis, S., Orczyk, W., Zalewski, W., and Nadolska-Orczyk, A., The RNA-mediated silencing of one of the Pin genes in allohexaploid wheat simultaneously decreases the expression of the other, and increases grain hardness, J. Exp. Bot., 2011, vol. 62, pp. 4025–4036. https://doi.org/10.1093/jxb/err103

Gasparis, S., Orczyk, W., and Nadolska-Orczyk, A., Sina and Sinb genes in triticale do not determine grain hardness contrary to their orthologs Pina and Pinb in wheat, BMC Plant Biol., 2013, vol. 13, p. 190. https://doi.org/10.1186/1471-2229-13-190

Ghag, S.B., Host induced gene silencing, an emerging science to engineer crop resistance against harmful plant pathogens, Physiol. Mol. Plant Pathol., vol. 100, pp. 242–254.

Gil-Humanes, J., Piston, F., Hernando, A., et al., Silencing of γ-gliadins by RNA interference (RNAi) in bread wheat, J. Cereal Sci., 2008, vol. 48, pp. 565–568. https://doi.org/10.1016/j.jcs.2008.03.005

Gil-Humanes, J., Pistón, F., Tollefsen, S., Sollid, L.M., and Barro, F., Effective shutdown in the expression of celiac disease-related wheat gliadin T-cell epitopes by RNA interference, Proc. Natl. Acad. Sci. U. S. A., 2010, vol. 107, no. 39, pp. 17023–17028. https://doi.org/10.1073/pnas.1007773107

Gil-Humanes, J., Piston, F., Gimenez, M.J., Martın, A., and Barro, F., The introgression of RNAi silencing of γ-gliadins into commercial lines of bread wheat changes the mixing and technological properties of the dough, PLoS One, 2012, vol. 7, no. 9, p. e45937. https://doi.org/10.1371/journal.pone.0045937

Godwin, I.D., Williams, S.B., Pandit, P.S., and Laidlaw, H.K., Multifunctional grains for the future: genetic engineering for enhanced and novel cereal quality, In Vitro Cell. Dev. Biol. - Plant, 2009, vol. 45, no. 3, pp. 383–399. https://doi.org/10.1007/s11627-008-9175-5

Grootboom, A.W., Mkhonza, N.L., Mbambo, Z., et al., Co-suppression of synthesis of major α-kafirin subclass together with γ-kafirin-1 and γ-kafirin-2 required for substantially improved protein digestibility in transgenic sorghum, Plant Cell Rep., 2014, vol. 33, pp. 521–537. https://doi.org/10.1007/s00299-013-1556-5

Guo, J., Gao, S., Lin, Q., Wang, H., et al., Transgenic sugarcane resistant to Sorghum mosaic virus based on coat protein gene silencing by RNA interference, BioMed Res. Int., vol. 2015, p. 861907. https://doi.org/10.1155/2015/861907

Hada, A., Kumari, C., Phani, V., et al., Host-induced silencing of FMRFamide-like peptide genes, flp-1 and flp-12, in rice impairs reproductive fitness of the root-knot nematode Meloidogyne graminicola, Front. Plant Sci., 2020, vol. 11, p. 894. https://doi.org/10.3389/fpls.2020.00894

Halder, K., Chaudhuri, A., Abdin, M.Z., and Datta, A., Tweaking the small non-coding RNAs to improve desirable traits in plant, Int. J. Mol. Sci., 2023, vol. 24, p. 3143. https://doi.org/10.3390/ijms24043143

Hamilton, A.J. and Baulcombe, D.C., A species of small antisense RNA in posttranscriptional gene silencing in plants, Science, 1999, vol. 286, no. 5441, pp. 950–952 https://doi.org/10.1126/science.286.5441.950

He, F., Zhang, R., Zhao, J., et al., Host induced silencing of Fusarium graminearum genes enhances the resistance of Brachypodium distachyon to Fusarium head blight, Front. Plant Sci., 2019, vol. 10, p. 1362. https://doi.org/10.3389/fpls.2019.01362

Hernández-Soto, A. and Chacón-Cerdas, R., RNAi crop protection advances, Int. J. Mol. Sci., 2021, vol. 22, no. 22, p. 12148. https://doi.org/10.3390/ijms222212148

Houmard, N.M., Mainville, J.L., Bonin, C.P., et al., High-lysine corn generated by endosperm-specific suppression of lysine catabolism using RNAi, Plant Biotechnol. J., 2007, vol. 5, pp. 605–614. https://doi.org/10.1111/j.1467-7652.2007.00265.x

Hu, X., Richtman, N.M., Zhao, J.Z., et al., Discovery of midgut genes for the RNA interference control of corn rootworm, Sci Rep., 2016, vol. 6, p. 30542. https://doi.org/10.1038/srep30542

Hu, Y., Wu, Q., Peng, Z., et al., Silencing of OsGRXS17 in rice improves drought stress tolerance by modulating ROS accumulation and stomatal closure, Sci. Rep., 2017, vol. 7, p. 15950. https://doi.org/10.1038/s41598-017-16230-7

Huang, S., Kruger, D.E., Frizzi, A., et al., High-lysine corn produced by the combination of enhanced lysine biosynthesis and reduced zein accumulation, Plant Biotechnol. J., 2005, vol. 3, pp. 555–569. https://doi.org/10.1111/j.1467-7652.2005.00146.x

Huang, S., Frizzi, A., Florida, C.A., et al., High lysine and high tryptophan transgenic maize resulting from the reduction of both 19- and 22-kD a-zeins, Plant Mol. Biol., 2006, vol. 61, pp. 525–535. https://doi.org/10.1007/s11103-006-0027-6

Jiang, C.J., Shimono, M., Maeda, S., et al., Suppression of the rice fatty-acid desaturase gene OsSSI2 enhances resistance to blast and leaf blight diseases in rice, Mol. Plant-Microbe Interact., 2009, vol. 22, no. 7, pp. 820–829. https://doi.org/10.1094/MPMI-22-7-0820

Joga, M.R., Zotti, M.J., Smaghe, G., et al., RNAi efficiency, systemic properties, and novel delivery methods for pest insect control: what we know so far, Front. Physiol., 2016, vol. 7, p. 553. https://doi.org/10.3389/fphys.2016.00553

Johnson, E.T., Proctor, R.H., Dunlap, C.A., and Busman, M., Reducing production of fumonisin mycotoxins in Fusarium verticillioides by RNA interference, Mycotoxin Res., 2018, vol. 34, p. 29. https://doi.org/10.1007/s12550-017-0296-8

Kamthan, A., Chaudhuri, A., Kamthan, M., and Datta, A., Small RNAs in plants: recent development and application for crop improvement, Front. Plant Sci., 2015, vol. 6, p. 208. https://doi.org/10.3389/fpls.2015.00208

Katoch, R. and Thakur, N., Advances in RNA interference technology and its impact on nutritional improvement, disease and insect control in plants, Appl. Biochem. Biotechnol., 2013, vol. 169, no. 5, pp. 1579–1605. https://doi.org/10.1007/s12010-012-0046-5

Kaur, R., Choudhury, A., Chauhan, S., et al., RNA interference and crop protection against biotic stresses, Physiol. Mol. Biol. Plants, 2021, vol. 27, no. 10, pp. 2357–2377. https://doi.org/10.1007/s12298-021-01064-5

Kawakatsu, T., Hirose, S., Yasuda, H., and Takaiwa, F., Reducing rice seed storage protein accumulation leads to changes in nutrient quality and storage organelle formation, Plant Physiol., 2010, vol. 154, pp. 1842–1854. https://doi.org/10.1104/pp.110.164343

Kim, H.-J., Lee, J.-Y., Yoon, U.-H., Lim, S.H., and Kim, Y.-M., Effects of reduced prolamin on seed storage protein composition and the nutritional quality of rice, Int. J. Mol. Sci., 2013, vol. 14, pp. 17073–17084. https://doi.org/10.3390/ijms140817073

Koch, A. and Kogel, K.H., New wind in the sails: improving the agronomic value of crop plants through RNAi-mediated gene silencing, Plant Biotechnol. J., 2014, vol. 12, pp. 821–831. https://doi.org/10.1111/pbi.12226

Koch, A., Kumar, N., Weber, L., et al., Host-induced gene silencing of cytochrome P450 lanosterol C14a-demethylase-encoding genes confers strong resistance to Fusarium species, Proc. Natl. Acad. Sci. U. S. A., 2013, vol. 110, no. 48, pp. 19324–19329. https://doi.org/10.1073/pnas.1306373110

Kong, X., Yang, M., Le, B.H., et al., The master role of SiRNAs in plant immunity, Mol. Plant Pathol., 2022, vol. 23, no. 10, pp. 1565–1574. https://doi.org/10.1111/mpp.13250

Kumar, K., Geetika, C., Dass, A., et al., Genetically modified crops: current status and future prospects, Planta, 2020, vol. 251, no. 4, p. 91. https://doi.org/10.1007/s00425-020-03372-8

Kumar, T., Dweikat, I., Sato, S., et al., Modulation of kernel storage proteins in grain sorghum (Sorghum bicolor (L.) Moench), Plant Biotechnol. J., 2012, vol. 10, pp. 533–544. https://doi.org/10.1111/j.1467-7652.2012.00685.x

Kusaba, M., Miyahara, K., Iida, S., et al., Low glutenin content1: a dominant mutation that suppresses the glutenin multigene family via RNA silencing in rice, Plant Cell, 2003, vol. 15, pp. 1455–1467. https://doi.org/10.1105/tpc.011452

Kuwano, M., Ohyama, A., Tanaka, Y., et al., Molecular breeding for transgenic rice with low-phytic-acid phenotype through manipulating myo-inositol 3-phosphate synthase gene, Mol. Breed., 2006, vol. 18, no. 3, pp. 263–272. https://doi.org/10.1007/s11032-006-9038-x

Lacombe, S., Bangratz, M., Ta, H., et al., Optimized RNA-silencing strategies for Rice ragged stunt virus resistance in rice, Plants (Basel), 2021, vol. 10, no. 10, p. 2008. https://doi.org/10.3390/plants10102008

Le, D., Chu, H., and Sasaya, T., Creation of transgenic rice plants producing small interfering RNA of Rice tungro spherical virus, GM Crops Food, 2015, vol. 6, no. 1, pp. 47–53. https://doi.org/10.1080/21645698.2015.1025188

Li, Z., Liu, Y., and Berger, P.H., Transgenic silencing in wheat transformed with the WSMV-CP gene, Biotechnology, 2005, vol. 4, pp. 62–68. https://doi.org/10.3923/biotech.2005.62.68

Li, D.H., Liu, H., Yang, Y.L., Zhen, P.P., and Liang, J.S., Down-regulated expression of RACK1 gene by RNA interference enhances drought tolerance in rice, Rice Sci., 2009, vol. 16, pp. 14–20. https://doi.org/10.1016/S1672-6308(08)60051-7

Li, J.L., Chen, X.X., Shi, C.C., et al., Effects of OsRPK1 gene overexpression and RNAi on the salt-tolerance at seedling stage in rice, Acta Agron. Sin., 2020, vol. 46, pp. 1217–1224. https://doi.org/10.3724/SP.J.1006.2020.92060

Lilley, C.J., Bakhetia, M., Charlton, W.L., and Urwin, P.E., Recent progress in the development of RNA interference for plant parasitic nematodes, Mol. Plant Pathol., 2007, vol. 8, pp. 701–711. https://doi.org/10.1111/j.1364-3703.2007.00422.x

Liu, F., Yang, B., Zhang, A., Ding, D., and Wang, G., Plant-mediated RNAi for controlling Apolygus lucorum, Front. Plant Sci., 2019, vol. 10, p. 64. https://doi.org/10.3389/fpls.2019.00064

Liu, S., Geng, S., Li, A., Mao, Y., and Mao, L., RNAi technology for plant protection and its application in wheat, aBIOTECH, 2021, vol. 2, pp. 365–374. https://doi.org/10.1007/s42994-021-00036-3

Long, X., Liu, Q., Chan, M., et al., Metabolic engineering and profiling of rice with increased lysine, Plant Biotechnol. J., 2012, vol. 11, no. 4, pp. 490–501. https://doi.org/10.1111/pbi.12037

Ma, J., Song, Y., Wu, B., et al., Production of transgenic rice new germplasm with strong resistance against two isolations of Rice stripe virus by RNA interference, Transgenic Res., 2011, vol. 20, pp. 1367–1377. https://doi.org/10.1007/s11248-011-9502-1

Machado, A.K., Brown, N.A., Urban, M., et al., RNAi as an emerging approach to control Fusarium head blight disease and mycotoxin contamination in cereals, Pest Manage. Sci., 2018, vol. 74, pp. 790–799. https://doi.org/10.1002/ps.4748

Masanga, J.O., Matheka, J.M., and Omer, R.A., Downregulation of transcription factor aflR in Aspergillus flavus confers reduction to aflatoxin accumulation in transgenic maize with alteration of host plant architecture, Plant Cell Rep., 2015, vol. 34, pp. 1379–1387. https://doi.org/10.1007/s00299-015-1794-9

Mezzetti, B., Smagghe, G., Arpaia, S., et al., RNAi: What is its position in agriculture?, J. Pest Sci., 2020, vol. 93, no. 4, pp. 1125–1130. https://doi.org/10.1007/s10340-020-01238-2

Mykhalska, S.I., Sergeeva, L.E., Matveeva, A.Yu., et al., The elevation of free proline content in osmotolerant transgenic corn plants with dsRNA suppressor of proline dehydrogenase gene, Plant Physiol. Genet., 2014, vol. 46, no. 6, pp. 482–489 http:// dspace.nbuv.gov.ua/handle/123456789/159462

Nowara, D., Gay, A., Lacomme, C., et al., HIGS: host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis, Plant Cell, 2010, vol. 22, pp. 3130–3141. https://doi.org/10.1105/tpc.110.077040

Panwar, V., McCallum, B., and Bakkeren, G., Endogenous silencing of Puccinia triticina pathogenicity genes through in planta-expressed sequences leads to the suppression of rust diseases on wheat, Plant J., 2013, vol. 73, no. 3, pp. 521–532. https://doi.org/10.1111/tpj.12047

Panwar, V., McCallum, B., and Bakkeren, G., Host-induced gene silencing of wheat leaf rust fungus Puccinia triticina pathogenicity genes mediated by the Barley stripe mosaic virus, Plant Mol. Biol., 2013, vol. 81, pp. 595–608. https://doi.org/10.1007/s11103-013-0022-7

Panwar, V., Jordan, M., McCallum, B., and Bakkeren, G., Host-induced silencing of essential genes in Puccinia triticina through transgenic expression of RNAi sequences reduces severity of leaf rust infection in wheat, Plant Biotechnol. J., 2018, vol. 16, pp. 1013–1023. https://doi.org/10.1111/pbi.12845

Pistón, F., Gil-Humanes, J., Rodríguez-Quijano, M., and Barro, F., Down-regulating γ-gliadins in bread wheat leads to non-specific increases in other gluten proteins and has no major effect on dough gluten strength, PLoS One, 2011, vol. 6, p. e24754. https://doi.org/10.1371/journal.pone.0024754

Qi, T., Zhu, X., Tan, C., et al., Host-induced gene silencing of an important pathogenicity factor PsCPK1 in Puccinia striiformis f. sp. tritici enhances resistance of wheat to stripe rust, Plant Biotechnol. J., 2018, vol. 16, pp. 797–807. https://doi.org/10.1111/pbi.12829

Qi, T., Guo, J., Liu, P., et al., Stripe rust effector PstGSRE1 disrupts nuclear localization of ROS-promoting transcription factor TaLOL2 to defeat ROS-induced defense in wheat, Mol. Plant, 2019a, vol. 12, pp. 1624–1638. https://doi.org/10.1016/j.molp.2019.09.010

Qi, T., Guo, J., Peng, H., et al., Host-induced gene silencing: a powerful strategy to control diseases of wheat and barley, Int. J Mol. Sci., 2019b, vol. 20, p. 206. https://doi.org/10.3390/ijms20010206

Qiao, F., Yang, Q., Wang, C.L., et al., Modification of plant height via RNAi suppression of OsGA20ox2 gene in rice, Euphytica, 2007, vol. 158, pp. 35–45. https://doi.org/10.1007/s10681-007-9422-6

Rajam, M.V., RNA silencing technology: A boon for crop improvement, J. Biosci., 2020, vol. 45, p. 118.

Raruang, Y., Omolehin, O., Hu, D., et al., Host induced gene silencing targeting Aspergillus flavus aflM reduced aflatoxin contamination in transgenic maize under field conditions, Front. Microbiol., 2020, vol. 11, p. 754. https://doi.org/10.3389/fmicb.2020.00754

Regina, A., Bird, A., Topping, D., et al., High-amylose wheat generated by RNA interference improves indices of large-bowel health in rats, Proc. Natl. Acad. Sci. U. S. A., 2006, vol. 103, no. 10, pp. 3546–3551. https://doi.org/10.1073/pnas.0510737103

Riechen, J., Establishment of broad-spectrum resistance against Blumeria graminis f.sp. tritici in Triticum aestivum by RNAi-mediated knock-down of MLO, J. Verbraucherschutz Lebensmittelsicherh., 2007, vol. 2, p. 120. https://doi.org/10.1007/s00003-007-0282-8

Rodrigues, T.B. and Petrick, J.S., Safety considerations for humans and other vertebrates regarding agricultural uses of externally applied RNA molecules, Front. Plant Sci., 2020, vol. 11, p. 407. https://doi.org/10.3389/fpls.2020.00407

Sang, H. and Kim, J., Advanced strategies to control plant pathogenic fungi by host-induced gene silencing (HIGS) and spray-induced gene silencing (SIGS), Plant Biotechnol. Rep., 2020, vol. 14, pp. 1–8. https://doi.org/10.1007/s11816-019-00588-3

Sasaya, T., Nakazono-Nagaoka, E., Saika, H., et al., Transgenic strategies to confer resistance against viruses in rice plants, Front. Microbiol., 2014, vol. 4, p. 409. https://doi.org/10.3389/fmicb.2013.00409

Schaefer, K.L., Parlange, F., Buchmann, G., et al., Cross-kingdom RNAi of pathogen effectors leads to quantitative adult plant resistance in wheat, Front. Plant Sci., 2020, vol. 11, p. 253. https://doi.org/10.3389/fpls.2020.00253

Segal, G., Song, R., and Messing, J., A new opaque variant of maize by a single dominant RNA-interference-inducing transgene, Genetics, 2003, vol. 165, pp. 387–397. http://www.genetics.org/content/165/1/ 387.full.pdf.

Sharma, S., Kumar, G., and Dasgupta, I., Simultaneous resistance against the two viruses causing rice tungro disease using RNA interference, Virus Res., 2018, vol. 255, pp. 157–164. https://doi.org/10.1016/j.virusres.2018.07.011

Shepherd, D.N., Mangwende, T., Martin, D.P., et al., Inhibition of maize streak virus (MSV) replication by transient and transgenic expression of MSV replication-associated protein mutants, J. Gen. Virol., 2007, vol. 88, pp. 325–336. https://doi.org/10.1099/vir.0.82338-0

Shimizu, T., Yoshii, M., Wei, T., et al., Silencing by RNAi of the gene for Pns12, a viroplasm matrix protein of Rice dwarf virus, results in strong resistance of transgenic rice plants to the virus, Plant Biotechnol. J., 2009, vol. 7, no. 1, pp. 24–32. https://doi.org/10.1111/j.1467-7652.2008.00366.x

Shimizu, T., Nakazono-Nagaoka, E., Uehara-Ichiki, T., et al., Targeting specific genes for RNA interference is crucial to the development of strong resistance to Rice stripe virus, Plant Biotechnol. J., 2011, vol. 9, no. 4, pp. 503–512. https://doi.org/10.1111/j.1467-7652.2010.00571.x

Shimizu, T., Nakazono-Nagaoka, E., Akita, F., et al., Hairpin RNA derived from the gene for Pns9, a viroplasm matrix protein of Rice gall dwarf virus, confers strong resistance to virus infection in transgenic rice plants, J. Biotechnol., 2012, vol. 157, no. 3, pp. 421–427. https://doi.org/10.1016/j.jbiotec.2011.12.015

Shimizu, T., Ogamino, T., Hiraguri, A., et al., Strong resistance against Rice grassy stunt virus is induced in transgenic rice plants expressing double-stranded RNA of the viral genes for nucleocapsid or movement proteins as targets for RNA interference, Phytopathology, 2013, vol. 103, no. 5, pp. 513–519. https://doi.org/10.1094/PHYTO-07-12-0165-R

Shoup Rupp, J.L., Cruz, L.F., Trick, H.N., and Fellers, J.P., RNAi-mediated, stable resistance to Triticum mosaic virus in wheat, Crop Sci., 2016, vol. 56, pp. 1602–1610. https://doi.org/10.2135/cropsci2015.09.0577

Singh, K., Dardick, Ch., and Kindu, J.K., RNAi-mediated resistance against viruses in perinnial fruit plants, Plants, 2019, vol. 8, p. 359. https://doi.org/103390/plants8100359

Sivamani, E., Brey, C., Dyer, W.E., et al., Resistance to wheat streak mosaic virus in transgenic wheat expressing the viral replicase (NIb) gene, Mol. Breed., 2000, vol. 6, pp. 469–477. https://doi.org/10.1023/A:1026576124482

Sivamani, E., Brey, C.W., Talbert, L.E., et al., Resistance to wheat streak mosaic virus in transgenic wheat engineered with the viral coat protein gene, Transgenic Res., 2002, vol. 11, no. 1, pp. 31–41. https://doi.org/10.1023/a:1013944011049

Sun, Y., Sparks, C., Jones, H., et al., Silencing an essential gene involved in infestation and digestion in grain aphid through plant-mediated RNA interference generates aphid-resistant wheat plants, Plant Biotechnol. J., 2019, vol. 17, pp. 852–854. https://doi.org/10.1111/pbi.13067

Thakare, D., Zhang, J., Wing, R., Cotty, P., Schmidt, M., Aflatoxin-free transgenic maize using hostinduced gene silencing, Sci. Adv., 2017, vol. 3, p. e1602382. https://doi.org/10.1126/sciadv.1602382

Tiwari, I.M., Jesuraj, A., Kamboj, R., et al., Host delivered RNAi, an efficient approach to increase rice resistance to sheath blight pathogen (Rhizoctonia solani), Sci. Rep., 2017, vol. 7, p. 7521. https://doi.org/10.1038/s41598-017-07749-w

Tsygankova, V.A., Blyuss, K.B., Shysha, E.N., et al., Using microbial biostimulants to deliver RNA interference in plants as an effective tool for biocontrol of pathogenic fungi, parasitic nematodes and insects, in Research Advances in Plant Biotechnology, Plant Science Research and Practices, Blume, Ya.B., Ed., Nova Sci., 2020, Chapter 6, pp. 205–319.

Tyagi, H., Rajasubramaniam, R.M.V., and Dasgupta, I., RNA-interference in rice against Rice tungro bacilliform virus results in its decreased accumulation in inoculated rice plants, Transgen. Res., 2008, vol. 17, no. 5, pp. 897–904. https://doi.org/10.1007/s11248-008-9174-7

Várallyay, É., Giczey, G., and Burgyán, J., Virus-induced gene silencing of Mlo genes induces powdery mildew resistance in Triticum aestivum, Arch. Virol., 2012, vol. 157, pp. 1345–1350. https://doi.org/10.1007/s00705-012-1286-y

Verma, V., Sharma, S., Devi, S.V., Rajasubramaniam, S., and Dasgupta, I., Delay in virus accumulation and low virus transmission from transgenic rice plants expressing Rice tungro spherical virus RNA, Virus Genes, 2012, vol. 45, pp. 350–359. https://doi.org/10.1007/s11262-012-0787-9

Wang, M.B., Abbott, D.C., and Waterhouse, P.M., A single copy of a virus-derived transgene encoding hairpin RNA gives immunity to barley yellow dwarf virus, Mol. Plant Pathol., 2000, vol. 1, no. 6, pp. 347–356. https://doi.org/10.1046/j.1364-3703.2000.2000.00038.x

Wang, Y., Cheng, X., Shan, Q., et al., Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew, Nat. Biotechnol., 2014, vol. 32, pp. 947–951. https://doi.org/10.1038/nbt.2969

Wang, F., Li, W., Zhu, J., et al., Hairpin RNA targeting multiple viral genes confers strong resistance to rice black-streaked dwarf virus, Int. J. Mol. Sci., 2016, vol. 17, no. 5, p. 705. https://doi.org/10.3390/ijms17050705

Wang, M., Wu, L., Mei, Y., et al., Host-induced gene silencing of multiple genes of Fusarium graminearum enhances resistance to Fusarium head blight in wheat, Plant Biotechnol. J., 2020, vol. 18, no. 12, pp. 2373–2375. https://doi.org/10.1111/pbi.13401

Weise, S.E., Aung, K., Jarou, Z.J., et al., Engineering starch accumulation by manipulation of phosphate metabolism of starch, Plant Biotechnol. J., 2012, vol. 10, pp. 545–554. https://doi.org/10.1111/j.1467-7652.2012.00684.x

Wen, S., Wen, N., Pang, J., et al., Structural genes of wheat and barley 5-methylcytosine DNA glycosylases and their potential applications for human health, Proc. Natl. Acad. Sci. U. S. A., 2012, vol. 109, pp. 20543–20548. https://doi.org/10.1073/pnas.1217927109

Wieser, H., Koehler, P., Folck, A., and Becker, D., Characterization of wheat with strongly reduced α-gliadin content, in Gluten Proteins, Lookhart, G.L. and Ng, P.K.W., Eds., St. Paul: AACC Int., 2006, vol. 2006, pp. 13–16

Xu, L., Duan, X., Lv, Y., et al., Silencing of an aphid carboxylesterase gene by use of plant-mediated RNAi impairs Sitobion avenae tolerance of Phoxim insecticides, Transgen. Res., 2014, vol. 23, no. 2, pp. 389–396. https://doi.org/10.1007/s11248-013-9765-9

Xu, L., Hou, Q., Zhao, Y., et al., Silencing of alipase maturation factor 2-like gene by wheat-mediated RNAi reduces the survivability and reproductive capacity of the grain aphid Sitobion avenae, Arch. Insect Biochem. Physiol., 2017, vol. 95, no. 3, p. e21392. https://doi.org/10.1002/arch.21392

Yang, B., Sugio, A., and White, F.F., Os8N3 is a host disease susceptibility gene for bacterial blight of rice, Proc. Natl. Acad. Sci. U. S. A., 2006, vol. 103, pp. 10503–10508. https://doi.org/10.1073/pnas.0604088103

Yara, A., Yaeno, T., Hasegawa, M., et al., Disease resistance against Magnaporthe grisea is enhanced in transgenic rice with suppression of ω-3 fatty acid desaturases, Plant Cell Physiol., 2007, vol. 48, pp. 1263–1274. https://doi.org/10.1093/pcp/pcm107

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

Yu, R., Xu, X., Liang, Y., et al., The insect ecdysone receptor is a good potential target for RNAi based pest control, Int. J. Biol. Sci., 2014, vol. 10, no. 10, pp. 1171–1180. https://doi.org/10.7150/ijbs.9598

Yu, H., Wang, Y., Fu, F., and Li, W., Transgenic improvement for biotic resistance of crops, Int. J. Mol. Sci., 2022, vol. 23, p. 14370. https://doi.org/10.3390/ijms232214370

Zha, W., Peng, X., Chen, R., et al., Knockdown of midgut genes by dsRNA-transgenic plant-mediated RNA interference in the hemipter an insect Nilaparvata lugens, PLoS One, 2011, vol. 6, p. e20504. https://doi.org/10.1371/journal.p

Zhang, Z.Y., Fu, F.L., Gou, L., et al., RNA interference-based transgenic maize resistant to maize dwarf mosaic virus, J. Plant Biol., 2010, vol. 53, pp. 297–305. https://doi.org/10.1016/j.jbiotec.2011.03.019

Zhang, Z.Y., Yang, L., Zhou, S.F., et al., Improvement of resistance to maize dwarf mosaic virus mediated by transgenic RNA interference, J. Biotechnol., 2011, vol. 153, pp. 181–187. https://doi.org/10.1016/j.jbiotec.2011.03.019

Zhang, Z.Y., Wang, Y.G., Shen, X.J., et al., RNA interference-mediated resistance to maize dwarf mosaic virus, Plant Cell Tissue Organ Cult., 2013, vol. 113, pp. 571–578. https://doi.org/10.1007/s11240-013-0289-z

Zhang, J., Khan, S.A., Heckel, D.G., and Bock, R., Next-generation insect-resistant plants: RNAi-mediated crop protection, Trends Biotechnol., 2017, vol. 35, pp. 871–882. https://doi.org/10.1016/j.tibtech.2017.04.009

Zhao, Y., et al., Plant-mediated RNAi of grain aphid CHS1 gene confers common wheat resistance against aphids, Pest Manage. Sci., 2018, vol. 74, pp. 2754–2760. https://doi.org/10.1002/ps.5062

Zhou, Y., Yuan, Y., Yuan, F., et al., RNAi-directed down-regulation of RSV results in increased resistance in rice (Oryza sativa L.), Biotechnol. Lett., 2012, vol. 34, pp. 965–972. https://doi.org/10.1007/s10529-012-0848-0

Zhou, B., Bailey, A., Niblett, C.L., and Qu, R., Control of brown patch (Rhizoctonia solani) in tall fescue (Festuca arundinacea Schreb.) by host induced gene silencing, Plant Cell Rep., 2016, vol. 35, pp. 791–802. https://doi.org/10.1007/s00299-015-1921-7

Zhu, L., Zhu, J., Liu, Z., et al., Host-induced gene silencing of rice blast fungus Magnaporthe oryzae pathogenicity genes mediated by the brome mosaic virus, Genes, 2017, vol. 8, p. 241. https://doi.org/10.3390/genes8100241

Zhu, X., Qi, T., Yang, Q., et al., Host-induced gene silencing of the MAPKK gene PsFUZ7 confers stable resistance to wheat stripe rust, Plant Physiol., 2017, vol. 175, pp. 1853–1863. https://doi.org/10.1104/pp.17.01223