Exploring the challenges of RNAi-based strategies for crop protection

Jian-Hua Zhao, Qing-Yan Liu, Zong-Ming Xie, Hui-Shan Guo

Advanced Biotechnology ›› 2024, Vol. 2 ›› Issue (3) : 0. DOI: 10.1007/s44307-024-00031-x

Exploring the challenges of RNAi-based strategies for crop protection

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Abstract

RNA silencing (or RNA interference, RNAi) initiated by double-stranded RNAs is a conserved mechanism for regulating gene expression in eukaryotes. RNAi-based crop protection strategies, including host-induced gene silencing (HIGS), spray-induced gene silencing (SIGS) and microbe-induced gene silencing (MIGS), have been successfully used against various pests and pathogens. Here, we highlight the challenges surrounding dsRNA design, large-scale production of dsRNA and dsRNA delivery systems. Addressing these questions will accelerate the lab-to-field transition of RNAi-based strategies. Moreover, based on studies of exogenous dsRNA-induced RNAi inheritance in Caenorhabditis elegans, we speculate that RNAi-based strategies would confer longer-lasting protection for crops against pests or fungal pathogens.

Keywords

RNAi / HIGS / SIGS / MIGS / RNAi inheritance

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Jian-Hua Zhao, Qing-Yan Liu, Zong-Ming Xie, Hui-Shan Guo. Exploring the challenges of RNAi-based strategies for crop protection. Advanced Biotechnology, 2024, 2(3): 0 https://doi.org/10.1007/s44307-024-00031-x

References

[]
Alcazar RM, Lin R, Fire AZ. Transmission dynamics of heritable silencing induced by double-stranded RNA in Caenorhabditis elegans. Genetics, 2008, 180: 1275-1288, pmcid: 2581934
CrossRef Pubmed Google scholar
[]
Bachman P, Fischer J, Song Z, Urbanczyk-Wochniak E, Watson G. Environmental Fate and Dissipation of Applied dsRNA in Soil, Aquatic Systems, and Plants. Front Plant Sci, 2020, 11: 21, pmcid: 7016216
CrossRef Pubmed Google scholar
[]
Beachy RN, Loeschfries S, Tumer NE. Coat Protein-Mediated Resistance against Virus-Infection. Annu Rev Phytopathol, 1990, 28: 451-474,
CrossRef Google scholar
[]
Burton NO, Burkhart KB, Kennedy S. Nuclear RNAi maintains heritable gene silencing in Caenorhabditis elegans. Proc Natl Acad Sci USA, 2011, 108: 19683-19688, pmcid: 3241819
CrossRef Pubmed Google scholar
[]
Chan CY, Carmack CS, Long DD, Maliyekkel A, Shao Y, Roninson IB, Ding Y. A structural interpretation of the effect of GC-content on efficiency of RNA interference. BMC Bioinformatics, 2009, 10(Suppl 1): S33, pmcid: 2648742
CrossRef Pubmed Google scholar
[]
Chen K, Wang Y, Zhang R, Zhang H, Gao C. CRISPR/Cas Genome Editing and Precision Plant Breeding in Agriculture. Annu Rev Plant Biol, 2019, 70: 667-697,
CrossRef Pubmed Google scholar
[]
Cheon SH, Kim ZH, Choi HY, Kang SH, Nam HJ, Kim JY, Kim DI. Effective delivery of siRNA to transgenic rice cells for enhanced transfection using PEI-based polyplexes. Biotechnol Bioprocess Eng, 2017, 22: 577-585,
CrossRef Google scholar
[]
Chen X, Rechavi O. Plant and animal small RNA communications between cells and organisms. Nat Rev Mol Cell Biol, 2022, 23: 185-203,
CrossRef Pubmed Google scholar
[]
Cui C, Wang Y, Li Y, Sun P, Jiang J, Zhou H, Liu J, Wang S. Expression of mosquito miRNAs in entomopathogenic fungus induces pathogen-mediated host RNA interference and increases fungal efficacy. Cell Rep, 2022, 41,
CrossRef Pubmed Google scholar
[]
Dalakouras A, Jarausch W, Buchholz G, Bassler A, Braun M, Manthey T, Krczal G, Wassenegger M. Delivery of Hairpin RNAs and Small RNAs Into Woody and Herbaceous Plants by Trunk Injection and Petiole Absorption. Front Plant Sci, 2018, 9: 1253, pmcid: 6120046
CrossRef Pubmed Google scholar
[]
De Schutter K, Taning CNT, Van Daele L, Van Damme EJM, Dubruel P, Smagghe G. RNAi-Based Biocontrol Products: Market Status, Regulatory Aspects, and Risk Assessment. Front Insect Sci, 2021, 1,
CrossRef Pubmed Google scholar
[]
Dietz-Pfeilstetter A, Mendelsohn M, Gathmann A, Klinkenbuss D. Considerations and Regulatory Approaches in the USA and in the EU for dsRNA-Based Externally Applied Pesticides for Plant Protection. Front Plant Sci, 2021, 12, pmcid: 8232971
CrossRef Pubmed Google scholar
[]
Duan CG, Wang CH, Fang RX, Guo HS. Artificial MicroRNAs highly accessible to targets confer efficient virus resistance in plants. J Virol, 2008, 82: 11084-11095, pmcid: 2573272
CrossRef Pubmed Google scholar
[]
Elston KM, Maeda GP, Perreau J, Barrick JE. Addressing the challenges of symbiont-mediated RNAi in aphids. PeerJ, 2023, 11, pmcid: 9983426
CrossRef Pubmed Google scholar
[]
Fang R. Microbe-induced gene silencing explores interspecies RNAi and opens up possibilities of crop protection. Science China Life Sciences, 2024, 67: 626-628,
CrossRef Pubmed Google scholar
[]
Frolows N, Ashe A. Small RNAs and chromatin in the multigenerational epigenetic landscape of Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci, 2021, 376: 20200112, pmcid: 8059974
CrossRef Pubmed Google scholar
[]
Gan D, Zhang J, Jiang H, Jiang T, Zhu S, Cheng B. Bacterially expressed dsRNA protects maize against SCMV infection. Plant Cell Rep, 2010, 29: 1261-1268,
CrossRef Pubmed Google scholar
[]
Gruber C, Gursinsky T, Gago-Zachert S, Pantaleo V, Behrens SE. Effective Antiviral Application of Antisense in Plants by Exploiting Accessible Sites in the Target RNA. Int J Mol Sci. 2023;24 https://doi.org/10.3390/ijms242417153
[]
Guo HS, Garcia JA. Delayed resistance to plum pox potyvirus mediated by a mutated RNA replicase gene: Involvement of a gene-silencing mechanism. Mol Plant Microbe in, 1997, 10: 160-170,
CrossRef Google scholar
[]
Guo Z, Li Y, Ding SW. Small RNA-based antimicrobial immunity. Nat Rev Immunol, 2019, 19: 31-44,
CrossRef Pubmed Google scholar
[]
Havrdova M, Hola K, Skopalik J, Tomankova K, Petr M, Cepe K, Polakova K, Tucek J, Bourlinos AB, Zboril R. Toxicity of carbon dots – Effect of surface functionalization on the cell viability, reactive oxygen species generation and cell cycle. Carbon, 2016, 99: 238-248,
CrossRef Google scholar
[]
Heale BS, Soifer HS, Bowers C, Rossi JJ. siRNA target site secondary structure predictions using local stable substructures. Nucleic Acids Res, 2005, 33, pmcid: 549425
CrossRef Pubmed Google scholar
[]
Hezakiel HE, Thampi M, Rebello S, Sheikhmoideen JM. Biopesticides: a Green Approach Towards Agricultural Pests. Appl Biochem Biotechnol, 2023,
CrossRef Pubmed Google scholar
[]
Holen T, Amarzguioui M, Wiiger MT, Babaie E, Prydz H. Positional effects of short interfering RNAs targeting the human coagulation trigger Tissue Factor. Nucleic Acids Res, 2002, 30: 1757-1766, pmcid: 113209
CrossRef Pubmed Google scholar
[]
Hou Y, Ma W. Natural Host-Induced Gene Silencing Offers New Opportunities to Engineer Disease Resistance. Trends Microbiol, 2020, 28: 109-117,
CrossRef Pubmed Google scholar
[]
Houri-Zeevi L, Rechavi O. A Matter of Time: Small RNAs Regulate the Duration of Epigenetic Inheritance. Trends in Genetics: TIG, 2017, 33: 46-57,
CrossRef Pubmed Google scholar
[]
Houri-Ze'evi L, Korem Y, Sheftel H, Faigenbloom L, Toker IA, Dagan Y, Awad L, Degani L, Alon U, Rechavi O. A Tunable Mechanism Determines the Duration of the Transgenerational Small RNA Inheritance in C. elegans. Cell., 2016, 165: 88-99,
CrossRef Pubmed Google scholar
[]
Hua C, Zhao JH, Guo HS. Trans-Kingdom RNA Silencing in Plant-Fungal Pathogen Interactions. Mol Plant, 2018, 11: 235-244,
CrossRef Pubmed Google scholar
[]
Huang C, Sede AR, Elvira-Gonzalez L, Yan Y, Rodriguez ME, Mutterer J, Boutant E, Shan L, Heinlein M. dsRNA-induced immunity targets plasmodesmata and is suppressed by viral movement proteins. Plant Cell, 2023, 35: 3845-3869, pmcid: 10533371
CrossRef Pubmed Google scholar
[]
Hudson GA, Bloomingdale RJ, Znosko BM. Thermodynamic contribution and nearest-neighbor parameters of pseudouridine-adenosine base pairs in oligoribonucleotides. RNA (new York, NY), 2013, 19: 1474-1482,
CrossRef Google scholar
[]
Hwang H, Chang HR, Baek D. Determinants of Functional MicroRNA Targeting. Mol Cells, 2023, 46: 21-32, pmcid: 9880601
CrossRef Pubmed Google scholar
[]
Islam MT, Sherif SM. RNAi-Based Biofungicides as a Promising Next-Generation Strategy for Controlling Devastating Gray Mold Diseases. Int J Mol Sci. 2020;21 https://doi.org/10.3390/ijms21062072
[]
Judge AD, Sood V, Shaw JR, Fang D, McClintock K, MacLachlan I. Sequence-dependent stimulation of the mammalian innate immune response by synthetic siRNA. Nat Biotechnol, 2005, 23: 457-462,
CrossRef Pubmed Google scholar
[]
Kamper J, Kahmann R, Bolker M, Ma LJ, Brefort T, Saville BJ, Banuett F, Kronstad JW, Gold SE, Muller O, Perlin MH, Wosten HA, de Vries R, Ruiz-Herrera J, Reynaga-Pena CG, Snetselaar K, McCann M, Perez-Martin J, Feldbrugge M, Basse CW, Steinberg G, Ibeas JI, Holloman W, Guzman P, Farman M, Stajich JE, Sentandreu R, Gonzalez-Prieto JM, Kennell JC, Molina L, Schirawski J, Mendoza-Mendoza A, Greilinger D, Munch K, Rossel N, Scherer M, Vranes M, Ladendorf O, Vincon V, Fuchs U, Sandrock B, Meng S, Ho EC, Cahill MJ, Boyce KJ, Klose J, Klosterman SJ, Deelstra HJ, Ortiz-Castellanos L, Li W, Sanchez-Alonso P, Schreier PH, Hauser-Hahn I, Vaupel M, Koopmann E, Friedrich G, Voss H, Schluter T, Margolis J, Platt D, Swimmer C, Gnirke A, Chen F, Vysotskaia V, Mannhaupt G, Guldener U, Munsterkotter M, Haase D, Oesterheld M, Mewes HW, Mauceli EW, DeCaprio D, Wade CM, Butler J, Young S, Jaffe DB, Calvo S, Nusbaum C, Galagan J, Birren BW. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature, 2006, 444: 97-101,
CrossRef Pubmed Google scholar
[]
Kanoria S, Rennie W, Liu C, Carmack CS, Lu J, Ding Y. STarMir Tools for Prediction of microRNA Binding Sites. Methods in Molecular Biology (clifton, NJ), 2016, 1490: 73-82,
CrossRef Google scholar
[]
Keon JP, Owen JW, Hargreaves JA. Lack of evidence for antisense suppression in the fungal plant pathogen Ustilago maydis. Antisense Nucleic Acid Drug Dev, 1999, 9: 101-104,
CrossRef Pubmed Google scholar
[]
Kertesz M, Wan Y, Mazor E, Rinn JL, Nutter RC, Chang HY, Segal E. Genome-wide measurement of RNA secondary structure in yeast. Nature, 2010, 467: 103-107,
CrossRef Pubmed Google scholar
[]
Kierzek E, Kierzek R. The thermodynamic stability of RNA duplexes and hairpins containing N6-alkyladenosines and 2-methylthio-N6-alkyladenosines. Nucleic Acids Res, 2003, 31: 4472-4480, pmcid: 169893
CrossRef Pubmed Google scholar
[]
Kierzek E, Mathews DH, Ciesielska A, Turner DH, Kierzek R. Nearest neighbor parameters for Watson-Crick complementary heteroduplexes formed between 2'-O-methyl RNA and RNA oligonucleotides. Nucleic Acids Res, 2006, 34: 3609-3614, pmcid: 1540717
CrossRef Pubmed Google scholar
[]
Kierzek E, Zhang X, Watson RM, Kennedy SD, Szabat M, Kierzek R, Mathews DH. Secondary structure prediction for RNA sequences including N(6)-methyladenosine. Nat Commun, 2022, 13: 1271, pmcid: 8917230
CrossRef Pubmed Google scholar
[]
Koch A, Biedenkopf D, Furch A, Weber L, Rossbach O, Abdellatef E, Linicus L, Johannsmeier J, Jelonek L, Goesmann A, Cardoza V, McMillan J, Mentzel T, Kogel KH. An RNAi-Based Control of Fusarium graminearum Infections Through Spraying of Long dsRNAs Involves a Plant Passage and Is Controlled by the Fungal Silencing Machinery. PLoS Pathog, 2016, 12, pmcid: 5063301
CrossRef Pubmed Google scholar
[]
Lai DY. Approach to using mechanism-based structure activity relationship (SAR) analysis to assess human health hazard potential of nanomaterials. Food and Chemical Toxicology : an International Journal Published for the British Industrial Biological Research Association, 2015, 85: 120-126,
CrossRef Pubmed Google scholar
[]
Laurie JD, Linning R, Bakkeren G. Hallmarks of RNA silencing are found in the smut fungus Ustilago hordei but not in its close relative Ustilago maydis. Curr Genet, 2008, 53: 49-58,
CrossRef Pubmed Google scholar
[]
Lewis CJ, Pan T, Kalsotra A. RNA modifications and structures cooperate to guide RNA-protein interactions. Nat Rev Mol Cell Biol, 2017, 18: 202-210, pmcid: 5542016
CrossRef Pubmed Google scholar
[]
Li J, Zhang BS, Wu HW, Liu CL, Guo HS, Zhao JH. The RNA-binding domain of DCL3 is required for long-distance RNAi signaling. aBIOTECH, 2024, 5: 17-28,
CrossRef Pubmed Google scholar
[]
Liu N, Dai Q, Zheng G, He C, Parisien M, Pan T. N(6)-methyladenosine-dependent RNA structural switches regulate RNA-protein interactions. Nature, 2015, 518: 560-564, pmcid: 4355918
CrossRef Pubmed Google scholar
[]
Liu S, Jaouannet M, Dempsey DA, Imani J, Coustau C, Kogel KH. RNA-based technologies for insect control in plant production. Biotechnol Adv, 2020, 39,
CrossRef Pubmed Google scholar
[]
Lomonossoff GP. Pathogen-derived resistance to plant viruses. Annu Rev Phytopathol, 1995, 33: 323-343,
CrossRef Pubmed Google scholar
[]
Luo KQ, Chang DC. The gene-silencing efficiency of siRNA is strongly dependent on the local structure of mRNA at the targeted region. Biochem Biophys Res Commun, 2004, 318: 303-310,
CrossRef Pubmed Google scholar
[]
Luo X, Nanda S, Zhang Y, Zhou X, Yang C, Pan H. Risk assessment of RNAi-based biopesticides. New Crops, 2024, 1,
CrossRef Google scholar
[]
Ma Z, Zheng Y, Chao Z, Chen H, Zhang Y, Yin M, Shen J, Yan S. Visualization of the process of a nanocarrier-mediated gene delivery: stabilization, endocytosis and endosomal escape of genes for intracellular spreading. Journal of Nanobiotechnology, 2022, 20: 124, pmcid: 8905852
CrossRef Pubmed Google scholar
[]
Madigan V, Zhang Y, Raghavan R, Wilkinson ME, Faure G, Puccio E, Segel M, Lash B, Macrae RK, Zhang F. Human paraneoplastic antigen Ma2 (PNMA2) forms icosahedral capsids that can be engineered for mRNA delivery. Proc Natl Acad Sci USA, 2024, 121, pmcid: 10945824
CrossRef Pubmed Google scholar
[]
Marre J, Traver EC, Jose AM. Extracellular RNA is transported from one generation to the next in Caenorhabditis elegans. Proc Natl Acad Sci USA, 2016, 113: 12496-12501, pmcid: 5098612
CrossRef Pubmed Google scholar
[]
Martinez Z, De Schutter K, Van Damme EJM, Vogel E, Wynant N, Vanden Broeck J, Christiaens O, Smagghe G. Accelerated delivery of dsRNA in lepidopteran midgut cells by a Galanthus nivalis lectin (GNA)-dsRNA-binding domain fusion protein. Pestic Biochem Physiol, 2021, 175,
CrossRef Pubmed Google scholar
[]
Mitter N, Worrall EA, Robinson KE, Li P, Jain RG, Taochy C, Fletcher SJ, Carroll BJ, Lu GQ, Xu ZP. Clay nanosheets for topical delivery of RNAi for sustained protection against plant viruses. Nat Plants, 2017, 3: 16207,
CrossRef Pubmed Google scholar
[]
Nakayashiki H, Kadotani N, Mayama S. Evolution and diversification of RNA silencing proteins in fungi. J Mol Evol, 2006, 63: 127-135,
CrossRef Pubmed Google scholar
[]
Nguyen TC, Zaleta-Rivera K, Huang X, Dai X, Zhong S. RNA, Action through Interactions. Trends in genetics : TIG., 2018, 34: 867-882,
CrossRef Pubmed Google scholar
[]
Niehl A, Wyrsch I, Boller T, Heinlein M. Double-stranded RNAs induce a pattern-triggered immune signaling pathway in plants. New Phytol, 2016, 211: 1008-1019,
CrossRef Pubmed Google scholar
[]
Nowara D, Gay A, Lacomme C, Shaw J, Ridout C, Douchkov D, Hensel G, Kumlehn J, Schweizer P. HIGS: host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis. Plant Cell, 2010, 22: 3130-3141, pmcid: 2965548
CrossRef Pubmed Google scholar
[]
Patzel V, Rutz S, Dietrich I, Koberle C, Scheffold A, Kaufmann SH. Design of siRNAs producing unstructured guide-RNAs results in improved RNA interference efficiency. Nat Biotechnol, 2005, 23: 1440-1444,
CrossRef Pubmed Google scholar
[]
Petrick JS, Brower-Toland B, Jackson AL, Kier LD. Safety assessment of food and feed from biotechnology-derived crops employing RNA-mediated gene regulation to achieve desired traits: a scientific review. Regulatory Toxicology and Pharmacology : RTP, 2013, 66: 167-176,
CrossRef Pubmed Google scholar
[]
Qureshi A, Thakur N, Kumar M. VIRsiRNApred: a web server for predicting inhibition efficacy of siRNAs targeting human viruses. J Transl Med, 2013, 11: 305, pmcid: 3878835
CrossRef Pubmed Google scholar
[]
Rank AP, Koch A. Lab-to-Field Transition of RNA Spray Applications - How Far Are We?. Front Plant Sci, 2021, 12, pmcid: 8554022
CrossRef Pubmed Google scholar
[]
Ren B, Wang X, Duan J, Ma J. Rhizobial tRNA-derived small RNAs are signal molecules regulating plant nodulation. Science, 2019, 365: 919-922,
CrossRef Pubmed Google scholar
[]
Rennie W, Kanoria S, Liu C, Carmack CS, Lu J, Ding Y. Sfold Tools for MicroRNA Target Prediction. Methods in Molecular Biology (clifton, NJ), 2019, 1970: 31-42,
CrossRef Google scholar
[]
Robbins M, Judge A, MacLachlan I. siRNA and innate immunity. Oligonucleotides, 2009, 19: 89-102,
CrossRef Pubmed Google scholar
[]
Rodrigues TB, Petrick JS. Safety Considerations for Humans and Other Vertebrates Regarding Agricultural Uses of Externally Applied RNA Molecules. Front Plant Sci, 2020, 11: 407, pmcid: 7191066
CrossRef Pubmed Google scholar
[]
Rodrigues T, Sridharan K, Manley B, Cunningham D, Narva K (2021) Development of dsRNA as a Sustainable Bioinsecticide: From Laboratory to Field. In: Crop Protection Products for Sustainable Agriculture, vol 1390. ACS Symposium Series, vol 1390. American Chemical Society, pp 65–82. https://doi.org/10.1021/bk-2021-1390.ch00510.1021/bk-2021-1390.ch005
[]
Roost C, Lynch SR, Batista PJ, Qu K, Chang HY, Kool ET. Structure and thermodynamics of N6-methyladenosine in RNA: a spring-loaded base modification. J Am Chem Soc, 2015, 137: 2107-2115, pmcid: 4405242
CrossRef Pubmed Google scholar
[]
Ruijtenberg S, Sonneveld S, Cui TJ, Logister I, de Steenwinkel D, Xiao Y, MacRae IJ, Joo C, Tanenbaum ME. mRNA structural dynamics shape Argonaute-target interactions. Nat Struct Mol Biol, 2020, 27: 790-801, pmcid: 8210632
CrossRef Pubmed Google scholar
[]
Schubert S, Grunweller A, Erdmann VA, Kurreck J. Local RNA target structure influences siRNA efficacy: systematic analysis of intentionally designed binding regions. J Mol Biol, 2005, 348: 883-893,
CrossRef Pubmed Google scholar
[]
Sciabola S, Cao Q, Orozco M, Faustino I, Stanton RV. Improved nucleic acid descriptors for siRNA efficacy prediction. Nucleic Acids Res, 2013, 41: 1383-1394,
CrossRef Pubmed Google scholar
[]
Secic E, Kogel KH. Requirements for fungal uptake of dsRNA and gene silencing in RNAi-based crop protection strategies. Curr Opin Biotechnol, 2021, 70: 136-142,
CrossRef Pubmed Google scholar
[]
Segel M, Lash B, Song J, Ladha A, Liu CC, Jin X, Mekhedov SL, Macrae RK, Koonin EV, Zhang F. Mammalian retrovirus-like protein PEG10 packages its own mRNA and can be pseudotyped for mRNA delivery. Science, 2021, 373: 882-889, pmcid: 8431961
CrossRef Pubmed Google scholar
[]
Shao Y, Chan CY, Maliyekkel A, Lawrence CE, Roninson IB, Ding Y. Effect of target secondary structure on RNAi efficiency. RNA (new York, NY), 2007, 13: 1631-1640,
CrossRef Google scholar
[]
Tabein S, Jansen M, Noris E, Vaira AM, Marian D, Behjatnia SAA, Accotto GP, Miozzi L. The Induction of an Effective dsRNA-Mediated Resistance Against Tomato Spotted Wilt Virus by Exogenous Application of Double-Stranded RNA Largely Depends on the Selection of the Viral RNA Target Region. Front Plant Sci, 2020, 11, pmcid: 7732615
CrossRef Pubmed Google scholar
[]
Tafer H, Ameres SL, Obernosterer G, Gebeshuber CA, Schroeder R, Martinez J, Hofacker IL. The impact of target site accessibility on the design of effective siRNAs. Nat Biotechnol, 2008, 26: 578-583,
CrossRef Pubmed Google scholar
[]
Tenllado F, Martinez-Garcia B, Vargas M, Diaz-Ruiz JR. Crude extracts of bacterially expressed dsRNA can be used to protect plants against virus infections. BMC Biotechnol, 2003, 3: 3, pmcid: 153545
CrossRef Pubmed Google scholar
[]
Thuesombat P, Hannongbua S, Akasit S, Chadchawan S. Effect of silver nanoparticles on rice (Oryza sativa L. cv. KDML 105) seed germination and seedling growth. Ecotoxicol Environ Saf., 2014, 104: 302-309,
CrossRef Pubmed Google scholar
[]
Townshend RJL, Eismann S, Watkins AM, Rangan R, Karelina M, Das R, Dror RO. Geometric deep learning of RNA structure. Science, 2021, 373: 1047-1051, pmcid: 9829186
CrossRef Pubmed Google scholar
[]
Underwood JG, Uzilov AV, Katzman S, Onodera CS, Mainzer JE, Mathews DH, Lowe TM, Salama SR, Haussler D. FragSeq: transcriptome-wide RNA structure probing using high-throughput sequencing. Nat Methods, 2010, 7: 995-1001, pmcid: 3247016
CrossRef Pubmed Google scholar
[]
Uslu VV, Bassler A, Krczal G, Wassenegger M. High-Pressure-Sprayed Double Stranded RNA Does Not Induce RNA Interference of a Reporter Gene. Front Plant Sci, 2020, 11, pmcid: 7773025
CrossRef Pubmed Google scholar
[]
Vastenhouw NL, Brunschwig K, Okihara KL, Muller F, Tijsterman M, Plasterk RH. Gene expression: long-term gene silencing by RNAi. Nature, 2006, 442: 882,
CrossRef Pubmed Google scholar
[]
Wang Q, Zhang C, Shen G, Liu H, Fu H, Cui D. Fluorescent carbon dots as an efficient siRNA nanocarrier for its interference therapy in gastric cancer cells. Journal of Nanobiotechnology, 2014, 12: 58, pmcid: 4304159
CrossRef Pubmed Google scholar
[]
Wang XW, Liu CX, Chen LL, Zhang QC. RNA structure probing uncovers RNA structure-dependent biological functions. Nat Chem Biol, 2021, 17: 755-766,
CrossRef Pubmed Google scholar
[]
Wen HG, Zhao JH, Zhang BS, Gao F, Wu XM, Yan YS, Zhang J, Guo HS. Microbe-induced gene silencing boosts crop protection against soil-borne fungal pathogens. Nat Plants, 2023, 9: 1409-1418,
CrossRef Pubmed Google scholar
[]
Westerhout EM, Ooms M, Vink M, Das AT, Berkhout B. HIV-1 can escape from RNA interference by evolving an alternative structure in its RNA genome. Nucleic Acids Res, 2005, 33: 796-804, pmcid: 548362
CrossRef Pubmed Google scholar
[]
Wright DJ, Force CR, Znosko BM. Stability of RNA duplexes containing inosinecytosine pairs. Nucleic Acids Res., 2018, 46: 12099-12108, pmcid: 6294561
CrossRef Pubmed Google scholar
[]
Xu L, Xu S, Sun L, Zhang Y, Luo J, Bock R, Zhang J. Synergistic action of the gut microbiota in environmental RNA interference in a leaf beetle. Microbiome, 2021, 9: 98, pmcid: 8097945
CrossRef Pubmed Google scholar
[]
Yang X, He Q, Guo F, Sun X, Zhang J, Chen Y. Impacts of carbon-based nanomaterials on nutrient removal in constructed wetlands: Microbial community structure, enzyme activities, and metabolism process. J Hazard Mater, 2021, 401,
CrossRef Pubmed Google scholar
[]
Yin GH, Sun ZN, Song YZ, An HL, Zhu CX, Wen FJ. Bacterially expressed double-stranded RNAs against hot-spot sequences of tobacco mosaic virus or potato virus Y genome have different ability to protect tobacco from viral infection. Appl Biochem Biotechnol, 2010, 162: 1901-1914,
CrossRef Pubmed Google scholar
[]
Zhang T, Jin Y, Zhao JH, Gao F, Zhou BJ, Fang YY, Guo HS. Host-Induced Gene Silencing of the Target Gene in Fungal Cells Confers Effective Resistance to the Cotton Wilt Disease Pathogen Verticillium dahliae. Mol Plant, 2016, 9: 939-942,
CrossRef Pubmed Google scholar
[]
Zhang T, Zhao YL, Zhao JH, Wang S, Jin Y, Chen ZQ, Fang YY, Hua CL, Ding SW, Guo HS. Cotton plants export microRNAs to inhibit virulence gene expression in a fungal pathogen. Nat Plants, 2016, 2: 16153,
CrossRef Pubmed Google scholar
[]
Zhao JH, Guo HS. RNA silencing: From discovery and elucidation to application and perspectives. J Integr Plant Biol, 2022, 64: 476-498,
CrossRef Pubmed Google scholar
[]
Zhao JH, Zhang T, Liu QY, Guo HS. Trans-kingdom RNAs and their fates in recipient cells: advances, utilization, and perspectives. Plant Commun, 2021, 2, pmcid: 8060725
CrossRef Pubmed Google scholar
[]
Zhao Q, Zhao Z, Fan X, Yuan Z, Mao Q, Yao Y. Review of machine learning methods for RNA secondary structure prediction. PLoS Comput Biol, 2021, 17, pmcid: 8389396
CrossRef Pubmed Google scholar
[]
Zhu KY, Palli SR. Mechanisms, Applications, and Challenges of Insect RNA Interference. Annu Rev Entomol, 2020, 65: 293-311,
CrossRef Pubmed Google scholar
Funding
the National Science Foundation of China(32230003); Science and Technology Bureau of Xinjiang Production and Construction Corps(2022DB014)

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