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Applications of gene drive systems for population suppression of insect pests

Published online by Cambridge University Press:  31 August 2022

Muhammad Asad Open the ORCID record for Muhammad Asad [Opens in a new window] ,
Dan Liu ,
Jing Chen  and
Guang Yang
Muhammad Asad
Affiliation:
State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Institute of Applied Ecology, Fujian Agriculture and Forestry University, Fuzhou 350002, China Joint International Research Laboratory of Ecological Pest Control, Ministry of Education, Fuzhou 350002, China Key Laboratory of Integrated Pest Management for Fujian-Taiwan Crops, Ministry of Agriculture, Fuzhou 350002, China Key Laboratory of Green Pest Control, Fujian Province University, Fuzhou 350002, China
Dan Liu
Affiliation:
State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Institute of Applied Ecology, Fujian Agriculture and Forestry University, Fuzhou 350002, China Joint International Research Laboratory of Ecological Pest Control, Ministry of Education, Fuzhou 350002, China Key Laboratory of Integrated Pest Management for Fujian-Taiwan Crops, Ministry of Agriculture, Fuzhou 350002, China Key Laboratory of Green Pest Control, Fujian Province University, Fuzhou 350002, China
Jing Chen
Affiliation:
State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Institute of Applied Ecology, Fujian Agriculture and Forestry University, Fuzhou 350002, China Joint International Research Laboratory of Ecological Pest Control, Ministry of Education, Fuzhou 350002, China Key Laboratory of Integrated Pest Management for Fujian-Taiwan Crops, Ministry of Agriculture, Fuzhou 350002, China Key Laboratory of Green Pest Control, Fujian Province University, Fuzhou 350002, China
Guang Yang*
Affiliation:
State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Institute of Applied Ecology, Fujian Agriculture and Forestry University, Fuzhou 350002, China Joint International Research Laboratory of Ecological Pest Control, Ministry of Education, Fuzhou 350002, China Key Laboratory of Integrated Pest Management for Fujian-Taiwan Crops, Ministry of Agriculture, Fuzhou 350002, China Key Laboratory of Green Pest Control, Fujian Province University, Fuzhou 350002, China Ministerial and Provincial Joint Innovation Centre for Safety Production of Cross-Strait Crops, Fujian Agriculture and Forestry University, Fuzhou 350002, China
*
Author for correspondence: Guang Yang, Email: yxg@fafu.edu.cn
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Abstract

Population suppression is an effective way for controlling insect pests and disease vectors, which cause significant damage to crop and spread contagious diseases to plants, animals and humans. Gene drive systems provide innovative opportunities for the insect pests population suppression by driving genes that impart fitness costs on populations of pests or disease vectors. Different gene-drive systems have been developed in insects and applied for their population suppression. Here, different categories of gene drives such as meiotic drive (MD), under-dominance (UD), homing endonuclease-based gene drive (HEGD) and especially the CRISPR/Cas9-based gene drive (CCGD) were reviewed, including the history, types, process and mechanisms. Furthermore, the advantages and limitations of applying different gene-drive systems to suppress the insect population were also summarized. This review provides a foundation for developing a specific gene-drive system for insect population suppression.

Keywords

CRISPR/Cas9-based gene driveengineered under-dominancehoming endonuclease-based gene drivemeiotic drive
Type
Review Article
Information
Bulletin of Entomological Research , Volume 112 , Issue 6 , December 2022 , pp. 724 - 733
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Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Adelman, ZN, Jasinskiene, N, Onal, S, Juhn, J, Ashikyan, A, Salampessy, M, MacCauley, T and James, AA (2007) Nanos gene control DNA mediates developmentally regulated transposition in the yellow fever mosquito Aedes aegypti. Proceedings of the National Academy of Sciences 104, 9970–9975.CrossRefGoogle ScholarPubMed
Akbari, OS, Matzen, KD, Marshall, JM, Huang, H, Ward, CM and Hay, BA (2013) A synthetic gene drive system for local, reversible modification and suppression of insect populations. Current Biology 23, 671–677.CrossRefGoogle ScholarPubMed
Alphey, L, Nimmo, D, O'Connell, S and Alphey, N (2008) Insect population suppression using engineered insects. In Aksoy, S (ed.), Transgenesis and the Management of Vector-Borne Disease. Advances in Experimental Medicine and Biology, Vol. 627. New York, NY: Springer, pp. 93–103.Google Scholar
Alphey, L, McKemey, A, Nimmo, D, Neira Oviedo, M, Lacroix, R, Matzen, K and Beech, C (2013) Genetic control of Aedes mosquitoes. Pathogens and Global Health 107, 170–179.CrossRefGoogle ScholarPubMed
Asad, M, Liu, D, Li, J, Chen, J and Yang, G (2022) Development of CRISPR/Cas9-mediated gene-drive construct targeting the phenotypic gene in Plutella xylostella. Frontiers in Physiology 13, 938621. doi:10.3389/fphys.2022.938621CrossRefGoogle ScholarPubMed
Asad, M, Munir, F, Xu, X, Li, M, Jiang, Y, Chu, L and Yang, G (2020) Functional characterization of the cis-regulatory region for the vitellogenin gene in Plutella xylostella. Insect Molecular Biology 29, 137–147.CrossRefGoogle ScholarPubMed
Basu, S, Aryan, A, Overcash, JM, Samuel, GH, Anderson, MA, Dahlem, TJ, Myles, KM and Adelman, ZN (2015) Silencing of end-joining repair for efficient site-specific gene insertion after TALEN/CRISPR mutagenesis in Aedes aegypti. Proceedings of the National Academy of Sciences 112, 4038–4043.CrossRefGoogle ScholarPubMed
Benedict, MQ (2014) Transgenic Insects: Techniques and Applications. British Library, London, UK: CABI.CrossRefGoogle Scholar
Boete, C and Koella, JC (2003) Evolutionary ideas about genetically manipulated mosquitoes and malaria control. Trends in Parasitology 19, 32–38.CrossRefGoogle ScholarPubMed
Branco, A, Tao, Y, Hartl, DL and Lemos, B (2013) Natural variation of the Y chromosome suppresses sex ratio distortion and modulates testis-specific gene expression in Drosophila simulans. Heredity 111, 8.CrossRefGoogle Scholar
Burt, A (2003) Site-specific selfish genes as tools for the control and genetic engineering of natural populations. Proceedings of the Royal Society B: Biological Sciences 270, 921–928.CrossRefGoogle ScholarPubMed
Burt, A (2014) Heritable strategies for controlling insect vectors of disease. Philosophical Transactions Royal Society B: Biological Sciences 369, 20130432.CrossRefGoogle ScholarPubMed
Champer, J, Buchman, A and Akbari, OS (2016) Cheating evolution: engineering gene drives to manipulate the fate of wild populations. Nature Reviews Genetics 17, 146.CrossRefGoogle ScholarPubMed
Champer, J, Zhao, J, Champer, S, Liu, J and Messer, PW (2020) Population dynamics of underdominance gene drive systems in continuous space. ACS Synthetic Biology 9(4), 779–792.CrossRefGoogle ScholarPubMed
Chan, Y-S, Naujoks, DA, Huen, DS and Russell, S (2011) Insect population control by homing endonuclease-based gene drive: an evaluation in Drosophila melanogaster. Genetics 188, 33–44.CrossRefGoogle ScholarPubMed
Chan, Y-S, Huen, DS, Glauert, R, Whiteway, E and Russell, S (2013 a) Optimising homing endonuclease gene drive performance in a semi-refractory species: the Drosophila melanogaster experience. PLoS One 8, e54130.CrossRefGoogle Scholar
Chan, Y-S, Takeuchi, R, Jarjour, J, Huen, DS, Stoddard, BL and Russell, S (2013 b) The design and in vivo evaluation of engineered I-OnuI-based enzymes for HEG gene drive. PLoS One 8, e74254.CrossRefGoogle ScholarPubMed
Craig, G, Hickey, W and VandeHey, R (1960) An inherited male-producing factor in Aedes aegypti. Science (New York, N.Y.) 132, 1887–1889.CrossRefGoogle ScholarPubMed
Curtis, C (1968) Possible use of translocations to fix desirable genes in insect pest populations. Nature 218, 360–368.CrossRefGoogle ScholarPubMed
Davis, S, Bax, N and Grewe, P (2001) Engineered underdominance allows efficient and economical introgression of traits into pest populations. Journal of Theoretical Biology 212, 83–98.CrossRefGoogle ScholarPubMed
Deredec, A, Burt, A and Godfray, HCJ (2008) The population genetics of using homing endonuclease genes in vector and pest management. Genetics 179, 2013–2026.CrossRefGoogle ScholarPubMed
Deredec, A, Godfray, HCJ and Burt, A (2011) Requirements for effective malaria control with homing endonuclease genes. Proceedings of the National Academy of Sciences 108, E874–E880.CrossRefGoogle ScholarPubMed
Dhole, S, Vella, MR, Lloyd, AL and Gould, F (2018) Invasion and migration of spatially self-limiting gene drives: a comparative analysis. Evolutionary Applications 11, 794–808.CrossRefGoogle ScholarPubMed
Dhole, S, Lloyd, AL and Gould, F (2019) Tethered homing gene drives: a new design for spatially restricted population replacement and suppression. Evolutionary Applications 12, 1688–1702.CrossRefGoogle Scholar
Drury, DW, Dapper, AL, Siniard, DJ, Zentner, GE and Wade, MJ (2017) CRISPR/Cas9 gene drives in genetically variable and nonrandomly mating wild populations. Science Advances 3, e1601910.CrossRefGoogle ScholarPubMed
Edgington, MP and Alphey, LS (2017) Conditions for success of engineered underdominance gene drive systems. Journal of Theoretical Biology 430, 128–140.CrossRefGoogle ScholarPubMed
Eppstein, MJ, Payne, JL and Goodnight, CJ (2009) Underdominance, multiscale interactions, and self-organizing barriers to gene flow. Journal of Artificial Evolution and Applications 2009, 5.CrossRefGoogle Scholar
Fu, Y, Sander, JD, Reyon, D, Cascio, VM and Joung, JK (2014) Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nature Biotechnology 32, 279–284.CrossRefGoogle ScholarPubMed
Galizi, R, Doyle, LA, Menichelli, M, Bernardini, F, Deredec, A, Burt, A, Stoddard, BL, Windbichler, N and Crisanti, A (2014) A synthetic sex ratio distortion system for the control of the human malaria mosquito. Nature Communications 5, 3977–3982.CrossRefGoogle ScholarPubMed
Gantz, VM and Bier, E (2015) The mutagenic chain reaction: a method for converting heterozygous to homozygous mutations. Science (New York, N.Y.) 348, 442–444.CrossRefGoogle ScholarPubMed
Gantz, VM, Jasinskiene, N, Tatarenkova, O, Fazekas, A, Macias, VM, Bier, E and James, AA (2015) Highly efficient Cas9-mediated gene drive for population modification of the malaria vector mosquito Anopheles stephensi. Proceedings of the National Academy of Sciences 112, E6736–E6743.CrossRefGoogle ScholarPubMed
Godfray, HCJ, North, A and Burt, A (2017) How driving endonuclease genes can be used to combat pests and disease vectors. BMC Biology 15, 1–12.CrossRefGoogle ScholarPubMed
Hamilton, WD (1967) Extraordinary sex ratios. Science (New York, N.Y.) 156, 477–488.CrossRefGoogle ScholarPubMed
Hammond, A, Galizi, R, Kyrou, K, Simoni, A, Siniscalchi, C, Katsanos, D, Gribble, M, Baker, D, Marois, E and Russell, S (2016) A CRISPR-Cas9 gene drive system targeting female reproduction in the malaria mosquito vector Anopheles gambiae. Nature Biotechnology 34, 78–83.CrossRefGoogle ScholarPubMed
Hartl, DL, Clark, AG and Clark, AG (1997) Principles of Population Genetics. Sunderland: Sinauer Associates.Google Scholar
Helleu, Q, Gérard, PR and Montchamp-Moreau, C (2015) Sex chromosome drive. Cold Spring Harbor Perspectives in Biology 7, a017616.CrossRefGoogle Scholar
Helleu, Q, Gerard, PR, Dubruille, R, Ogereau, D, Homme, BP, Loppin, B and Montchampmoreau, C (2016) Rapid evolution of a Y-chromosome heterochromatin protein underlies sex chromosome meiotic drive. Proceedings of the National Academy of Sciences of the United States of America 113, 4110–4115.CrossRefGoogle ScholarPubMed
Hickey, WA and Craig, GB (1966) Genetic distortion of sex ratio in a mosquito, Aedes aegypti. Genetics 53, 1177–1196.CrossRefGoogle Scholar
James, AA (2005) Gene drive systems in mosquitoes: rules of the road. Trends in Parasitology 21, 64–67.CrossRefGoogle ScholarPubMed
Jinek, M, Chylinski, K, Fonfara, I, Hauer, M, Doudna, JA and Charpentier, E (2012) A programmable dual-RNA–guided DNA endonuclease in adaptive bacterial immunity. Science (New York, N.Y.) 337, 816–821.CrossRefGoogle ScholarPubMed
KaramiNejadRanjbar, M, Eckermann, KN, Ahmed, HM, Dippel, S, Marshall, JM and Wimmer, EA (2018) Consequences of resistance evolution in a Cas9-based sex-conversion suppression gene drive for insect pest management. Proceedings of the National Academy of Sciences 115, 6189–6194.Google Scholar
Keais, G, Hanson, M, Gowen, B and Perlman, S (2017) X chromosome drive in a widespread Palearctic woodland fly, Drosophila testacea. Journal of Evolutionary Biology 30, 1185–1194.CrossRefGoogle Scholar
Kidwell, M and Ribeiro, J (1992) Can transposable elements be used to drive disease refractoriness genes into vector populations? Parasitology Today 8, 325–329.CrossRefGoogle ScholarPubMed
Kondo, S and Ueda, R (2013) Highly improved gene targeting by germline-specific Cas9 expression in Drosophila. Genetics 195, 715–721.CrossRefGoogle ScholarPubMed
Kyrou, K, Hammond, AM, Galizi, R, Kranjc, N, Burt, A, Beaghton, AK, Nolan, T and Crisanti, A (2018) A CRISPR–Cas9 gene drive targeting doublesex causes complete population suppression in caged Anopheles gambiae mosquitoes. Nature Biotechnology 36, 1062–1066.CrossRefGoogle ScholarPubMed
Letourneau, DK and Burrows, BE (2001) Genetically Engineered Organisms: Assessing Environmental and Human Health Effects. Boca Raton: CRC press.CrossRefGoogle Scholar
Li, J, Shou, J, Guo, Y, Tang, Y, Wu, Y, Jia, Z, Zhai, Y, Chen, Z, Xu, Q and Wu, Q (2015) Efficient inversions and duplications of mammalian regulatory DNA elements and gene clusters by CRISPR/Cas9. Journal of Molecular Cell Biology 7, 284–298.CrossRefGoogle ScholarPubMed
Lindholm, AK, Dyer, KA, Firman, RC, Fishman, L, Forstmeier, W, Holman, L, Johannesson, H, Knief, U, Kokko, H and Larracuente, AM (2016) The ecology and evolutionary dynamics of meiotic drive. Trends in Ecology & Evolution 31, 315–326.CrossRefGoogle ScholarPubMed
Lyttle, TW (1977) Experimental population genetics of meiotic drive systems I. Pseudo-Y chromosomal drive as a means of eliminating cage populations of Drosophila melanogaster. Genetics 86, 413–445.CrossRefGoogle ScholarPubMed
Ma, S, Chang, J, Wang, X, Liu, Y, Zhang, J, Lu, W, Gao, J, Shi, R, Zhao, P and Xia, Q (2014) CRISPR/Cas9 mediated multiplex genome editing and heritable mutagenesis of BmKu70 in Bombyx mori. Scientific Reports 4, 4489.CrossRefGoogle ScholarPubMed
Magori, K and Gould, F (2006) Genetically engineered underdominance for manipulation of pest populations: a deterministic model. Genetics 172, 2613–2620.CrossRefGoogle ScholarPubMed
Mali, P, Yang, L, Esvelt, KM, Aach, J, Guell, M, DiCarlo, JE, Norville, JE and Church, GM (2013) RNA-guided human genome engineering via Cas9. Science (New York, N.Y.) 339, 823–826.CrossRefGoogle ScholarPubMed
Marshall, JM and Akbari, OS (2016) Gene drive strategies for population replacement. In Adelman, ZN (ed.), Genetic Control of Malaria and Dengue. Boston: Academic Press, pp. 169–200.CrossRefGoogle Scholar
Marshall, JM and Hay, BA (2012) Confinement of gene drive systems to local populations: a comparative analysis. Journal of Theoretical Biology 294, 153–171.CrossRefGoogle ScholarPubMed
McFarlane, GR, Whitelaw, CBA and Lillico, SG (2018) CRISPR-based gene drives for pest control. Trends Biotechnology 36, 130–133.CrossRefGoogle ScholarPubMed
Mori, A, Chadee, DD, Graham, DH and Severson, DW (2004) Reinvestigation of an endogenous meiotic drive system in the mosquito, Aedes aegypti (Diptera: Culicidae). Journal of Medical Entomology 41, 1027–1033.CrossRefGoogle ScholarPubMed
Pavlovic, G, Erbs, V, Andre, P, Sylvie, J, Eisenman, B, Dreyer, D, Lorentz, R, Wattenhofer-Donze, M, Birling, M-C and Herault, Y (2016) Generation of targeted overexpressing models by CRISPR/Cas9 and need of careful validation of your knock-in line obtained by nuclease genome editing. Transgenic Research 25, 254–265.Google Scholar
Pieper, KE and Dyer, KA (2016) Occasional recombination of a selfish X-chromosome may permit its persistence at high frequencies in the wild. Journal of Evolutionary Biology 29, 2229–2241.CrossRefGoogle ScholarPubMed
Preston, CR, Flores, CC and Engels, WR (2006) Differential usage of alternative pathways of double-strand break repair in Drosophila. Genetics 172, 1055–1068.CrossRefGoogle ScholarPubMed
Reeves, RG, Bryk, J, Altrock, PM, Denton, JA and Reed, FA (2014) First steps towards underdominant genetic transformation of insect populations. PLoS One 9, e97557.CrossRefGoogle ScholarPubMed
Ren, X, Sun, J, Housden, BE, Hu, Y, Roesel, C, Lin, S, Liu, L-P, Yang, Z, Mao, D and Sun, L (2013) Optimized gene editing technology for Drosophila melanogaster using germ line-specific Cas9. Proceedings of the National Academy of Sciences 110, 19012–19017.CrossRefGoogle ScholarPubMed
Rode, NO, Estoup, A, Bourguet, D, Courtier-Orgogozo, V and Débarre, F (2019) Population management using gene drive: molecular design, models of spread dynamics and assessment of ecological risks. Conservation Genetics 20, 671–690.CrossRefGoogle Scholar
Rutkowska, J and Badyaev, AV (2008) Meiotic drive and sex determination: molecular and cytological mechanisms of sex ratio adjustment in birds. Philosophical Transactions of the Royal Society of London B: Biological Sciences 363, 1675–1686.CrossRefGoogle ScholarPubMed
Sinkins, SP and Gould, F (2006) Gene drive systems for insect disease vectors. Nature Reviews Genetics 7, 427–433.CrossRefGoogle ScholarPubMed
Stoddard, BL (2005) Homing endonuclease structure and function. Quarterly Reviews of Biophysics 38, 49–95.CrossRefGoogle Scholar
Stoddard, BL (2011) Homing endonucleases: from microbial genetic invaders to reagents for targeted DNA modification. Structure (London, England: 1993) 19, 7–15.CrossRefGoogle ScholarPubMed
Unckless, RL, Larracuente, AM and Clark, AG (2015) Sex-ratio meiotic drive and Y-linked resistance in Drosophila affinis. Genetics 199, 831–840.CrossRefGoogle ScholarPubMed
Williams, AE, Franz, AWE, Reid, WR and Olson, KE (2020) Antiviral effectors and gene drive strategies for mosquito population suppression or replacement to mitigate arbovirus transmission by Aedes aegypti. Insects 11, 52.CrossRefGoogle ScholarPubMed
Windbichler, N, Papathanos, PA, Catteruccia, F, Ranson, H, Burt, A and Crisanti, A (2007) Homing endonuclease mediated gene targeting in Anopheles gambiae cells and embryos. Nucleic Acids Research 35, 5922–5933.CrossRefGoogle ScholarPubMed
Windbichler, N, Menichelli, M, Papathanos, PA, Thyme, SB, Li, H, Ulge, UY, Hovde, BT, Baker, D, Monnat, RJ and Burt, A (2011) A synthetic homing endonuclease-based gene drive system in the human malaria mosquito. Nature 473, 212–216.CrossRefGoogle ScholarPubMed
Wood, RJ and Newton, ME (1991) Sex-ratio distortion caused by meiotic drive in mosquitoes. The American Naturalist 137, 379–391.CrossRefGoogle Scholar
Xu, J, Xu, X, Zhan, S and Huang, Y (2019) Genome editing in insects: current status and challenges. National Science Review 6, 399–401.CrossRefGoogle ScholarPubMed