|
|
|
| Progress in the Application of CRISPR/Cas9 Gene Editing Technology in Pest Gene Function and Pest Control Research |
| XIANG Yun-Ju1, ZHANG Wang-He1,*, XU Jin1,2,*, YE Hui3 |
1 Yunnan Key Laboratory of Forest Disaster Warning and Control, Southwest Forestry University, Kunming 650224, China;
2 Key Laboratory of Ministry of Education for Forest Resources Conservation and Utilization in the Southwest Mountains of China, Southwest Forestry University, Kunming 650224, China;
3 School of Ecology and Environment, Yunnan University, Kunming 650091, China |
|
|
|
|
Abstract CRISPR/Cas9 technology, as the third generation of gene editing technology with simple design, convenient and quick operation, and low cost of use, has set off a technological revolution in the field of life sciences research. Currently, CRISPR/Cas9 has been successfully applied to gene editing in eukaryotic and prokaryotic organisms such as animals, plants and microorganisms. In recent years, CRISPR/Cas9 has also been used in the study of insects, and has shown great promise in the exploration of new technologies for pest control. This paper mainly provides an overview of the working principle of the CRISPR/Cas9 system and summarizes the progress of this technology in pest gene function and pest control. This review provides a reference for the use of CRISPR/Cas9 to carry out broader research in insect molecular biology and pest management strategies.
|
|
Received: 21 August 2023
|
|
|
|
Corresponding Authors:
* Corresponding authors, zhangwanghe0116@163.com; xujin2798@126.com
|
|
|
|
[1] Adli M.2018. The CRISPR tool kit for genome editing and beyond[J]. Nature Communications, 9(1): 1911.
[2] Awata H, Watanabe T, Hamanaka Y, et al.2015. Knockout crickets for the study of learning and memory: Dopamine receptor Dop1 mediates aversive but not appetitive reinforcement in crickets[J]. Scientific Reports, 5(2): 15885.
[3] Bai X, Zeng T, Ni X Y, et al.2019. CRISPR/Cas9‐mediated knockout of the eye pigmentation gene white leads to alterations in colour of head spots in the oriental fruit fly,Bactrocera dorsalis[J]. Insect Molecular Biology, 28(6): 837-849.
[4] Barton N H, Hammond A M, Kyrou K, et al.2017. The creation and selection of mutations resistant to a gene drive over multiple generations in the malaria mosquito[J]. PLOS Genetics, 13(10): e1007039.
[5] Bassett A R, Tibbit C, Ponting C P, et al.2013. Highly efficient targeted mutagenesis of Drosophila with the CRISPR/Cas9 system[J]. Cell Reports, 4(1): 220-228.
[6] Bi H, Li X, Xu X, et al.2022a. Masculinizer and doublesex as key factors regulate sexual dimorphism in Ostrinia furnacalis[J]. Cells, 11(14): 2161.
[7] Bi H, Merchant A, Gu J, et al.2022b. CRISPR/Cas9-mediated mutagenesis of Abdominal-A and Ultrabithorax in the asian corn borer, Ostrinia furnacalis[J]. Insects, 13(4): 384.
[8] Bi H, Xu X, Li X, et al.2022c. CRISPR/Cas9-mediated Serine protease 2 disruption induces male sterility in Spodoptera litura[J]. Frontiers In Physiology, 13: 931824.
[9] Bi H L, Xu J, He L, et al.2019. CRISPR/Cas9-mediated ebony knockout results in puparium melanism in Spodoptera litura[J]. Insect Science, 26(6): 1011-1019.
[10] Bi H L, Xu J, Tan A J, et al.2016. CRISPR/Cas9-mediated targeted gene mutagenesis in Spodoptera litura[J]. Insect Science, 23(3): 469-477.
[11] Bin Moon S, Lee J M, Kang J G, et. al.2018. Highly efficient genome editing by CRISPR-Cpf1 using CRISPR RNA with a uridinylate-rich 3′-overhang[J]. Nature Communications, 9(1): 3651.
[12] Bolukbasi M F, Gupta A, Wolfe S A.2016. Creating and evaluating accurate CRISPR-Cas9 scalpels for genomic surgery[J]. Nature Methods, 13(1): 41-50.
[13] Buchman A, Marshall J M, Ostrovski D, et al.2018. Synthetically engineered Medea gene drive system in the worldwide crop pest Drosophila suzukii[J]. Proceedings of the National Academy of Sciences of the USA, 115(18): 4725-4730.
[14] Cagliari D, Smagghe G, Zotti M, et al.2020. RNAi and CRISPR/Cas9 as functional genomics tools in the neotropical stink bug, Euschistus heros[J]. Insects, 11(12): 838.
[15] Chang H, Liu Y, Ai D, et al.2017. A Pheromone antagonist regulates optimal mating time in the moth Helicoverpa armigera[J]. Current Biology, 27(11): 1610-1615.
[16] Chen H, Sun H, Xie J, et al.2023. CRISPR/Cas9-induced mutation of sex peptide receptor gene Bdspr affects ovary, egg laying, and female fecundity in Bactrocera dorsalis (Hendel) (Diptera: Tephritidae)[J]. Journal of Insect Science, 23(1): 2.
[17] Chen J S, Ma E, Harrington L B, et al.2018. CRISPR-Cas12a target binding unleashes indiscriminate single-stranded DNase activity[J]. Science, 360(6387): 436-439.
[18] Chen J X, Li W X, Lyu J, et al.2021. CRISPR/Cas9-mediated knockout of the NlCSAD gene results in darker cuticle pigmentation and a reduction in female fecundity in Nilaparvata lugens (Hemiptera: Delphacidae)[J]. Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology, 256: 110921.
[19] Cong L, Ran F A, Cox D, et al.2013. Multiplex genome engineering using CRISPR/Cas systems[J]. Science, 339(6121): 819-823.
[20] de Souza Pacheco I, Doss A A, Vindiola B G, et al.2022. Efficient CRISPR/Cas9-mediated genome modification of the glassy-winged sharpshooter Homalodisca vitripennis (Germar)[J]. Scientific Reports, 12(1): 6428.
[21] Deltcheva E, Chylinski K, Sharma C M,et al.2011. CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III[J]. Nature, 471(7340): 602-607.
[22] Dong S, Lin J, Held N L, et al.2015. Heritable CRISPR/Cas9-mediated genome editing in the yellow fever mosquito, Aedes aegypti[J]. Public Library of Science ONE, 10(3): e0122353.
[23] Doudna J A, Charpentier E.2014. Genome editing. The new frontier of genome engineering with CRISPR-Cas9[J]. Science, 346(6213): 1258096.
[24] Esvelt K M, Smidler A L, Catteruccia F, et al.2014. Concerning RNA-guided gene drives for the alteration of wild populations[J]. eLife, 3: e03401
[25] Gantz V M, Bier E.2015. Genome editing. The mutagenic chain reaction: A method for converting heterozygous to homozygous mutations[J]. Science, 348(6233): 442-444.
[26] Gantz V M, Jasinskiene N, Tatarenkova O, et al.2015. Highly efficient Cas9-mediated gene drive for population modification of the malaria vector mosquito Anopheles stephensi[J]. Proceedings of the National Academy of Sciences, 112(49): E6736-43.
[27] Gratz S J, Cummings A M, Nguyen J N, et al.2013. Genome engineering of Drosophila with the CRISPR RNA-guided Cas9 nuclease[J]. Genetics, 194(4): 1029-1035.
[28] Gould F, Willis K, Burt A.2021. Double drives and private alleles for localised population genetic control[J]. PLOS Genetics, 17(3): e1009333.
[29] Gu J, Wang J, Bi H, et al.2022. CRISPR/Cas9-mediated mutagenesis of exs-specific doublesex splicing variants leads to sterility in Spodoptera frugiperda, a global invasive pest[J]. Cells, 11(22): 3557.
[30] Gui S, Taning C N T, Wei D, et al.2020. First report on CRISPR/Cas9-targeted mutagenesis in the Colorado potato beetle, Leptinotarsa decemlineata[J]. Journal Of Insect Physiology, 121: 104013.
[31] Guo X, Yu Q, Chen D, et al.2020. 4-vinylanisole is an aggregation pheromone in locusts[J]. Nature, 584(7822): 584-588.
[32] Guo Z, Sun D, Kang S, et al.2019. CRISPR/Cas9-mediated knockout of both the PxABCC2 and PxABCC3 genes confers high-level resistance to Bacillus thuringiensis Cry1Ac toxin in the diamondback moth, Plutella xylostella (L.)[J]. Insect Biochemistry and Molecular Biology, 107: 31-38.
[33] Hammond A, Galizi R, Kyrou K, et al.2016. A CRISPR-Cas9 gene drive system targeting female reproduction in the malaria mosquito vector Anopheles gambiae[J]. Nature Biotechnology, 34(1): 78-83.
[34] Han W, Tang F, Zhong Y, et al.2021. Identification of yellow gene family and functional analysis of Spodoptera frugiperda yellow-y by CRISPR/Cas9[J]. Pesticide Biochemistry and Physiology, 178: 104937.
[35] Harris A F, McKemey A R, Nimmo D, et al.2012. Successful suppression of a field mosquito population by sustained release of engineered male mosquitoes[J]. Nature Biotechnology, 30(9): 828-830.
[36] Harris A F, Nimmo D, McKemey A R, et al.2011. Field performance of engineered male mosquitoes[J]. Nature Biotechnology, 29(11): 1034-1037.
[37] Heu C C, Gross R J, Le K P, et al.2022. CRISPR-mediated knockout of cardinal and cinnabar eye pigmentation genes in the western tarnished plant bug[J]. Scientific Reports, 12(1): 4917.
[38] Heu C C, McCullough F M, Luan J, et al.2020. CRISPR-Cas9-based genome editing in the silverleaf whitefly (Bemisia tabaci)[J]. Crispr Journal, 3(2): 89-96.
[39] Hsu P D, Lander E S, Zhang F.2014. Development and applications of CRISPR-Cas9 for genome engineering[J]. Cell, 157(6): 1262-1278.
[40] Hu J H, Miller S M, Geurts M H, et al.2018. Evolved Cas9 variants with broad PAM compatibility and high DNA specificity[J]. Nature, 556(7699): 57-63.
[41] Huang S, Weigel D, Beachy R N, et al.2016a. A proposed regulatory framework for genome-edited crops[J]. Nature Genetics, 48(2): 109-111.
[42] Huang Y, Chen Y, Zeng B, et al.2016b. CRISPR/Cas9 mediated knockout of the abdominal-A homeotic gene in the global pest, diamondback moth (Plutella xylostella)[J]. Insect Biochemistry and Molecular Biology, 75: 98-106.
[43] Jansen R, van Embden J D, Gaastra W, et al.2002. Identification of a novel family of sequence repeats among prokaryotes[J]. OMICS A Journal of Integrative Biology, 6(1): 23-33.
[44] Ji S X, Bi S Y, Wang X D, et al.2022. First report on CRISPR/Cas9-based genome editing in the destructive invasive pest Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae)[J]. Frontiers in Genetics, 13: 865622.
[45] Ishino Y, Shinagawa H, Makino K, et al.1987. Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product[J]. Journal of Bacteriology, 169(12): 5429-5433.
[46] Jin M-h, Tao J-h, Li Q, et al.2021. Genome editing of the SfABCC2 gene confers resistance to Cry1F toxin from Bacillus thuringiensis in Spodoptera frugiperda[J]. Journal of Integrative Agriculture, 20(3): 815-820.
[47] Jinek M, Chylinski K, Fonfara I, et al.2012. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity[J]. Science, 337(6096): 816-821.
[48] Kim I, Jeong M, Ka D, et al.2018. Solution structure and dynamics of anti-CRISPR AcrIIA4, the Cas9 inhibitor[J]. Scientific Reports, 8(1): 3883.
[49] Kim Y G, Shi Y, Berg J M, et al.1997. Site-specific cleavage of DNA-RNA hybrids by zinc finger/FokI cleavage domain fusions[J]. Gene, 203(1): 43-49.
[50] Kistler K E, Vosshall L B, Matthews B J.2015. Genome engineering with CRISPR-Cas9 in the mosquito Aedes aegypti[J]. Cell Reports, 11(1): 51-60.
[51] Kotwica-Rolinska J, Chodakova L, Chvalova D, et al.2019. CRISPR/Cas9 genome editing introduction and optimization in the non-model insect Pyrrhocoris apterus[J]. Frontiers in Physiology, 10: 891.
[52] Lees R S, Gilles J R L, Hendrichs J, et al.2015. Back to the future: The sterile insect technique against mosquito disease vectors[J]. Current Opinion in Insect Science, 10: 156-162.
[53] Li F, Scott M J.2016. CRISPR/Cas9-mediated mutagenesis of the white and sex lethal loci in the invasive pest, Drosophila suzukii[J]. Biochemical and Biophysical Research Communications, 469(4): 911-916.
[54] Li J, Handler A M.2017. Temperature-dependent sex-reversal by a transformer-2 gene-edited mutation in the spotted wing drosophila, Drosophila suzukii[J]. Scientific Reports, 7(1): 12363.
[55] Li T, Huang S, Zhao X, et al.2011. Modularly assembled designer TAL effector nucleases for targeted gene knockout and gene replacement in eukaryotes[J]. Nucleic Acids Research, 39(14): 6315-6325.
[56] Li X, Fan D, Zhang W, et al.2015. Outbred genome sequencing and CRISPR/Cas9 gene editing in butterflies[J]. Nature Communications, 6: 8212.
[57] Li Y, Zhang J, Chen D, et al.2016. CRISPR/Cas9 in locusts: Successful establishment of an olfactory deficiency line by targeting the mutagenesis of an odorant receptor co-receptor (Orco)[J]. Insect Biochemistry and Molecular Biology, 79: 27-35.
[58] Liu X L, Zhang J, Yan Q, et al.2020.The molecular basis of host selection in a crucifer-specialized moth[J]. Current Biology, 30(22): 4476-4482.
[59] Lotfi M, Rezaei N.2020. CRISPR/Cas13: A potential therapeutic option of COVID-19[J]. Biomedicine & Pharmacotherapy, 131: 110738.
[60] Marraffini L A, Sontheimer E J.2010. Self versus non-self discrimination during CRISPR RNA-directed immunity[J]. Nature, 463(7280): 568-571.
[61] Meccariello A, Tsoumani K T, Gravina A, et al.2020. Targeted somatic mutagenesis through CRISPR/Cas9 ribonucleoprotein complexes in the olive fruit fly, Bactrocera oleae[J]. Archives of Insect Biochemistry and Physiology, 104(2): e21667.
[62] Moscou M J, Bogdanove A J.2009. A simple cipher governs DNA recognition by TAL effectors[J]. Science, 326(5959): 1501.
[63] Port F, Chen H M, Lee T, et al.2014. Optimized CRISPR/Cas tools for efficient germline and somatic genome engineering in Drosophila[J]. Proceedings of the National Academy of Sciences of the USA, 111(29): E2967-2976.
[64] Raban R R, Marshall J M, Akbari O S, et al.2020. Progress towards engineering gene drives for population control[J]. Journal of Experimental Biology, 223(Pt Suppl 1):jeb208181.
[65] Ran F A, Hsu P D, Wright J, et al.2013. Genome engineering using the CRISPR-Cas9 system[J]. Nature Protocols, 8(11): 2281-2308.
[66] Rauch B J, Silvis M R, Hultquist J F, et al.2017. Inhibition of CRISPR-Cas9 with bacteriophage proteins[J]. Cell, 168(1-2): 150-158.
[67] Reding K, Pick L.2020. High-efficiency CRISPR/Cas9 mutagenesis of the white gene in the milkweed bug Oncopeltus fasciatus[J]. Genetics, 215(4): 1027-1037.
[68] Rees H A, Liu D R.2018. Base editing: Precision chemistry on the genome and transcriptome of living cells[J]. Nature Reviews Genetics, 19(12): 770-788.
[69] Sajwan S, Takasu Y, Tamura T, et al.2013. Efficient disruption of endogenous Bombyx gene by TAL effector nucleases[J]. Insect Biochemistry and Molecular Biology, 43(1): 17-23.
[70] Somers J, Nguyen J, Lumb C, et al.2015. In vivo functional analysis of the Drosophila melanogaster nicotinic acetylcholine receptor Dalpha6 using the insecticide spinosad[J]. Insect Biochemistry and Molecular Biology, 64: 116-127.
[71] Sontheimer E J, Davidson A R.2017. Inhibition of CRISPR-Cas systems by mobile genetic elements[J]. Current Opinion in Microbiology, 37: 120-127.
[72] Takasu Y, Kobayashi I, Beumer K, et al.2010. Targeted mutagenesis in the silkworm Bombyx mori using zinc finger nuclease mRNA injection[J]. Insect Biochemistry and Molecular Biology, 40(10): 759-765.
[73] Wang H, Shi Y, Wang L, et al.2018. CYP6AE gene cluster knockout in Helicoverpa armigera reveals role in detoxification of phytochemicals and insecticides[J]. Nature Communications, 9(1): 4820.
[74] Wang J, Zhang H, Wang H, et al.2016. Functional validation of cadherin as a receptor of Bt toxin Cry1Ac in Helicoverpa armigera utilizing the CRISPR/Cas9 system[J]. Insect Biochemistry and Molecular Biology, 76: 11-17.
[75] Wang Y, Huang Y, Xu X, et al.2021. CRISPR/Cas9-based functional analysis of yellow gene in the diamondback moth, Plutella xylostella[J]. Insect Science, 28(5): 1504-1509.
[76] Wang Y, Li Z, Xu J, et al.2013. The CRISPR/Cas system mediates efficient genome engineering in Bombyx mori[J]. Cell Research, 23(12): 1414-1416.
[77] Wei W, Xin H, Roy B, et al.2014. Heritable genome editing with CRISPR/Cas9 in the silkworm, Bombyx mori[J]. Public Library of Science ONE , 9(7): e101210.
[78] Wu K, Shirk P D, Taylor C E, et al.2018. CRISPR/Cas9 mediated knockout of the abdominal-A homeotic gene in fall armyworm moth (Spodoptera frugiperda)[J]. Public Library of Science ONE , 13(12): e0208647.
[79] Xu L, Jiang H-B, Yu J-L, et al.2023. Two odorant receptors regulate 1-octen-3-ol induced oviposition behavior in the oriental fruit fly[J]. Communications Biology, 6(1): 176.
[80] Xu X, Harvey-Samuel T, Yang J, et al.2021. CRISPR/Cas9-based functional characterization of the pigmentation gene ebony in Plutella xylostella[J]. Insect Molecular Biology, 30(6): 615-623.
[81] Xue W H, Xu N, Yuan X B, et al.2018. CRISPR/Cas9-mediated knockout of two eye pigmentation genes in the brown planthopper, Nilaparvata lugens (Hemiptera: Delphacidae)[J]. Insect Biochemistry and Molecular Biology, 93: 19-26.
[82] Yan Y, Ziemek J, Schetelig M F.2020. CRISPR/Cas9 mediated disruption of the white gene leads to pigmentation deficiency and copulation failure in Drosophila suzukii[J]. Journal of Insect Physiology, 126: 104091.
[83] Ye Z F, Liu X L, Han Q, et al.2017. Functional characterization of PBP1 gene in Helicoverpa armigera (Lepidoptera: Noctuidae) by using the CRISPR/Cas9 system[J]. Scientific Reports, 7(1): 8470.
[84] You L, Bi H L, Wang Y H, et al.2019. CRISPR/Cas9-based mutation reveals Argonaute 1 is essential for pigmentation in Ostrinia furnacalis[J]. Insect Science, 26(6): 1020-1028.
[85] Yu Z, Ren M, Wang Z, et al.2013. Highly efficient genome modifications mediated by CRISPR/Cas9 in Drosophila[J]. Genetics, 195(1): 289-291.
[86] Zetsche B, Gootenberg Jonathan S, Abudayyeh Omar O, et al.2015. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system[J]. Cell, 163(3): 759-771.
[87] Zhao S, Xing Z, Liu Z, et al.2019a. Efficient somatic and germline genome engineering of Bactrocera dorsalis by the CRISPR/Cas9 system[J]. Pest Management Science, 75(7): 1921-1932.
[88] Zhao Y, Huang G, Zhang W.2019b. Mutations in NlInR1 affect normal growth and lifespan in the brown planthopper Nilaparvata lugens[J]. Insect Biochemistry and Molecular Biology, 115: 103246.
[89] Zhu G H, Chereddy S, Howell J L, et al.2020. Genome editing in the fall armyworm, Spodoptera frugiperda: Multiple sgRNA/Cas9 method for identification of knockouts in one generation[J]. Insect Biochemistry and Molecular Biology, 122: 103373.
[90] Zhu G H, Peng Y C, Zheng M Y, et al.2017. CRISPR/Cas9 mediated BLOS2 knockout resulting in disappearance of yellow strips and white spots on the larval integument in Spodoptera litura[J]. Journal of Insect Physiology, 103: 29-35.
[91] Zhu G H, Xu J, Cui Z, et al.2016. Functional characterization of SlitPBP3 in Spodoptera litura by CRISPR/Cas9 mediated genome editing[J]. Insect Biochemistry and Molecular Biology, 75: 1-9.
[92] Zhu G H, Zheng M Y, Sun J B, et al.2019. CRISPR/Cas9 mediated gene knockout reveals a more important role of PBP1 than PBP2 in the perception of female sex pheromone components in Spodoptera litura[J]. Insect Biochemistry and Molecular Biology, 115: 103244.
[93] Zimmer C T, Garrood W T, Puinean A M, et al.2016. A CRISPR/Cas9 mediated point mutation in the alpha 6 subunit of the nicotinic acetylcholine receptor confers resistance to spinosad in Drosophila melanogaster[J]. Insect Biochemistry and Molecular Biology, 73: 62-69.
[94] Zuo Y, Wang H, Xu Y, et al.2017. CRISPR/Cas9 mediated G4946E substitution in the ryanodine receptor of Spodoptera exigua confers high levels of resistance to diamide insecticides[J]. Insect Biochemistry and Molecular Biology, 89: 79-85. |
|
|
|
