Genetic analyses and detection of point mutations in the acetylcholinesterase-1 gene associated with organophosphate insecticide resistance in fall armyworm (Spodoptera frugiperda) populations from Uganda
Abstract Background The fall armyworm (FAW), Spodoptera frugiperda; J.E. Smith (Lepidoptera: Noctuidae), is now an economically important pest that causes huge losses to maize productivity in sub-Saharan Africa. Variations in sub-population genetics and the processes of rapid adaptation underpinning...
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| Format: | Article |
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BMC
2023-01-01
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| Series: | BMC Genomics |
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| Online Access: | https://doi.org/10.1186/s12864-022-09093-4 |
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| author | Geresemu Omuut Happyness G. Mollel Dalton Kanyesigye Félicien Akohoue Stella Adumo Aropet Henry Wagaba Michael H. Otim |
| author_facet | Geresemu Omuut Happyness G. Mollel Dalton Kanyesigye Félicien Akohoue Stella Adumo Aropet Henry Wagaba Michael H. Otim |
| author_sort | Geresemu Omuut |
| collection | DOAJ |
| description | Abstract Background The fall armyworm (FAW), Spodoptera frugiperda; J.E. Smith (Lepidoptera: Noctuidae), is now an economically important pest that causes huge losses to maize productivity in sub-Saharan Africa. Variations in sub-population genetics and the processes of rapid adaptation underpinning the invasion remain unclear. For this, the genetic identity and diversity of FAW populations in Uganda were revealed by sequencing 87 samples (collected across the country). Based on the partial mitochondrial cytochrome oxidase I (COI) gene polymorphisms, we further examined the mitochondrial haplotype configuration and compared the FAW in Uganda with sequences from other parts of the world. The molecular target for organophosphate and carbamate resistance, acetylcholinesterase, was also investigated. Results Analysis of the partial COI gene sequences showed the presence of both rice (predominant) and corn strain haplotypes, with a haplotype diversity of 0.382. Based on the COI marker, pairwise difference distribution analyses, and neutrality tests, showed that the FAW populations in Uganda and the rest of Africa are evolving neutrally, but those in America and Asia are undergoing expansion. Our findings support observations that invasive FAW populations throughout the rest of Africa and Asia share a common origin. Sequencing of the S. frugiperda ace-1 gene revealed four amino acid substitutions, two of which (A201S and F290V) were previously shown to confer organophosphate resistance in both S. frugiperda and several other insect species. The other two previously reported new variations in positions g-396 and g-768, are presumed to be related to the development of insecticide resistance. Conclusions This research has increased our knowledge of the genetics of FAW in Uganda, which is critical for pest surveillance and the detection of resistance. However, due to the low gene polymorphism of COI, more evolutionary studies incorporating the Spodoptera frugiperda whole-genome sequence are required to precisely understand the FAW population dynamics, introduction paths, origin, and subsequent spread. |
| first_indexed | 2024-04-10T21:04:27Z |
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| id | doaj.art-980914441be04616ad23abc1e08cde93 |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-04-10T21:04:27Z |
| publishDate | 2023-01-01 |
| publisher | BMC |
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| series | BMC Genomics |
| spelling | doaj.art-980914441be04616ad23abc1e08cde932023-01-22T12:05:36ZengBMCBMC Genomics1471-21642023-01-0124111510.1186/s12864-022-09093-4Genetic analyses and detection of point mutations in the acetylcholinesterase-1 gene associated with organophosphate insecticide resistance in fall armyworm (Spodoptera frugiperda) populations from UgandaGeresemu Omuut0Happyness G. Mollel1Dalton Kanyesigye2Félicien Akohoue3Stella Adumo Aropet4Henry Wagaba5Michael H. Otim6National Agricultural Research Organization, National Crops Resources Research InstituteTanzania Agricultural Research Institute-MikocheniNational Agricultural Research Organization, National Crops Resources Research InstituteLaboratory of Genetics, Biotechnology and Seed Science (GBioS), Faculty of Agronomic Sciences, University of Abomey-CalaviNational Agricultural Research Organization, National Agricultural Research LaboratoriesNational Agricultural Research Organization, National Crops Resources Research InstituteNational Agricultural Research Organization, National Crops Resources Research InstituteAbstract Background The fall armyworm (FAW), Spodoptera frugiperda; J.E. Smith (Lepidoptera: Noctuidae), is now an economically important pest that causes huge losses to maize productivity in sub-Saharan Africa. Variations in sub-population genetics and the processes of rapid adaptation underpinning the invasion remain unclear. For this, the genetic identity and diversity of FAW populations in Uganda were revealed by sequencing 87 samples (collected across the country). Based on the partial mitochondrial cytochrome oxidase I (COI) gene polymorphisms, we further examined the mitochondrial haplotype configuration and compared the FAW in Uganda with sequences from other parts of the world. The molecular target for organophosphate and carbamate resistance, acetylcholinesterase, was also investigated. Results Analysis of the partial COI gene sequences showed the presence of both rice (predominant) and corn strain haplotypes, with a haplotype diversity of 0.382. Based on the COI marker, pairwise difference distribution analyses, and neutrality tests, showed that the FAW populations in Uganda and the rest of Africa are evolving neutrally, but those in America and Asia are undergoing expansion. Our findings support observations that invasive FAW populations throughout the rest of Africa and Asia share a common origin. Sequencing of the S. frugiperda ace-1 gene revealed four amino acid substitutions, two of which (A201S and F290V) were previously shown to confer organophosphate resistance in both S. frugiperda and several other insect species. The other two previously reported new variations in positions g-396 and g-768, are presumed to be related to the development of insecticide resistance. Conclusions This research has increased our knowledge of the genetics of FAW in Uganda, which is critical for pest surveillance and the detection of resistance. However, due to the low gene polymorphism of COI, more evolutionary studies incorporating the Spodoptera frugiperda whole-genome sequence are required to precisely understand the FAW population dynamics, introduction paths, origin, and subsequent spread.https://doi.org/10.1186/s12864-022-09093-4Fall armywormSpodoptera frugiperdaCorn/rice strainsHaplotypesCytochrome oxidase ITriosephosphate Isomerase |
| spellingShingle | Geresemu Omuut Happyness G. Mollel Dalton Kanyesigye Félicien Akohoue Stella Adumo Aropet Henry Wagaba Michael H. Otim Genetic analyses and detection of point mutations in the acetylcholinesterase-1 gene associated with organophosphate insecticide resistance in fall armyworm (Spodoptera frugiperda) populations from Uganda BMC Genomics Fall armyworm Spodoptera frugiperda Corn/rice strains Haplotypes Cytochrome oxidase I Triosephosphate Isomerase |
| title | Genetic analyses and detection of point mutations in the acetylcholinesterase-1 gene associated with organophosphate insecticide resistance in fall armyworm (Spodoptera frugiperda) populations from Uganda |
| title_full | Genetic analyses and detection of point mutations in the acetylcholinesterase-1 gene associated with organophosphate insecticide resistance in fall armyworm (Spodoptera frugiperda) populations from Uganda |
| title_fullStr | Genetic analyses and detection of point mutations in the acetylcholinesterase-1 gene associated with organophosphate insecticide resistance in fall armyworm (Spodoptera frugiperda) populations from Uganda |
| title_full_unstemmed | Genetic analyses and detection of point mutations in the acetylcholinesterase-1 gene associated with organophosphate insecticide resistance in fall armyworm (Spodoptera frugiperda) populations from Uganda |
| title_short | Genetic analyses and detection of point mutations in the acetylcholinesterase-1 gene associated with organophosphate insecticide resistance in fall armyworm (Spodoptera frugiperda) populations from Uganda |
| title_sort | genetic analyses and detection of point mutations in the acetylcholinesterase 1 gene associated with organophosphate insecticide resistance in fall armyworm spodoptera frugiperda populations from uganda |
| topic | Fall armyworm Spodoptera frugiperda Corn/rice strains Haplotypes Cytochrome oxidase I Triosephosphate Isomerase |
| url | https://doi.org/10.1186/s12864-022-09093-4 |
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