Please wait a minute...
浙江大学学报（农业与生命科学版）
Journal of Zhejiang University (Agriculture and Life Sciences)  2022, Vol. 48 Issue (6): 683-691    DOI: 10.3785/j.issn.1008-9209.2022.06.302
Reviews     
Application of RNA interference technology in pest control and its safety
Fang WANG1(),Cong DANG1,Hongxia JIN1,2,Shan XIAO1,Fujun ZHONG1,Qi FANG1,Hongwei YAO1,Gongyin YE1()
1.State Key Laboratory of Rice Biology/Ministry of Agriculture and Rural Affairs Key Laboratory of Molecular Biology of Crop Pathogens and Insects/Zhejiang Provincial Key Laboratory of Biology of Crop Pathogens and Insects, Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, China
2.Zhejiang University Library, Hangzhou 310058, China
Download: HTML   HTML ( )    PDF(2718KB)
Export: BibTeX | EndNote (RIS)      

Abstract  

RNA interference (RNAi) is a highly conserved gene-silencing phenomenon, induced by 20-30 nucleotide (nt) small molecules of non-coding RNA in vivo. Three non-coding RNAs, such as small interfering RNA (siRNA), microRNA (miRNA) and PIWI-interacting RNA (piRNA), play important roles in RNAi of eukaryotes including insects. The applications of RNAi in pest control are mainly on the research of gene function, transgenic insect-resistant plants and novel nucleic acid pesticides. Before the applications, the safety risks in terms of non-target effects, target pest resistance and environmental persistence of interfering RNAs need to be strictly evaluated. In this paper, the mechanism of RNAi technology, application and safety of RNAi in agro-forestry pest control are described, which provide some theoretical basis for RNAi technology in pest control.

Key words： RNA interference      double-stranded RNA      microRNA      pest control      application      safety     
Received: 30 June 2022      Published: 27 December 2022
CLC:  Q 963  
Corresponding Authors: Gongyin YE     E-mail: wangf121@163.com;chu@zju.edu.cn
Service
E-mail this article
Add to my bookshelf
Add to citation manager
E-mail Alert
RSS
Articles by authors
Fang WANG
Cong DANG
Hongxia JIN
Shan XIAO
Fujun ZHONG
Qi FANG
Hongwei YAO
Gongyin YE
Cite this article:

Fang WANG,Cong DANG,Hongxia JIN,Shan XIAO,Fujun ZHONG,Qi FANG,Hongwei YAO,Gongyin YE. Application of RNA interference technology in pest control and its safety. Journal of Zhejiang University (Agriculture and Life Sciences), 2022, 48(6): 683-691.

URL:

https://www.zjujournals.com/agr/10.3785/j.issn.1008-9209.2022.06.302     OR     https://www.zjujournals.com/agr/Y2022/V48/I6/683


RNA干扰技术在害虫防治中的应用及其安全性

RNA干扰（RNA interference, RNAi）是一种在生物体内高度保守的、由20～30个核苷酸（nucleotide, nt）组成的小分子非编码RNA引发的基因沉默现象。在昆虫等真核生物中，干扰小RNA（small interfering RNA, siRNA）、微RNA（microRNA, miRNA）和PIWI蛋白互作RNA（PIWI-interacting RNA, piRNA）等小分子非编码RNA在RNA干扰中发挥着重要作用。RNA干扰在害虫防治中的应用主要体现在基因功能研究、转基因抗虫植物及新型核酸农药研发等方面。RNA干扰技术及其产品在应用之前，需严格评价其在非靶标效应、靶标害虫的抗性及环境持久性方面的安全风险。本文就RNA干扰技术的作用机制、RNA干扰在农林害虫防治中的应用及其安全性等方面进行了综述，以期为RNA干扰技术在害虫防治中获得更广泛的应用提供一定的理论依据。


关键词： RNA干扰,  双链RNA,  微RNA,  害虫防治,  应用,  安全性 
Fig. 1 High-frequency key words of insect RNAi from papers searched in Web of Science

植物

Plant

靶标基因

Target gene

靶标害虫

Target pest

文献

Reference

烟草

Nicotiana spp.

CYP82E4v1、hunchback桃蚜 Myzus persicae[24-25]
gut sucrase、aquaporin、sugar transporter番茄木虱 Bactericera cockerelli[26]

V-ATPase A、acetylcholinesterase、ecdysone receptor、

trehalose-6-phosphate synthase

烟粉虱 Bemisia tabaci[27-28]
β-glucosidase 1、CYP6B46烟草天蛾 Manduca sexta[29]
chitinase东方黏虫 Mythimna separata[30]

gst16、cytochrome p450 monooxygenase、V-ATPase A、

chitin synthase

棉铃虫 Helicoverpa armigera[31-32]
actin、tubulin、V-ATPase B、Snf7西花蓟马 Frankliniella occidentalis[33]

拟南芥

Arabidopsis thaliana

Rack1、C002、cuticular protein桃蚜 Myzus persicae[34-35]
glutathione S-transferase烟粉虱 Bemisia tabaci[18]
arginine kinase棉铃虫 Helicoverpa armigera[36]
arginine kinase、integrin β1subunit小菜蛾 Plutella xylostella[37]
莴苣 Lactuca sativaV-ATPase A烟粉虱 Bemisia tabaci[38]

马铃薯

Solanum tuberosum

β-actin

马铃薯甲虫

Leptinotarsa decemlineata

[19]

番茄

Solanum lycopersicum

V-ATPase A、arginine kinase番茄潜麦蛾 Tutaabsoluta[39]
V-ATPase A烟粉虱 Bemisia tabaci[40]
juvenile hormone acid methyl transferase、chitinase棉铃虫 Helicoverpa armigera[41-42]
棉花Gossypium hirsutumNDUFV2、HaHR3、CYP6AE14棉铃虫 Helicoverpa armigera[1，43-44]
大麦 Hordeum vulgarestructural sheath protein麦长管蚜 Sitobion avenae[45]
小麦 Triticum aestivumlipase maturation factor 2-like、zinc finger protein麦长管蚜 Sitobion avenae[46-47]

玉米

Zea mays

fvvgr、dvbol、V-ATPase A

玉米根萤叶甲

Diabrotica virgifera virgifera

[2，48]

水稻

Oryza sativa

HT1、car、try、EcR褐飞虱 Nilaparvata lugens[49-50]
heat shock protein二化螟 Chilo suppressalis[51]
Table 1 Summary of transgenic insect-resistant plants based on RNAi technology
[1]   MAO Y B, CAI W J, WANG J W, et al. Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol[J]. Nature Biotechnology, 2007, 25(11): 1307-1313. DOI:10.1038/nbt1352
doi: 10.1038/nbt1352
[2]   BAUM J A, BOGAERT T, CLINTON W, et al. Control of coleopteran insect pests through RNA interference[J]. Nature Biotechnology, 2007, 25(11): 1322-1326. DOI:10.1038/nbt1359
doi: 10.1038/nbt1359
[3]   PRICE D R G, GATEHOUSE J A. RNAi-mediated crop protection against insects[J]. Trends in Biotechnology, 2008, 26(7): 393-400. DOI:10.1016/j.tibtech.2008.04.004
doi: 10.1016/j.tibtech.2008.04.004
[4]   JINEK M, DOUDNA J A. A three-dimensional view of the molecular machinery of RNA interference[J]. Nature, 2009, 457(7228): 405-412. DOI:10.1038/nature07755
doi: 10.1038/nature07755
[5]   MELLO C C, CONTE D. Revealing the world of RNA interference[J]. Nature, 2004, 431(7006): 338-342. DOI:10.1038/nature02872
doi: 10.1038/nature02872
[6]   TOMARI Y, ZAMORE P D. Perspective: machines for RNAi[J]. Genes & Development, 2005, 19(5): 517-529. DOI:10.1101/gad.1284105
doi: 10.1101/gad.1284105
[7]   GATEHOUSE J A, PRICE D R G. Protection of crops against insect pests using RNA interference[M]//VILCINSKAS A. Insect Biotechnology. London, UK: Springer, 2011:145-168.
[8]   CARTHEW R W, SONTHEIMER E J. Origins and mechanisms of miRNAs and siRNAs[J]. Cell, 2009, 136(4): 642-655. DOI:10.1016/j.cell.2009.01.035
doi: 10.1016/j.cell.2009.01.035
[9]   KIM V N. MicroRNA biogenesis: coordinated cropping and dicing[J]. Nature Reviews-Molecular Cell Biology, 2005, 6(5): 376-385. DOI:10.1038/nrm1644
doi: 10.1038/nrm1644
[10]   Origin VOINNET O., biogenesis, and activity of plant microRNAs [J]. Cell, 2009, 136(4): 669-687. DOI:10.1016/j.cell.2009.01.046
doi: 10.1016/j.cell.2009.01.046
[11]   SIOMI M C, SATO K, PEZIC D, et al. PIWI-interacting small RNAs: the vanguard of genome defence[J]. Nature Reviews-Molecular Cell Biology, 2011, 12(4): 246-258. DOI:10.1038/nrm3089
doi: 10.1038/nrm3089
[12]   IWASAKI Y W, SIOMI M C, SIOMI H. PIWI-interacting RNA: its biogenesis and functions[J]. Annual Review of Biochemistry, 2015, 84: 405-433. DOI:10.1146/annurev-biochem-060614-034258
doi: 10.1146/annurev-biochem-060614-034258
[13]   WEICK E M, MISKA E A. piRNAs: from biogenesis to function[J]. Development, 2014, 141(18): 3458-3471. DOI:10.1242/dev.094037
doi: 10.1242/dev.094037
[14]   KENNERDELL J R, CARTHEW R W. Use of dsRNA-mediated genetic interference to demonstrate that frizzled and frizzled 2 act in the wingless pathway[J]. Cell, 1998, 95(7): 1017-1026. DOI:10.1016/s0092-8674(00)81725-0
doi: 10.1016/s0092-8674(00)81725-0
[15]   MA Z Z, ZHOU H, WEI Y L, et al. A novel plasmid-Escherichia coli system produces large batch dsRNAs for insect gene silencing[J]. Pest Management Science, 2020, 76(7): 2505-2512. DOI:10.1002/ps.5792
doi: 10.1002/ps.5792
[16]   SHANG F, NIU J Z, DING B Y, et al. The miR-9b microRNA mediates dimorphism and development of wing in aphids[J]. PNAS, 2020, 117(15): 8404-8409. DOI:10.1073/pnas.1919204117
doi: 10.1073/pnas.1919204117
[17]   JOGA M R, ZOTTI M J, SMAGGHE G, et al. RNAi efficiency, systemic properties, and novel delivery methods for pest insect control: What we know so far[J]. Frontiers in Physiology, 2016, 7: 533. DOI:10.3389/fphys.2016.00553
doi: 10.3389/fphys.2016.00553
[18]   EAKTEIMAN G, MOSES-KOCH R, MOSHITZKY P, et al. Targeting detoxification genes by phloem-mediated RNAi: a new approach for controlling phloem-feeding insect pests[J]. Insect Biochemistry and Molecular Biology, 2018, 100: 10-21. DOI:10.1016/j.ibmb.2018.05.008
doi: 10.1016/j.ibmb.2018.05.008
[19]   ZHANG J, KHAN S A, HASSE C, et al. Full crop protection from an insect pest by expression of long double-stranded RNAs in plastids[J]. Science, 2015, 347(6225): 991-994. DOI:10.1126/science.1261680
doi: 10.1126/science.1261680
[20]   AGRAWAL A, RAJAMANI V, REDDY V S, et al. Transgenic plants over-expressing insect-specific microRNA acquire insecticidal activity against Helicoverpa armigera: an alternative to Bt-toxin technology[J]. Transgenic Research, 2015, 24(5): 791-801. DOI:10.1007/s11248-015-9880-x
doi: 10.1007/s11248-015-9880-x
[21]   JIANG S, WU H, LIU H J, et al. The overexpression of insect endogenous small RNAs in transgenic rice inhibits growth and delays pupation of striped stem borer (Chilo suppressalis)[J]. Pest Management Science, 2017, 73(7): 1453-1461. DOI:10.1002/ps.4477
doi: 10.1002/ps.4477
[22]   HE K, XIAO H M, SUN Y, et al. Transgenic microRNA-14 rice shows high resistance to rice stem borer[J]. Plant Biotechnology Journal, 2018, 17(2): 461-471. DOI:10.1111/pbi.12990
doi: 10.1111/pbi.12990
[23]   ZHENG X X, WENG Z J, LI H, et al. Transgenic rice overexpressing insect endogenous microRNA csu-novel-260 is resistant to striped stem borer under field conditions[J]. Plant Biotechnology Journal, 2021, 19(3): 421-423. DOI:10.1111/pbi.13504
doi: 10.1111/pbi.13504
[24]   ZHAO D, QIN L J, ZHAO D G. RNA interference of the nicotine demethylase gene CYP82E4v1 reduces nornicotine content and enhances Myzus persicae resistance in Nicotiana tabacum L.[J]. Plant Physiology and Biochemistry, 2016, 107: 214-221. DOI:10.1016/j.plaphy.2016.04.016
doi: 10.1016/j.plaphy.2016.04.016
[25]   MAO J J, ZENG F R. Plant-mediated RNAi of a gap gene-enhanced tobacco tolerance against the Myzus persicae [J]. Transgenic Research, 2014, 23(1): 145-152. DOI:10.1007/s 11248-013-9739-y
doi: 10.1007/s
[26]   TZIN V, YANG X W, JING X F, et al. RNA interference against gut osmoregulatory genes in phloem-feeding insects[J]. Journal of Insect Physiology, 2015, 79: 105-112. DOI:10 .1016/j.jinsphys.2015.06.006
doi: 10
[27]   MALIK H J, RAZA A, AMIN I, et al. RNAi-mediated mortality of the whitefly through transgenic expression of double-stranded RNA homologous to acetylcholinesterase and ecdysone receptor in tobacco plants[J]. Scientific Reports, 2016, 6: 38469. DOI:10.1038/srep38469
doi: 10.1038/srep38469
[28]   GONG C, YANG Z Z, HU Y, et al. Silencing of the BtTPS genes by transgenic plant-mediated RNAi to control Bemisia tabaci MED[J]. Pest Management Science, 2022, 78(3): 1128-1137. DOI:10.1002/ps.6727
doi: 10.1002/ps.6727
[29]   POREDDY S, LI J C, BALDWIN I T. Plant-mediated RNAi silences midgut-expressed genes in congeneric lepidopteran insects in nature[J]. BMC Plant Biology, 2017, 17: 199. DOI:10.1186/s12870-017-1149-5
doi: 10.1186/s12870-017-1149-5
[30]   BAO W H, CAO B D, ZHANG Y N, et al. Silencing of Mythimna separata chitinase genes via oral delivery of in planta-expressed RNAi effectors from a recombinant plant virus[J]. Biotechnology Letters, 2016, 38(11): 1961-1966. DOI:10.1007/s10529-016-2186-0
doi: 10.1007/s10529-016-2186-0
[31]   SHABAB M, KHAN S A, VOGEL H, et al. OPDA isomerase GST16 is involved in phytohormone detoxification and insect development[J]. FEBS Journal, 2014, 281(12): 2769-2783. DOI:10.1111/febs.12819
doi: 10.1111/febs.12819
[32]   JIN S X, SINGH N D, LI L B, et al. Engineered chloroplast dsRNA silences cytochrome p450 monooxygenase, V-ATPase and chitin synthase genes in the insect gut and disrupts Helicoverpa armigera larval development and pupation[J]. Plant Biotechnology Journal, 2015, 13(3): 435-446. DOI:10.1111/pbi.12355
doi: 10.1111/pbi.12355
[33]   WU M T, DONG Y, ZHANG Q, et al. Efficient control of western flower thrips by plastid-mediated RNA interference[J]. PNAS, 2022, 119(15): e2120081119. DOI:10.1073/pnas.2120081119
doi: 10.1073/pnas.2120081119
[34]   PITINO M, COLEMAN A D, MAFFEI M E, et al. Silencing of aphid genes by dsRNA feeding from plants[J]. PLoS ONE, 2011, 6(10): e25709. DOI:10.1371/journal.pone.0025709
doi: 10.1371/journal.pone.0025709
[35]   BHATIA V, BHATTACHARYA R. Host mediated RNAi of cuticular protein gene impaired fecundity in green peach aphid Myzus persicae [J]. Pest Management Science, 2018, 74(9): 2059-2068. DOI:10.1002/ps.4900
doi: 10.1002/ps.4900
[36]   LIU F, WANG X D, ZHAO Y Y, et al. Silencing the HaAK gene by transgenic plant-mediated RNAi impairs larval growth of Helicoverpa armigera [J]. International Journal of Biological Sciences, 2015, 11(1): 67-74. DOI:10.7150/ijbs.10468
doi: 10.7150/ijbs.10468
[37]   FU S, LIU Z X, CHEN J Z, et al. Silencing arginine kinase/integrin β1 subunit by transgenic plant expressing dsRNA inhibits the development and survival of Plutella xylostella [J]. Pest Management Science, 2020, 76(5): 1761-1771. DOI:10.1002/ps.5701
doi: 10.1002/ps.5701
[38]   IBRAHIM A B, MONTEIRO T R, CABRAL G B, et al. RNAi-mediated resistance to whitefly (Bemisia tabaci) in genetically engineered lettuce (Lactuca sativa)[J]. Transgenic Research, 2017, 26(5): 613-624. DOI:10.1007/s11248-017-0035-0
doi: 10.1007/s11248-017-0035-0
[39]   CAMARGO R A, BARBOSA G O, POSSIGNOLO I P, et al. RNA interference as a gene silencing tool to control Tuta absoluta in tomato (Solanum lycopersicum)[J]. PeerJ, 2016, 4: e2673. DOI:10.7717/peerj.2673
doi: 10.7717/peerj.2673
[40]   PIZETTA C S R, RIBEIRO W R, FERREIRA A L, et al. RNA interference-mediated tolerance to whitefly (Bemisia tabaci) in genetically engineered tomato[J]. Plant Cell Tissue and Organ Culture, 2022, 148(2): 281-291. DOI:10.1007/s11240-021-02185-1
doi: 10.1007/s11240-021-02185-1
[41]   PRAKASH N M, MALIGEPPAGOL M, ASOKAN R, et al. Transgenic tomato expressing dsRNA of juvenile hormone acid O-methyl transferase gene of Helicoverpa armigera (Lepidoptera: Noctuidae) affects larval growth and its development[J]. Journal of Asia-Pacific Entomology, 2017, 20(2): 559-567. DOI:10.1016/j.aspen.2017.03.016
doi: 10.1016/j.aspen.2017.03.016
[42]   MAMTA, REDDY K R K, RAJAM M V. Targeting chitinase gene of Helicoverpa armigera by host-induced RNA interference confers insect resistance in tobacco and tomato[J]. Plant Molecular Biology, 2016, 90: 281-292. DOI:10.1007/s11103-015-0414-y
doi: 10.1007/s11103-015-0414-y
[43]   WU X M, YANG C Q, MAO Y B, et al. Targeting insect mitochondrial complexⅠfor plant protection[J]. Plant Biotechnology Journal, 2016, 14(9): 1925-1935. DOI:10.1111/pbi.12553
doi: 10.1111/pbi.12553
[44]   HAN Q, WANG Z Z, HE Y X, et al. Transgenic cotton plants expressing the HaHR3 gene conferred enhanced resistance to Helicoverpa armigera and improved cotton yield[J]. International Journal of Molecular Sciences, 2017, 18(9): 1874. DOI:10.3390/ijms18091874
doi: 10.3390/ijms18091874
[45]   ABDELLATEF E, WILL T, KOCH A, et al. Silencing the expression of the salivary sheath protein causes transgenera-tional feeding suppression in the aphid Sitobion avenae [J]. Plant Biotechnology Journal, 2015, 13(6): 849-857. DOI:10.1111/pbi.12322
doi: 10.1111/pbi.12322
[46]   XU L J, HOU Q L, ZHAO Y J, et al. Silencing of a lipase maturation factor 2-like gene by wheat-mediated RNAi reduces the survivability and reproductive capacity of the grain aphid, Sitobion avenae [J]. Archives of Insect Biochemistry and Physiology, 2017, 95(3): e21392. DOI:10.1002/arch.21392
doi: 10.1002/arch.21392
[47]   SUN Y W, 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[J]. Plant Biotechnology Journal, 2019, 17(5): 852-854. DOI:10.1111/pbi.13067
doi: 10.1111/pbi.13067
[48]   NIU X P, KASSA A, HU X, et al. Control of western corn rootworm (Diabrotica virgifera virgifera) reproduction through plant-mediated RNA interference[J]. Scientific Reports, 2017, 7: 12591. DOI:10.1038/s41598-017-12638-3
doi: 10.1038/s41598-017-12638-3
[49]   ZHA W J, PENG X X, CHEN R Z, et al. Knockdown of midgut genes by dsRNA-transgenic plant-mediated RNA interference in the hemipteran insect Nilaparvata lugens [J]. PLoS ONE, 2011, 6(5): e20504. DOI:10.1371/journal.pone.0020504
doi: 10.1371/journal.pone.0020504
[50]   YU R, XU X P, LIANG Y K, et al. The insect ecdysone receptor is a good potential target for RNAi-based pest control[J]. International Journal of Biological Sciences, 2014, 10(10): 1171-1180. DOI:10.7150/ijbs.9598
doi: 10.7150/ijbs.9598
[51]   MAO C, ZHU X P, WANG P P, et al. Transgenic double-stranded RNA rice, a potential strategy for controlling striped stem borer (Chilo suppressalis)[J]. Pest Management Science, 2022, 78(2): 785-792. DOI:10.1002/ps.6692 .
doi: 10.1002/ps.6692
[52]   王治文,高翔,马德君,等.核酸农药:极具潜力的新型植物保护产品[J].农药学学报,2019,21(5/6):681-691. DOI:10.16801/j.issn.1008-7303.2019.0112
WANG Z W, GAO X, MA D J, et al. Nucleic acid pesticides: the new plant protection products with great potential[J]. Chinese Journal of Pesticide Science, 2019, 21(5/6): 681-691. (in Chinese with English abstract)
doi: 10.16801/j.issn.1008-7303.2019.0112
[53]   GONG L, CHEN Y, HU Z, et al. Testing insecticidal activity of novel chemically synthesized siRNA against Plutella xylostella under laboratory and field conditions[J]. PLoS ONE, 2013, 8(5): e62990. DOI:10.1371/journal.pone.0062990
doi: 10.1371/journal.pone.0062990
[54]   ZHANG H, LI H C, GUAN R B, et al. Lepidopteran insect species-specific, broad-spectrum, and systemic RNA inter-ference by spraying dsRNA on larvae[J]. Entomologia Experimentalis et Applicata, 2015, 155(3): 218-228. DOI:10.1111/eea.12300
doi: 10.1111/eea.12300
[55]   MIGUEL K SAN, SCOTT J G. The next generation of insecticides: dsRNA is stable as a foliar-applied insecticide[J]. Pest Management Science, 2016, 72(4): 801-809. DOI:10.1002/ps.4056
doi: 10.1002/ps.4056
[56]   LI H C, GUAN R B, GUO H M, et al. New insights into an RNAi approach for plant defence against piercing-sucking and stem-borer insect pests[J]. Plant Cell and Environment, 2015, 38(11): 2277-2285. DOI:10.1111/pce.12546
doi: 10.1111/pce.12546
[57]   MA Z Z, ZHANG Y H, LI M S, et al. A first greenhouse application of bacteria-expressed and nanocarrier-delivered RNA pesticide for Myzus persicae control[J]. Journal of Pest Science, 2022.
[58]   FLETCHER S J, REEVES P T, HOANG B T, et al. A perspective on RNAi-based biopesticides[J]. Frontiers in Plant Science, 2020, 11: 51. DOI:10.3389/fpls.2020.00051
doi: 10.3389/fpls.2020.00051
[59]   FEDOROV Y, ANDERSON E M, BIRMINGHAM A, et al. Off-target effects by siRNA can induce toxic phenotype[J]. RNA, 2006, 12(7): 1188-1196. DOI:10.1261/rna.28106
doi: 10.1261/rna.28106
[60]   TSCHUCH C, SCHULZ A, PSCHERER A, et al. Off-target effects of siRNA specific for GFP [J]. BMC Molecular Biology, 2008, 9: 60. DOI:10.1186/1471-2199-9-60
doi: 10.1186/1471-2199-9-60
[61]   NUNES F M F, ALEIXO A C, BARCHUK A R, et al. Non-target effects of green fluorescent protein (GFP)-derived double-stranded RNA (dsRNA-GFP) used in honey bee RNA interference (RNAi) assays[J]. Insects, 2013, 4(1): 90-103. DOI:10.3390/insects4010090
doi: 10.3390/insects4010090
[62]   王锦达.赤拟谷盗RNAi及dsRNA脱靶效应的研究[D].南京:南京农业大学,2015.
WANG J D. RNAi in Tribolium castaneum and the off target effect of dsRNA[D]. Nanjing: Nanjing Agricultural University, 2015. (in Chinese with English abstract)
[63]   BACHMAN P M, BOLOGNESI R, MOAR W J, et al. Characterization of the spectrum of insecticidal activity of a double-stranded RNA with targeted activity against western corn rootworm (Diabrotica virgifera virgifera LeConte)[J]. Transgenic Research, 2013, 22: 1207-1222. DOI:10.1007/s11248-013-9716-5
doi: 10.1007/s11248-013-9716-5
[64]   PAN H P, YANG X W, ROMEIS J, et al. Dietary RNAi toxicity assay exhibits differential responses to ingested dsRNAs among lady beetles[J]. Pest Management Science, 2020, 76(11): 3606-3614. DOI:10.1002/ps.5894
doi: 10.1002/ps.5894
[65]   GUO M J, NANDA S, CHEN S M, et al. Oral RNAi toxicity assay suggests clathrin heavy chain as a promising molecular target for controlling the 28-spotted potato ladybird, Henosepilachna vigintioctopunctata [J]. Pest Management Science, 2022, 78(9): 3871-3879. DOI:10.1002/ps.6594
doi: 10.1002/ps.6594
[66]   NAITO Y, YAMADA T, MATSUMIYA T, et al. dsCheck: highly sensitive off-target search software for double-stranded RNA-mediated RNA interference[J]. Nucleic Acids Research, 2005, 33(): W589-W591. DOI:10.1093/nar/gki419
doi: 10.1093/nar/gki419
[67]   PAN H P, XU L H, NOLAND J E, et al. Assessment of potential risks of dietary RNAi to a soil micro-arthropod, Sinella curviseta Brook (Collembola: Entomobryidae)[J]. Frontiers in Plant Science, 2016, 7: 1028. DOI:10.3389/fpls.2016.01028
doi: 10.3389/fpls.2016.01028
[68]   DANG C, ZHANG Y P, SUN C Y, et al. dsRNAs targeted to the brown planthopper Nilaparvata lugens: assessing risk to a non-target, beneficial predator, Cyrtorhinus lividipennis [J]. Journal of Agricultural and Food Chemistry, 2022, 70(1): 373-380. DOI:10.1021/acs.jafc.1c05487
doi: 10.1021/acs.jafc.1c05487
[69]   KRISHNAN N, HALL M J, HELLMICH R L, et al. Evaluating toxicity of Varroa mite (Varroa destructor)-active dsRNA to monarch butterfly (Danaus plexippus) larvae[J]. PLoS ONE, 2021, 16(6): e0251884. DOI:10.1371/journal.pone.0251884
doi: 10.1371/journal.pone.0251884
[70]   ULRICH J, DAO V A, MAJUMDAR U, et al. Large scale RNAi screen in Tribolium reveals novel target genes for pest control and the proteasome as prime target[J]. BMC Genomics, 2015, 16: 674. DOI:10.1186/s12864-015-1880-y
doi: 10.1186/s12864-015-1880-y
[71]   TABARA H, SARKISSIAN M, KELLY W G, et al. The rde-1 gene, RNA interference, and transposon silencing in C. elegans [J]. Cell, 1999, 99(2): 123-132. DOI:10.1016/s0092-8674(00)81644-x
doi: 10.1016/s0092-8674(00)81644-x
[72]   何康来,王振营,沈萍.RNAi生物技术作物环境风险评估研究进展[J].生物安全学报,2014,23(4):238-247. DOI:10.3969/j.issn.2095-1787.2014.04.003
HE K L, WANG Z Y, SHEN P. Progress for environmental risk assessments of RNAi-based crops[J]. Journal of Biosafety, 2014, 23(4): 238-247. (in Chinese with English abstract)
doi: 10.3969/j.issn.2095-1787.2014.04.003
[73]   KHAJURIA C, IVASHUTA S, WIGGINS E, et al. Development and characterization of the first dsRNA-resistant insect population from western corn rootworm, Diabrotica virgifera virgifera LeConte[J]. PLoS ONE, 2018, 13(5): e0197059. DOI:10.1371/journal.pone.0197059
doi: 10.1371/journal.pone.0197059
[74]   MISHRA S, DEE J, MOAR W, et al. Selection for high levels of resistance to double-stranded RNA (dsRNA) in Colorado potato beetle (Leptinotarsa decemlineata Say) using non-transgenic foliar delivery[J]. Scientific Reports, 2021, 11: 6523. DOI:10.1038/s41598-021-85876-1
doi: 10.1038/s41598-021-85876-1
[75]   PEREIRA A E, TENHUMBERG B, MEINKE L J, et al. Southern corn rootworm (Coleoptera: Chrysomelidae) adult emergence and population growth assessment after selection with vacuolar ATPase-A double-stranded RNA over multiple generations[J]. Journal of Economic Entomology, 2019, 112(3): 1354-1364. DOI:10.1093/jee/toz008
doi: 10.1093/jee/toz008
[76]   DUBELMAN S, FISCHER J, ZAPATA F, et al. Environmental fate of double-stranded RNA in agricultural soils[J]. PLoS ONE, 2014, 9(3): e93155. DOI:10.1371/journal.pone.0093155
doi: 10.1371/journal.pone.0093155
[77]   BACHMAN P, FISCHER J, SONG Z H, et al. Environmental fate and dissipation of applied dsRNA in aoil, aquatic systems, and plants[J]. Frontiers in Plant Science, 2020, 11: 21. DOI:10.3389/fpls.2020.00021
doi: 10.3389/fpls.2020.00021
[1] Pengcheng NIE,Hui ZHANG,Hongliang GENG,Zheng WANG,Yong HE. Current situation and development trend of agricultural Internet of Things technology[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2021, 47(2): 135-146.
[2] Ying DU,Shuihu JIN,Zilu WEI,Xiaochen LI. Investigation of fragrant plant resources in Ziweishan National Forest Park and their landscape application evaluation[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2020, 46(4): 475-483.
[3] Meihua DENG,Youwei ZHU,Lili DUAN,Jing SHEN,Ying FENG. Analysis on integrated remediation model of “phytoremediation coupled with agro-production” for heavy metal pollution in farmland soil[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2020, 46(2): 135-150.
[4] Xinxia WANG,Jifeng WANG,Qiong HOU,Xiaojun WANG,Wuzhong NI. Effects of different fertilizing models on growth of single crop rice and nitrogen and phosphorus runoff losses[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2020, 46(2): 225-233.
[5] Long MENG,Tuhai HUANG,Jian CHEN,Fulin ZHONG,Jiachun SHI,Jianming XU. Safe utilization of farmland soil with cadmium pollution: strategies and deliberations.[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2019, 45(3): 263-271.
[6] Gangshuan BAI,Wei GENG,Dengfeng HE. Effects of super absorbent polymer with different application rates on soil characteristics and flue-cured tobacco growth in Qinba mountain area[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2019, 45(3): 343-354.
[7] Yanhua CHEN,Tao JIANG,Xuezhen WANG,Ping QIAN,Shunming TANG,Xingjia SHEN. Bmo-miR-0031-3p down-regulates the expression of Bombyx mori fibroin light chain gene BmFib-L in vivo[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2019, 45(2): 229-236.
[8] CHEN Pengfei. Applications and trends of unmanned aerial vehicle in agriculture[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2018, 44(4): 399-406.
[9] SHU Xinyuan, YAN Xu, PU Yehong, WANG Chao, PAN Jianwei. Action mechanisms of CRISPR/Cas system and its application in genetic improvement of crops[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2018, 44(3): 259-268.
[10] YANG Yang, GUO Zonglou. Key technology design of ecological ditch and its application in modern agriculture[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2017, 43(3): 377-388.
[11] LAN Yan, HUANG Peng, JIANG Guchihong, LEI Xiaobo, DING Chunbang, LI Tian. Effect of nitrogen application and planting density on grain yield and quality of japonica rice cultivar D46 in the planting area of Chengdu plain[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2016, 42(1): 63-73.
[12] Chen Fangyong1,2*, Ni Haizhi1, Wang Yin1, Ren Zhengchu1, Liu Jihong2, Wang Yiguang3. Effect of paclobutrazol (PP333) on twig dieback of Myrica rubra and control.[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2014, 40(6): 653-660.
[13] You Zhaotong1, Kong Yaguang2*, Hu Xiaofei2, Chen Tianjun2. Research and development of quality traceability system based on intellectual technology for bee products[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2014, 40(5): 533-540.
[14] Shen Enhui, Liu Yang, Ye Chuyu, Fan Longjiang. Recent studies on non-coding small RNAs in plants[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2014, 40(4): 370-378.
[15] GUO Yan, JU Qingsong, YAO Hongwei*, JIANG Mingxing, YE Gongyin, CHENG Jiaan. Effect of environmental factor changes on the activity of nonspecific esterase in brown planthopper, Nilaparvata lugens Stl (Hemiptera: Delphacidae)[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2013, 39(6): 591-599.