A small-molecule approach to restore female sterility phenotype targeted by a homing suppression gene drive in the fruit pest Drosophila suzukii
CRISPR-based gene drives offer promising prospects for controlling disease-transmitting vectors and agricultural pests. A significant challenge for successful suppression-type drive is the rapid evolution of resistance alleles. One approach to mitigate the development of resistance involves targetin...
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| creator | Ma, Suhan Ni, Xuyang Chen, Shimin Qiao, Xiaomu Xu, Xuejiao Chen, Weizhe Champer, Jackson Huang, Jia |
| description | CRISPR-based gene drives offer promising prospects for controlling disease-transmitting vectors and agricultural pests. A significant challenge for successful suppression-type drive is the rapid evolution of resistance alleles. One approach to mitigate the development of resistance involves targeting functionally constrained regions using multiple gRNAs. In this study, we constructed a 3-gRNA homing gene drive system targeting the recessive female fertility gene Tyrosine decarboxylase 2 (Tdc2) in Drosophila suzukii, a notorious fruit pest. Our investigation revealed only a low level of homing in the germline, but feeding octopamine restored the egg-laying defects in Tdc2 mutant females, allowing easier line maintenance than for other suppression drive targets. We tested the effectiveness of a similar system in Drosophila melanogaster and constructed additional split drive systems by introducing promoter-Cas9 transgenes to improve homing efficiency. Our findings show that genetic polymorphisms in wild populations may limit the spread of gene drive alleles, and the position effect profoundly influences Cas9 activity. Furthermore, this study highlights the potential of conditionally rescuing the female infertility caused by the gene drive, offering a valuable tool for the industrial-scale production of gene drive transgenic insects. |
| doi_str_mv | 10.1371/journal.pgen.1011226 |
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A significant challenge for successful suppression-type drive is the rapid evolution of resistance alleles. One approach to mitigate the development of resistance involves targeting functionally constrained regions using multiple gRNAs. In this study, we constructed a 3-gRNA homing gene drive system targeting the recessive female fertility gene Tyrosine decarboxylase 2 (Tdc2) in Drosophila suzukii, a notorious fruit pest. Our investigation revealed only a low level of homing in the germline, but feeding octopamine restored the egg-laying defects in Tdc2 mutant females, allowing easier line maintenance than for other suppression drive targets. We tested the effectiveness of a similar system in Drosophila melanogaster and constructed additional split drive systems by introducing promoter-Cas9 transgenes to improve homing efficiency. Our findings show that genetic polymorphisms in wild populations may limit the spread of gene drive alleles, and the position effect profoundly influences Cas9 activity. Furthermore, this study highlights the potential of conditionally rescuing the female infertility caused by the gene drive, offering a valuable tool for the industrial-scale production of gene drive transgenic insects.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1011226</identifier><identifier>PMID: 38578788</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Alleles ; Animals ; Biological research ; Biology and Life Sciences ; Biology, Experimental ; Chromosomes ; Control ; CRISPR ; CRISPR-Cas Systems ; Drosophila ; Drosophila - genetics ; Drosophila melanogaster - genetics ; Drosophila suzukii ; Egg laying ; Female ; Females ; Fruit ; Gene Drive Technology ; Gene polymorphism ; Genetic aspects ; Genetic engineering ; Genotype & phenotype ; gRNA ; Humans ; Infertility ; Infertility in animals ; Infertility, Female - genetics ; Insects ; Males ; Octopamine ; Pest resistance ; Pests ; Phenotype ; Phenotypes ; Population genetics ; Research and Analysis Methods ; RNA, Guide, CRISPR-Cas Systems ; Sterility ; Suppression, Genetic ; Transgenes ; Tyrosine decarboxylase ; Vectors</subject><ispartof>PLoS genetics, 2024-04, Vol.20 (4), p.e1011226-e1011226</ispartof><rights>Copyright: © 2024 Ma et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>COPYRIGHT 2024 Public Library of Science</rights><rights>2024 Ma et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2024 Ma et al 2024 Ma et al</rights><rights>2024 Ma et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c642t-fb986763227bd26de18cf6c7d1e5ccfdfb7da25db1d4b192c72dedff3c4443e83</cites><orcidid>0000-0002-3814-3774 ; 0000-0001-8336-1562 ; 0000-0001-9590-1319 ; 0000-0001-7543-5592 ; 0000-0002-4781-5747 ; 0000-0002-9025-093X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11023630/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11023630/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,729,782,786,866,887,2104,2930,23873,27931,27932,53798,53800</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38578788$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Copenhaver, Gregory P.</contributor><creatorcontrib>Ma, Suhan</creatorcontrib><creatorcontrib>Ni, Xuyang</creatorcontrib><creatorcontrib>Chen, Shimin</creatorcontrib><creatorcontrib>Qiao, Xiaomu</creatorcontrib><creatorcontrib>Xu, Xuejiao</creatorcontrib><creatorcontrib>Chen, Weizhe</creatorcontrib><creatorcontrib>Champer, Jackson</creatorcontrib><creatorcontrib>Huang, Jia</creatorcontrib><title>A small-molecule approach to restore female sterility phenotype targeted by a homing suppression gene drive in the fruit pest Drosophila suzukii</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>CRISPR-based gene drives offer promising prospects for controlling disease-transmitting vectors and agricultural pests. A significant challenge for successful suppression-type drive is the rapid evolution of resistance alleles. One approach to mitigate the development of resistance involves targeting functionally constrained regions using multiple gRNAs. In this study, we constructed a 3-gRNA homing gene drive system targeting the recessive female fertility gene Tyrosine decarboxylase 2 (Tdc2) in Drosophila suzukii, a notorious fruit pest. Our investigation revealed only a low level of homing in the germline, but feeding octopamine restored the egg-laying defects in Tdc2 mutant females, allowing easier line maintenance than for other suppression drive targets. We tested the effectiveness of a similar system in Drosophila melanogaster and constructed additional split drive systems by introducing promoter-Cas9 transgenes to improve homing efficiency. 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A significant challenge for successful suppression-type drive is the rapid evolution of resistance alleles. One approach to mitigate the development of resistance involves targeting functionally constrained regions using multiple gRNAs. In this study, we constructed a 3-gRNA homing gene drive system targeting the recessive female fertility gene Tyrosine decarboxylase 2 (Tdc2) in Drosophila suzukii, a notorious fruit pest. Our investigation revealed only a low level of homing in the germline, but feeding octopamine restored the egg-laying defects in Tdc2 mutant females, allowing easier line maintenance than for other suppression drive targets. We tested the effectiveness of a similar system in Drosophila melanogaster and constructed additional split drive systems by introducing promoter-Cas9 transgenes to improve homing efficiency. 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| subjects | Alleles Animals Biological research Biology and Life Sciences Biology, Experimental Chromosomes Control CRISPR CRISPR-Cas Systems Drosophila Drosophila - genetics Drosophila melanogaster - genetics Drosophila suzukii Egg laying Female Females Fruit Gene Drive Technology Gene polymorphism Genetic aspects Genetic engineering Genotype & phenotype gRNA Humans Infertility Infertility in animals Infertility, Female - genetics Insects Males Octopamine Pest resistance Pests Phenotype Phenotypes Population genetics Research and Analysis Methods RNA, Guide, CRISPR-Cas Systems Sterility Suppression, Genetic Transgenes Tyrosine decarboxylase Vectors |
| title | A small-molecule approach to restore female sterility phenotype targeted by a homing suppression gene drive in the fruit pest Drosophila suzukii |
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