Dataset Information

Symbiont-Mediated Insecticide Detoxification as an Emerging Problem in Insect Pests.

ABSTRACT: Pesticide use is prevalent with applications from the backyard gardener to large-scale agriculture and combatting pests in homes and industrial settings. Alongside the need to control unwanted pests comes the selective pressure generated by sustained pesticide use has become a concern leading to environmental contamination, pest resistance, and, thus, reduced pesticide efficacy. Despite efforts to improve the environmental impact and reduce off-target effects, chemical pesticides are relied on and control failures are costly. Though pesticide resistance mechanisms vary, one pattern that has recently emerged is symbiont-mediated detoxification within insect pests. The localization within the insect host, the identity of the symbiotic partner, and the stability of the associations across different systems vary. The diversity of insects and ecological settings linked to this phenomenon are broad. In this mini-review, we summarize the recent trend of insecticide detoxification modulated by symbiotic associations between bacteria and insects, as well as highlight the implications for pesticide development, pest management strategies, and pesticide bioremediation.

SUBMITTER: Blanton AG

PROVIDER: S-EPMC7554331 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Symbiont-Mediated Insecticide Detoxification as an Emerging Problem in Insect Pests.

Blanton Alison G AG Peterson Brittany F BF

Frontiers in microbiology 20200930

Pesticide use is prevalent with applications from the backyard gardener to large-scale agriculture and combatting pests in homes and industrial settings. Alongside the need to control unwanted pests comes the selective pressure generated by sustained pesticide use has become a concern leading to environmental contamination, pest resistance, and, thus, reduced pesticide efficacy. Despite efforts to improve the environmental impact and reduce off-target effects, chemical pesticides are relied on a ...[more]

PMID: 33101225

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Project description:Abstract Target?site mutations and detoxification gene overexpression are two major mechanisms conferring insecticide resistance. Molecular assays applied to detect these resistance genetic markers are time?consuming and with high false?positive rates. RNA?Seq data contains information on the variations within expressed genomic regions and expression of detoxification genes. However, there is no corresponding method to detect resistance markers at present. Here, we collected 66 reported resistance mutations of four insecticide targets (AChE, VGSC, RyR, and nAChR) from 82 insect species. Next, we obtained 403 sequences of the four target genes and 12,665 sequences of three kinds of detoxification genes including P450s, GSTs, and CCEs. Then, we developed a Perl program, FastD, to detect target?site mutations and overexpressed detoxification genes from RNA?Seq data and constructed a web server for FastD (http://www.insect-genome.com/fastd). The estimation of FastD on simulated RNA?Seq data showed high sensitivity and specificity. We applied FastD to detect resistant markers in 15 populations of six insects, Plutella xylostella, Aphis gossypii, Anopheles arabiensis, Musca domestica, Leptinotarsa decemlineata and Apis mellifera. Results showed that 11 RyR mutations in P. xylostella, one nAChR mutation in A. gossypii, one VGSC mutation in A. arabiensis and five VGSC mutations in M. domestica were found to be with frequency difference >40% between resistant and susceptible populations including previously confirmed mutations G4946E in RyR, R81T in nAChR and L1014F in VGSC. And 49 detoxification genes were found to be overexpressed in resistant populations compared with susceptible populations including previously confirmed detoxification genes CYP6BG1, CYP6CY22, CYP6CY13, CYP6P3, CYP6M2, CYP6P4 and CYP4G16. The candidate target?site mutations and detoxification genes were worth further validation. Resistance estimates according to confirmed markers were consistent with population phenotypes, confirming the reliability of this program in predicting population resistance at omics?level. We developed a program called FastD to detect the insecticide target?site mutations and overexpressed detoxification genes from RNA?Seq data and constructed a corresponding web server for FastD (http://www.insect-genome.com/fastd) in this article.

Project description:Many insect species, such as aphids, leafhoppers, planthoppers, and whiteflies harbor obligate bacterial symbionts that can be transovarially transmitted to offspring through the oocytes of female insects. Whether obligate bacterial symbionts can carry important molecules/resources to the embryos to support egg development is still unknown. Here, we show that the vitellogenin (Vg) precursor of rice leafhopper Nephotettix cincticeps is biosynthesized by the fat body, secreted into the hemolymph and subsequently cleaved into the 35- and 178-kDa subunits, whereas only the 178-kDa subunit is taken up by the leading end of oocytes in a receptor-dependent manner or moves into the posterior pole of the terminal oocyte in association with obligate bacterial symbiont "Candidatus Nasuia deltocephalinicola" (hereafter Nasuia) in a receptor-independent manner. Furthermore, the 178-kDa Vg subunit can directly interact with a surface channel molecule (porin) on the envelope of Nasuia, allowing Vg to enter bacterial cytoplasm. Thus, Vg can hitchhike the ancient oocyte entry path of Nasuia, the common obligate symbiont of leafhoppers. Knocking down a Nasuia growth-related protein expression or treatment with porin antibody strongly prevents the ability of Nasuia to carry Vgs into oocytes and impair insect egg development. Nasuia-carried Vgs provide at least 20% of the total Vgs in the developing eggs. We anticipate that the bacterial symbiont-mediated Vg uptake into oocytes to support efficient egg development may be a common pattern shared by many insects.IMPORTANCE Many insects harbor obligate bacterial symbionts that can be vertically transmitted to offspring by female insects through eggs. Here, we report that leafhopper vitellogenin (Vg) recognizes and binds a surface channel molecule (porin) on the envelope of obligate bacterial symbiont Nasuia, which potentially induces the opening of porin channels for Vg to access the cytoplasm of Nasuia Thus, Vg can exploit bacterial symbionts as the independent carriers into the oocytes. Such Nasuia-carried Vg contents support efficient insect egg development. Thus, our findings indicate that insects have evolved strategies to exploit the symbionts for carrying additional Vgs to guarantee optimal insect reproduction.

Dataset Information

Symbiont-Mediated Insecticide Detoxification as an Emerging Problem in Insect Pests.

Publications

Symbiont-Mediated Insecticide Detoxification as an Emerging Problem in Insect Pests.

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