CRISPR-based genetic control strategies for insect pests

doi:10.1016/j.jia.2022.11.003

摘要/Abstract

Abstract:

Genetic control strategies such as the sterile insect technique have successfully fought insect pests worldwide. The CRISPR (clustered regularly interspaced short palindromic repeats) technology, together with high-quality genomic resources obtained in more and more species, greatly facilitates the development of novel genetic control insect strains that can be used in area-wide and species-specific pest control programs. Here, we review the research progress towards state-of-art CRISPR-based genetic control strategies, including gene drive, sex ratio distortion, CRISPR-engineered genetic sexing strains, and precision-guided sterile insect technique. These strategies’ working mechanisms, potential resistance development mechanisms, and regulations are illustrated and discussed. In addition, recent developments such as stacked and conditional systems are introduced. We envision that the advances in genetic technology will continue to be one of the driving forces for developing the next generation of pest control strategies.

Key words: insect pest , genetic control , sterile insect technique , gene drive , genetic sexing strains , CRISPR-Cas9

Ying YAN, Roswitha A. AUMANN, Irina HÄCKER, Marc F. SCHETELIG. [J]. Journal of Integrative Agriculture, 2023, 22(3): 651-668.

Ying YAN, Roswitha A. AUMANN, Irina HÄCKER, Marc F. SCHETELIG. CRISPR-based genetic control strategies for insect pests[J]. Journal of Integrative Agriculture, 2023, 22(3): 651-668.

参考文献

Akbari O S, Bellen H J, Bier E, Bullock S L, Burt A, Church G M, Cook K R, Duchek P, Edwards O R, Esvelt K M, Gantz V M, Golic K G, Gratz S J, Harrison M M, Hayes K R, James A A, Kaufman T C, Knoblich J, Malik H S, Matthews K A, et al. 2015. Safeguarding gene drive experiments in the laboratory. Science, 349, 927–929.
Akbari O S, Chen C H, Marshall J M, Huang H X, Antoshechkin I, Hay B A. 2014. Novel synthetic Medea selfish genetic elements drive population replacement in Drosophila; a theoretical exploration of Medea-dependent population suppression. ACS Synthetic Biology, 3, 915–928.
Akbari O S, Matzen K D, Marshall J M, Huang H X, Ward C M, Hay B A. 2013. A synthetic gene drive system for local, reversible modification and suppression of insect populations. Current Biology, 23, 671–677.
Aketarawong N, Isasawin S, Laohakieat K, Thanaphum S. 2020. Genetic stability, genetic variation, and fitness performance of the genetic sexing Salaya1 strain for Bactrocera dorsalis, under long-term mass rearing conditions. BMC Genetics, 21, 131.
Alphey N, Bonsall M B. 2018. Genetics-based methods for agricultural insect pest management. Agricultural and Forest Entomology, 20, 131–140.
Alphey N, Bonsall M B, Alphey L. 2011. Modeling resistance to genetic control of insects. Journal of Theoretical Biology, 270, 42–55.
Altrock P M, Traulsen A, Reeves R G, Reed F A. 2010. Using underdominance to bi-stably transform local populations. Journal of Theoretical Biology, 267, 62–75.
Amrein H, Maniatis T, Nothiger R. 1990. Alternatively spliced transcripts of the sex-determining gene tra-2 of Drosophila encode functional proteins of different size. EMBO Journal, 9, 3619–3629.
Augustinos A A, Misbah-ul-Haq M, Carvalho D O, de la Fuente L D, Koskinioti P, Bourtzis K. 2020. Irradiation induced inversions suppress recombination between the M locus and morphological markers in Aedes aegypti. BMC Genetics, 21(Suppl. 2), 142.
Aumann R A, Hacker I, Schetelig M F. 2020. Female-to-male sex conversion in Ceratitis capitata by CRISPR/Cas9 HDR-induced point mutations in the sex determination gene transformer-2. Scientific Reports, 10, 18611.
Beeman R W, Friesen K S. 1999. Properties and natural occurrence of maternal-effect selfish genes (‘Medea’ factors) in the Red Flour Beetle, Tribolium castaneum. Heredity, 82, 529–534.
Beeman R W, Friesen K S, Denell R E. 1992. Maternal-effect selfish genes in flour beetles. Science, 256, 89–92.
Belfort M, Perlman P S. 1995. Mechanisms of intron mobility. Journal of Biological Chemistry, 270, 30237–30240.
Bier E. 2022. Gene drives gaining speed. Nature Reviews, 23, 5–22.
Bonner M R, Alavanja M C R. 2017. Pesticides, human health, and food security. Food and Energy Security, 6, 89–93.
Brunet E, Jasin M. 2018. Induction of chromosomal translocations with CRISPR-Cas9 and other nucleases: understanding the repair mechanisms that give rise to translocations. Advances in Experimental Medicine and Biology, 1044, 15–25.
Buchman A, Marshall J M, Ostrovski D, Yang T, Akbari O S. 2018. Synthetically engineered Medea gene drive system in the worldwide crop pest Drosophila suzukii. Proceedings of the National Academy of Sciences of the United States of America, 115, 4725–4730.
Burt A, Deredec A. 2018. Self-limiting population genetic control with sex-linked genome editors. Proceedings of the Royal Society (B: Biological Sciences), 285, 20180776.
Cannon P M, Kiem H P. 2021. The genome-editing decade. Molecular Therapy, 29, 3093–3094.
Carrami E M, Eckermann K N E, Ahmed H M M, Sanchez C H, Dippel S, Marshalld J M, Wimmer E A. 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 od the United States of America, 115, 6189–6194.
Champer J, Buchman A, Akbari O S. 2016. Cheating evolution: engineering gene drives to manipulate the fate of wild populations. Nature Reviews, 17, 146–159.
Champer J, Champer S E, Kim I K, Clark A G, Messer P W. 2021. Design and analysis of CRISPR-based underdominance toxin-antidote gene drives. Evolutionary Applications, 14, 1052–1069.
Champer J, Lee E, Yang E, Liu C, Clark A G, Messer P W. 2020a. A toxin-antidote CRISPR gene drive system for regional population modification. Nature Communications, 11, 1082.
Champer J, Liu J, Oh S Y, Reeves R, Luthra A, Oakes N, Clark A G, Messer P W. 2018. Reducing resistance allele formation in CRISPR gene drive. Proceedings of the National Academy of Sciences of the United States of America, 115, 5522–5527.
Champer J, Zhao J, Champer S E, Liu J, Messer P W. 2020b. Population dynamics of underdominance gene drive systems in continuous space. ACS Synthetic Biology, 9, 779–792.
Chen C H, Huang H X, Ward C M, Su J T, Schaeffer L V, Guo M, Hay B A. 2007. A synthetic maternal-effect selfish genetic element drives population replacement in Drosophila. Science, 316, 597–600.
Chen C J, Compton A, Nikolouli K, Wang A, Aryan A, Sharma A, Qi Y, Dellinger C, Hempel M, Potters M, Augustinos A, Severson D W, Bourtzis K, Tu Z J. 2022. Marker-assisted mapping enables forward genetic analysis in Aedes aegypti, an arboviral vector with vast recombination deserts, Genetics, doi: 10.1093/genetics/iyac140.
Chen X Y, Li M, Feng X Z, Guang S H. 2015. Targeted chromosomal translocations and essential gene knockout using CRISPR/Cas9 technology in Caenorhabditis elegans. Genetics, 201, 1295–1306.
Cline T W. 1978. Two closely linked mutations in Drosophila melanogaster that are lethal to opposite sexes and interact with daughterless. Genetics, 90, 683–698.
Cline T W. 1993. The Drosophila sex determination signal - how do flies count to two. Trends in Genetics, 9, 385–390.
Cockburn A F, Howells A J, Whitten M J. 1984. Recombinant DNA technology and genetic-control of pest insects. Biotechnology & Genetic Engineering Reviews, 2, 69–99.
Craig Jr G B, Hickey W A, Vandehey R C. 1960. An inherited male-producing factor in Aedes aegypti. Science, 132, 1887–1889.
Curtis C F. 1968. Possible use of translocations to fix desirable genes in insect pest populations. Nature, 218, 368–369.
Curtis C F. 1985. Genetic-control of insect pests - growth industry or lead balloon. Biological Journal of the Linnean Society, 26, 359–374.
Deltcheva E, Chylinski K, Sharma C M, Gonzales K, Chao Y, Pirzada Z A, Eckert M R, Vogel J, Charpentier E. 2011. CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature, 471, 602–607.
Deutsch C A, Tewksbury J J, Tigchelaar M, Battisti D S, Merrill S C, Huey R B, Naylor R L. 2018. Increase in crop losses to insect pests in a warming climate. Science, 361, 916–919.
Devos Y, Mumford J D, Bonsall M B, Camargo A M, Firbank L G, Glandorf D C M, Nogue F, Paraskevopoulos K, Wimmer E A. 2022. Potential use of gene drive modified insects against disease vectors, agricultural pests and invasive species poses new challenges for risk assessment. Critical Reviews in Biotechnology, 42, 254–270.
Dias V S, Caceres C, Parker A G, Pereira R, Demirbas-Uzel G, Abd-Alla A M M, Teets N M, Schetelig M F, Handler A M, Hahn D A. 2021. Mitochondrial superoxide dismutase overexpression and low oxygen conditioning hormesis improve the performance of irradiated sterile males. Scientific Reports, 11, 20182.
Doudna J A, Charpentier E. 2014. The new frontier of genome engineering with CRISPR-Cas9. Science, 346, 1258096.
Drury D W, Dapper A L, Siniard D J, Zentner G E, Wade M J. 2017. CRISPR/Cas9 gene drives in genetically variable and nonrandomly mating wild populations. Science Advances, 3, e1601910.
Eckermann K N, Dippel S, Carrami E M, Ahmed H M, Curril I M, Wimmer E A. 2014. Perspective on the combined use of an independent transgenic sexing and a multifactorial reproductive sterility system to avoid resistance development against transgenic sterile insect technique approaches. BMC Genetics, 15, S17.
Fackenthal J D, Hutchens J A, Turner F R, Raff E C. 1995. Structural analysis of mutations in the Drosophila beta 2-tubulin isoform reveals regions in the beta-tubulin molecular required for general and for tissue-specific microtubule functions. Genetics, 139, 267–286.
Fasulo B, Meccariello A, Morgan M, Borufka C, Papathanos P A, Windbichler N. 2020. A fly model establishes distinct mechanisms for synthetic CRISPR/Cas9 sex distorters. PLoS Genetics, 16, e1008647.
Flick K E, Jurica M S, Monnat Jr R J, Stoddard B L. 1998. DNA binding and cleavage by the nuclear intron-encoded homing endonuclease I-PpoI. Nature, 394, 96–101.
Franz G. 2005. Genetic sexing strains in Mediterranean fruit fly, an example for other species amenable to large-scale rearing for the sterile insect technique. In: Dyck V A, Hendrichs J A R, eds., Sterile Insect Technique. Springer, Dordrecht. pp. 428–449.
Franz G, Bourtzis K, Cáceres C. 2021. Practical and operational genetic sexing systems based on classical genetic approaches in fruit flies, an example for other species amenable to large-scale rearing for the sterile insect technique. In: Dyck V A, Hendrichs J, Robinson A S, eds., Sterile Insect Technique Principles and Practice in Area-Wide Integrated Pest Management. CRC Press, Boca Raton, Florida, USA. pp. 575–604.
Franz G, Gencheva E, Kerremans P. 1994. Improved stability of genetic sex-separation strains for the Mediterranean fruit fly, Ceratitis capitata. Genome, 37, 72–82.
Galizi R, Doyle L A, Menichelli M, Bernardini F, Deredec A, Burt A, Stoddard B L, Windbichler N, Crisanti A. 2014. A synthetic sex ratio distortion system for the control of the human malaria mosquito. Nature Communications, 5, 3977.
Galizi R, Hammond A, Kyrou K, Taxiarchi C, Bernardini F, O’Loughlin S M, Papathanos P A, Nolan T, Windbichler N, Crisanti A. 2016. A CRISPR-Cas9 sex-ratio distortion system for genetic control. Scientific Reports, 6, 31139.
Gamez S, Vesga L C, Mendez-Sanchez S C, Akbari O S. 2021. Spatial control of gene expression in flies using bacterially derived binary transactivation systems. Insect Molecular Biology, 30, 461–471.
Gantz V M, Bier E. 2015. The mutagenic chain reaction: A method for converting heterozygous to homozygous mutations. Science. 348, 442–444.
Gantz V M, Jasinskiene N, Tatarenkova O, Fazekas A, Macias V M, Bier E, James A A. 2015. Highly efficient Cas9-mediated gene drive for population modification of the malaria vector mosquito Anopheles stephensi. Proceedings of the National Academy of Sciences of the United States of America, 112, E6736–E6743.
Gimble F S. 2000. Invasion of a multitude of genetic niches by mobile endonuclease genes. FEMS Microbiology Letters, 185, 99–107.
Gould F, Schliekelman P. 2004. Population genetics of autocidal control and strain replacement. Annual Review of Entomology, 49, 193–217.
Gutzmann N, Elsensohn J E, Barnes J C, Baltzegar J, Jones M S, Sudweeks J. 2017. CRISPR-based gene drive in agriculture will face technical and governance challenges. EMBO Reports, 18, 1479–1480.
Häcker I, Bourtzis K, Schetelig M F. 2021. Applying modern molecular technologies in support of the sterile insect technique. In: Dyck V A, Hendrichs J, Robinson A S, eds., Sterile Insect Technique. Principles and Practice in Area-Wide Integrated Pest Management. CRC Press, Boca Raton, Florida, USA. pp. 657–702.
Hammond A, Galizi R, Kyrou K, Simoni A, Siniscalchi C, Katsanos D, Gribble M, Baker D, Marois E, Russell S, Burt A, Windbichler N, Crisanti A, Nolan T. 2016. A CRISPR-Cas9 gene drive system targeting female reproduction in the malaria mosquito vector Anopheles gambiae. Nature Biotechnology, 34, 78–83.
Hammond A M, Kyrou K, Bruttini M, North A, Galizi R, Karlsson X, Kranjc N, Carpi F M, D’Aurizio R, Crisanti A, Nolan T. 2017. The creation and selection of mutations resistant to a gene drive over multiple generations in the malaria mosquito. PLoS Genetics, 13, e1007039.
Handler A. 2016. Enhancing the stability and ecological safety of mass-reared transgenic strains for field release by redundant conditional lethality systems. Insect Science, 23, 225–234.
Harvey-Samuel T, Ant T, Alphey L. 2017. Towards the genetic control of invasive species. Biological Invasions, 19, 1683–1703.
Hay B A, Oberhofer G, Guo M. 2021. Engineering the composition and fate of wild populations with gene drive. Annual Review of Entomology, 66, 407–434.
Hickey W A, Craig Jr G B. 1966. Genetic distortion of sex ratio in a mosquito, Aedes Aegypti. Genetics, 53, 1177–1196.
Holman L. 2019. Evolutionary simulations of Z-linked suppression gene drives. Proceedings of the Royal Society (B: Biological Sciences), 286, 20191070.
Horvath P, Barrangou R. 2010. CRISPR/Cas, the immune system of bacteria and archaea. Science, 327, 167–170.
Hsu P D, Lander E S, Zhang F. 2014. Development and applications of CRISPR-Cas9 for genome engineering. Cell, 157, 1262–1278.
Iwata S, Yoshina S, Suehiro Y, Hori S, Mitani S. 2016. Engineering new balancer chromosomes in C. elegans via CRISPR/Cas9. Scientific Reports, 6, 33840.
Jactel H, Koricheva J, Castagneyrol B. 2019. Responses of forest insect pests to climate change: not so simple. Current Opinion in Insect Science, 35, 103–108.
Jaffri S A, Yan Y, Scott M J, Schetelig M F. 2021. Conditional expression systems for Drosophila suzukii pest control. In: Garcia F R M, ed., Drosophila Suzukii Management. Springer Cham, Switzerland. pp. 199–215.
Jurat-Fuentes J L, Heckel D G, Ferre J. 2021. Mechanisms of resistance to insecticidal proteins from Bacillus thuringiensis. Annual Review of Entomology, 66, 121–140.
Kandul N P, Liu J, Akbari O S. 2021a. Temperature-inducible precision-guided sterile insect technique. CRISPR Journal, 4, 822–835.
Kandul N P, Liu J, Bennett J B, Marshall J M, Akbari O S. 2021b. A confinable home-and-rescue gene drive for population modification. eLife, 10, e65939.
Kandul N P, Liu J, Sanchez C H M, Wu S L, Marsha J M, Akbari O S. 2019. Transforming insect population control with precision guided sterile males with demonstration in flies. Nature Communications, 10, 84.
Kemphues K J, Kaufman T C, Raff R A, Raff E C. 1982. The testis-specific beta-tubulin subunit in Drosophila melanogaster has multiple functions in spermatogenesis. Cell, 31, 655–670.
Klassen W, Curtis C F. 2005. History of the sterile insect technique. In: Dyck V A, Hendrichs J, Robinson A, eds., Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management. Springer, Dordrecht, The Netherlands. pp. 4–19.
Knipling E F. 1955. Possibilities of insect control or eradication through the use of sexually sterile males. Journal of Economic Entomology, 48, 459–462.
Knipling E F. 1959. Sterile-male method of population control. Science, 130, 902–904.
Knipling E F, Laven H, Craig G B, Pal R, Kitzmiller J B, Smith C N, Brown A W. 1968. Genetic control of insects of public health importance. Bull World Health Organ, 38, 421–438.
Knott G J, Doudna J A. 2018. CRISPR-Cas guides the future of genetic engineering. Science, 361, 866–869.
Knudsen K E, Reid W R, Barbour T M, Bowes L M, Duncan J, Philpott E, Potter S, Scott M J. 2020. Genetic variation and potential for resistance development to the tTA overexpression lethal system in insects. G3 (Bethesda), 10, 1271–1281.
Koskinioti P, Augustinos A A, Carvalho D O, Misbah-Ul-Haq M, Pillwax G, de la Fuente L D, Salvador-Herranz G, Herrero R A, Bourtzis K. 2021. Genetic sexing strains for the population suppression of the mosquito vector Aedes aegypti. Philosophical Transactions of the Royal Society (B: Biological Sciences), 376, 20190808.
Kyrou K, Hammond A M, Galizi R, Kranjc N, Burt A, Beaghton A K, Nolan T, Crisanti A. 2018. A CRISPR-Cas9 gene drive targeting doublesex causes complete population suppression in caged Anopheles gambiae mosquitoes. Nature Biotechnology, 36, 1062–1066.
Lance D R, McInnis D O, Rendon P, Jackson C G. 2000. Courtship among sterile and wild Ceratitis capitata (Diptera : Tephritidae) in field cages in Hawaii and Guatemala. Annals of the Entomological Society of America, 93, 1179–1185.
Lees R S, Amato R D, Benedict M Q. 2022. Inducible and repressible systems for transgene expression. In: Benedict M Q, Scott M J, eds., Transgenic Insects: Techniques and Applications. Commonwealth Agricultural Bureaux International Publishing, Wallingford, UK.
Lefevre G, Johnson T K. 1973. Evidence for a sex-linked haplo-inviable locus in the cut-singed region of Drosophila melanogaster. Genetics, 74, 633–645.
Li F, Zhao X, Li M, He K, Huang C, Zhou Y, Li Z, Walters J R. 2019. Insect genomes: Progress and challenges. Insect Molecular Biology, 28, 739–758.
Li J, Handler A M. 2017. Temperature-dependent sex-reversal by a transformer-2 gene-edited mutation in the spotted wing drosophila, Drosophila suzukii. Scientific Reports, 7, 12363.
Li J J, Shi Y, Wu J N, Li H, Smagghe G, Liu T X. 2021. CRISPR/Cas9 in lepidopteran insects: Progress, application and prospects. Journal of Insect Physiology, 135, 104325.
Li M, Yang T, Bui M, Gamez S, Wise T, Kandul N P, Liu J, Alcantara L, Lee H, Edula J R, Raban R, Zhan Y, Wang Y, DeBeaubien N, Chen J, Sanchez C H, Bennett J B, Antoshechkin I, Montell C, Marshall J M, et al. 2021. Suppressing mosquito populations with precision guided sterile males. Nature Communications, 12, 5374.
Liu N. 2015. Insecticide resistance in mosquitoes: impact, mechanisms, and research directions. Annual Review of Entomology, 60, 537–559.
Lunshof J E, Birnbaum A. 2017. Adaptive risk management of gene drive experiments-biosafety, biosecurity, and ethics. Journal of ABSA International, 22, 97–103.
Magori K, Gould F. 2006. Genetically engineered underdominance for manipulation of pest populations: A deterministic model. Genetics, 172, 2613–2620.
Marec F, Neven L G, Robinson A S, Vreysen M, Goldsmith M R, Nagaraju J, Franz G. 2005. Development of genetic sexing strains in Lepidoptera: from traditional to transgenic approaches. Journal of Economic Entomology, 98, 248–259.
Marec F, Vreysen M J B. 2019. Advances and challenges of using the sterile insect technique for the management of pest Lepidoptera. Insects, 10, 371.
Meccariello A, Krsticevic F, Colonna R, Del Corsano G, Fasulo B, Papathanos P A, Windbichler N. 2021. Engineered sex ratio distortion by X-shredding in the global agricultural pest Ceratitis capitata. BMC Biology, 19, 78.
Meccariello A, Salvemini M, Primo P, Hall B, Koskinioti P, Dalikova M, Gravina A, Gucciardino M A, Forlenza F, Gregoriou M E, Ippolito D, Monti S M, Petrella V, Perrotta M M, Schmeing S, Ruggiero A, Scolari F, Giordano E, Tsoumani K T, Marec F, et al. 2019. Maleness-on-the-Y (MoY) orchestrates male sex determination in major agricultural fruit fly pests. Science, 65, 1457–1460.
Meltzer H, Marom E, Alyagor I, Mayseless O, Berkun V, Segal-Gilboa N, Unger T, Luginbuhl D, Schuldiner O. 2019. Tissue-specific (ts) CRISPR as an efficient strategy for in vivo screening in Drosophila. Nature Communications, 10, 2113.
Mills E M, Barlow V L, Luk L Y P, Tsai Y H. 2020. Applying switchable Cas9 variants to in vivo gene editing for therapeutic applications. Cell Biology and Toxicology, 36, 17–29.
Murovec J, Pirc Z, Yang B. 2017. New variants of CRISPR RNA-guided genome editing enzymes. Plant Biotechnology Journal, 15, 917–926.
Nguyen T N M, Choo A, Baxter S W. 2021. Lessons from Drosophila: engineering genetic sexing strains with temperature-sensitive lethality for sterile insect technique applications. Insects, 12, 243.
Noble C, Adlam B, Church G M, Esvelt K M, Nowak M A. 2018. Current CRISPR gene drive systems are likely to be highly invasive in wild populations. eLife, 7, e33423.
Oberhofer G, Ivy T, Hay B A. 2018. Behavior of homing endonuclease gene drives targeting genes required for viability or female fertility with multiplexed guide RNAs. Proceedings of the National Academy of Sciences of the United States of America, 115, E9343–E9352.
Oberhofer G, Ivy T, Hay B A. 2019. Cleave and Rescue, a novel selfish genetic element and general strategy for gene drive. Proceedings of the National Academy of Sciences of the United States of America, 116, 6250–6259.
Oberhofer G, Ivy T, Hay B A. 2020. Gene drive and resilience through renewal with next generation Cleave and Rescue selfish genetic elements. Proceedings of the National Academy of Sciences of the United States of America, 117, 9013–9021.
Oberhofer G, Ivy T, Hay B A. 2021. Split versions of cleave and rescue selfish genetic elements for measured self limiting gene drive. PLoS Genetics, 17, e1009385.
Oerke E C. 2006. Crop losses to pests. Journal of Agricultural Science, 144, 31–43.
Oye K A, Esvelt K, Appleton E, Catteruccia F, Church G, Kuiken T, Lightfoot S B, McNamara J, Smidler A, Collins J P. 2014. Regulating gene drives. Science, 345, 626–628.
Pane A, Salvemini M, Delli B P, Polito C, Saccone G. 2002. The transformer gene in Ceratitis capitata provides a genetic basis for selecting and remembering the sexual fate. Development, 129, 3715–3725.
Papathanos P A, Windbichler N. 2018. Redkmer: An assembly-free pipeline for the identification of abundant and specific X-chromosome target sequences for X-Shredding by CRISPR endonucleases. The CRISPR Journal, 1, 88–98.
Pham T B, Phong C H, Bennett J B, Hwang K, Jasinskiene N, Parker K, Stillinger D, Marshall J M, Carballar-Lejarazu R, James A A. 2019. Experimental population modification of the malaria vector mosquito, Anopheles stephensi. PLoS Genetics, 15, e1008440.
Poelchau M, Childers C, Moore G, Tsavatapalli V, Evans J, Lee C Y, Lin H, Lin J W, Hackett K. 2015. The i5k Workspace@NAL - enabling genomic data access, visualization and curation of arthropod genomes. Nucleic Acids Research, 43, D714–D719.
Port F, Strein C, Stricker M, Rauscher B, Heigwer F, Zhou J, Beyersdorffer C, Frei J, Hess A, Kern K, Lange L, Langner N, Malamud R, Pavlovic B, Radecke K, Schmitt L, Voos L, Valentini E, Boutros M. 2020. A large-scale resource for tissue-specific CRISPR mutagenesis in Drosophila. eLife, 9, e53865.
Price T A R, Windbichler N, Unckless R L, Sutter A, Runge J N, Ross P A, Pomiankowski A, Nuckolls N L, Montchamp-Moreau C, Mideo N, Martin O Y, Manser A, Legros M, Larracuente A M, Holman L, Godwin J, Gemmell N, Courret C, Buchman A, Barrett L G, et al. 2020. Resistance to natural and synthetic gene drive systems. Journal of Evolutionary Biology, 33, 1345–1360.
Qian W Q, Wan F H. 2018. China launches the “IAS1000 Project”. Journal of Integrative Agriculture, 17, 2840–2841.
Raban R R, Marshall J M, Akbari O S. 2020. Progress towards engineering gene drives for population control. Journal of Experimental Biology, 223, jeb208181.
Rani L, Thapa K, Kanojia N, Sharma N, Singh S, Grewal A S, Srivastav A L, Kaushal J. 2021. An extensive review on the consequences of chemical pesticides on human health and environment. Journal of Cleaner Production, 283, 124657.
Rendon P, McInnis D, Lance D, Stewart J. 2004. Medfly (Diptera: Tephritidae) genetic sexing: Large-scale field comparison of males-only and bisexual sterile fly releases in Guatemala. Journal of Economic Entomology, 97, 1547–1553.
Ribeiro J M C, Kidwell M G. 1994. Transposable elements as population drive mechanisms-specification of critical parameter values. Journal of Medical Entomology, 31, 10–16.
Richter F, Fonfara I, Gelfert R, Nack J, Charpentier E, Moglich A. 2017. Switchable Cas9. Current Opinion in Biotechnology, 48, 119–126.
Robinson A S. 1976. Progress in the use of chromosomal translocations for the control of insect pests. Biological Reviews of the Cambridge Philosophical Society, 51, 1–24.
Robinson A S, Knols B G, Voigt G, Hendrichs J. 2009. Conceptual framework and rationale. Malaria Journal, 8(Suppl. 2), S1.
Sander J D, Joung J K. 2014. CRISPR-Cas systems for editing, regulating and targeting genomes. Nature Biotechnology, 32, 347–355.
Schliekelman P, Ellner S, Gould F. 2005. Pest control by genetic manipulation of sex ratio. Journal of Economic Entomology, 98, 18–34.
Scott M J, Concha C, Welchc J B, Phillips P L, Skoda S R. 2017. Research advances in the screwworm eradication program over the past 25 years. Entomologia Experimentalis et Applicata, 164, 226–236.
Simmons G S, Suckling D M, Carpenter J E, Addison M F, Dyck V A, Vreysen M J B. 2010. Improved quality management to enhance the efficacy of the sterile insect technique for lepidopteran pests. Journal of Applied Entomology, 134, 261–273.
Simoni A, Hammond A M, Beaghton A K, Galizi R, Taxiarchi C, Kyrou K, Meacci D, Gribble M, Morselli G, Burt A, Nolan T, Crisanti A. 2020. A male-biased sex-distorter gene drive for the human malaria vector Anopheles gambiae. Nature Biotechnology, 38, 1054–1060.
Sinkins S P, Godfray H C J. 2004. Use of Wolbachia to drive nuclear transgenes through insect populations. Proceedings of the Royal Society (B: Biological Sciences), 271, 1421–1426.
Sinkins S P, Gould F. 2006. Gene drive systems for insect disease vectors. Nature Reviews, 7, 427–435.
Stewart M J, Denell R. 1993. Mutations in the Drosophila gene encoding ribosomal protein S6 cause tissue overgrowth. Molecular and Cellular Biology, 13, 2524–2535.
Sun D, Guo Z J, Liu Y, Zhang Y J. 2017. Progress and prospects of CRISPR/Cas systems in insects and other arthropods. Frontiers in Physiology, 8, 608.
Taning C N T, Van Eynde B, Yu N, Ma S Y, Smagghe G. 2017. CRISPR/Cas9 in insects: Applications, best practices and biosafety concerns. Journal of Insect Physiology, 98, 245–257.
Tonnang H E, Sokame B M, Abdel-Rahman E M, Dubois T. 2022. Measuring and modelling crop yield losses due to invasive insect pests under climate change. Current Opinion in Insect Science, 50, 100873.
Traut W, Sahara K, Marec F. 2007. Sex chromosomes and sex determination in Lepidoptera. Sexual Development, 1, 332–346.
Tsoumani K T, Meccariello A, Mathiopoulos K D, Papathanos P A. 2020. Developing CRISPR-based sex-ratio distorters for the genetic control of fruit fly pests: A how to manual. Archives of Insect Biochemistry and Physiology, 103, e21652.
Turelli M, Hoffmann A A. 1991. Rapid spread of an inherited incompatibility factor in California Drosophila. Nature, 53, 440–442.
Upadhyay A, Feltman N R, Sychla A, Janzen A, Das S R, Maselko M, Smanski M. 2022. Genetically engineered insects with sex-selection and genetic incompatibility enable population suppression. eLife, 11, e71230.
Vanseventer H A. 1975. Genetic-control of insect pests. Tropical and Geographical Medicine, 27, 115–115.
Venken K J, Simpson J H, Bellen H J. 2011. Genetic manipulation of genes and cells in the nervous system of the fruit fly. Neuron, 72, 202–230.
Verkuijl S A N, Ang J X D, Alphey L, Bonsall M B, Anderson M A E. 2022. The challenges in developing efficient and robust synthetic homing endonuclease gene drives. Front Bioeng Biotechnol, 10, 856981.
Vreysen M J B, Abd-Alla A M M, Bourtzis K, Bouyer J, Caceres C, de Beer C, Oliveira Carvalho D, Maiga H, Mamai W, Nikolouli K, Yamada H, Pereira R. 2021. The insect pest control laboratory of the joint FAO/IAEA programme: Ten years (2010–2020) of research and development, achievements and challenges in support of the sterile insect technique. Insects, 12, 346.
Wade M J, Beeman R W. 1994. The population dynamics of maternal-effect selfish genes. Genetics, 138, 1309–1314.
Wan F H, Yin C L, Tang R, Chen M H, Wu Q, Huang C, Qian W Q, Rota-Stabelli O, Yang N W, Wang S P, Wang G R, Zhang G F, Guo J Y, Gu L Q, Chen L F, Xing L S, Xi Y, Liu F L, Lin K J, Guo M B, et al. 2019. A chromosome-level genome assembly of Cydia pomonella provides insights into chemical ecology and insecticide resistance. Nature Communications, 10, 4237.
Wang G H, Du J, Chu C Y, Madhav M, Hughes G L, Champer J. 2022. Symbionts and gene drive: Two strategies to combat vector-borne disease. Trends in Genetics, 38, 708–723.
Wang Y, Xu X, Chen X, Li X, Bi H, Xu J, Zhu C, Niu C, Huang Y. 2021. Mutation of P-element somatic inhibitor induces male sterility in the diamondback moth, Plutella xylostella. Pest Management Science, 77, 3588–3596.
Ward C M, Aumann R A, Whitehead M A, Nikolouli K, Leveque G, Gouvi G, Fung E, Reiling S J, Djambazian H, Hughes M A, Whiteford S, Caceres-Barrios C, Nguyen T N M, Choo A, Crisp P, Sim S B, Geib S M, Marec F, Hacker I, Ragoussis J, et al. 2021. White pupae phenotype of tephritids is caused by parallel mutations of a MFS transporter. Nature Communications, 12, 491.
Ward C M, Su J T, Huang Y X, Lloyd A L, Gould F, Hay B A. 2011. Medea selfish genetic elements as tools for altering traits of wild populations: A theoretical analysis. Evolution, 65, 1149–1162.
Webber B L, Raghu S, Edwards O R. 2015. Opinion: Is CRISPR-based gene drive a biocontrol silver bullet or global conservation threat? Proceedings of the National Academy of Sciences of the United States of America, 112, 10565–10567.
WHO (World Health Organization). 2014. A global brief on vector-borne diseases. [2021-10-25]. https://apps.who.int/iris/handle/10665/111008
WHO (World Health Organization). 2021. Guidance framework for testing genetically modified mosquitoes. [2021-10-25]. https://apps.who.int/iris/bitstream/handle/10665/341370/9789240025233-eng.pdf?sequence=1
Wiedenheft B, Sternberg S H, Doudna J A. 2012. RNA-guided genetic silencing systems in bacteria and archaea. Nature, 482, 331–338.
Windbichler N, Papathanos P A, Catteruccia F, Ranson H, Burt A, Crisanti A. 2007. Homing endonuclease mediated gene targeting in Anopheles gambiae cells and embryos. Nucleic Acids Research, 35, 5922–5933.
Xu J, Chen S, Zeng B, James A A, Tan A, Huang Y. 2017. Bombyx mori P-element somatic inhibitor (BmPSI) is a key auxiliary factor for Silkworm male sex determination. PLoS Genetics, 13, e1006576.
Xu X, Harvey-Samuel T, Siddiqui H A, Ang J X, Anderson M E, Reitmayer C M, Lovett E, Leftwich P T, You M, Alphey L. 2022. Toward a CRISPR-Cas9-based gene drive in the diamondback moth Plutella xylostella. CRISPR Journal, 5, 224–236.
Xu X, Yang J, Harvey-Samuel T, Huang Y, Asad M, Chen W, He W, Yang G, Alphey L, You M. 2020. Identification and characterization of the vasa gene in the diamondback moth, Plutella xylostella. Insect Biochemistry and Molecular Biology, 122, 103371.
Yan Y, Kobayashi Y, Huang C, Liu B, Qian W, Wan F, Schetelig M F. 2021. Highly efficient temperature inducible CRISPR-Cas9 gene targeting in Drosophila suzukii. International Journal of Molecular Sciences, 22, 6724.
Yan Y, Scott M J. 2020. Building a transgenic sexing strain for genetic control of the Australian sheep blow fly Lucilia cuprina using two lethal effectors. BMC Genetics, 21, 141.
Yan Y, Williamson M E, Davis R J, Andere A A, Picard C J, Scott M J. 2020. Improved transgenic sexing strains for genetic control of the Australian sheep blow fly Lucilia cuprina using embryo-specific gene promoters. Molecular Genetics and Genomics, 295, 287–298.
Yang D, Xu J, Chen K, Liu Y, Yang X, Tang L, Luo X, Liu Z, Li M, Walters J R, Huang Y. 2022. BmPMFBP1 regulates the development of eupyrene sperm in the silkworm, Bombyx mori. PLoS Genetics, 18, e1010131.
Yin C, Shen G, Guo D, Wang S, Ma X, Xiao H, Liu J, Zhang Z, Liu Y, Zhang Y, Yu K, Huang S, Li F. 2016. InsectBase: A resource for insect genomes and transcriptomes. Nucleic Acids Research, 44, D801–D807.
You M S, Ke F S, You S J, Wu Z Y, Liu Q F, He W Y, Baxter S W, Yuchi Z G, Vasseur L, Gurr G M, Ward C M, Cerda H, Yang G, Peng L, Jin Y C, Xie M, Cai L J, Douglas C J, Isman M B, Goettel M S, et al. 2020. Variation among 532 genomes unveils the origin and evolutionary history of a global insect herbivore. Nature Communications, 11, 2321.
Zhang Z J, Niu B L, Ji D F, Li M W, Li K, James A A, Tan A J, Huang Y P. 2018. Silkworm genetic sexing through W chromosome-linked, targeted gene integration. Proceedings of the National Academy of Sciences of the United States of America, 115, 8752–8756.
Zhao Y, Schetelig M F, Handler A M. 2020. Genetic breakdown of a Tet-off conditional lethality system for insect population control. Nature Communications, 11, 3095.