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Insecticide resistance mechanisms in the green peach aphid Myzus persicae (Hemiptera: Aphididae) I: A transcriptomic survey.

Silva AX, Jander G, Samaniego H, Ramsey JS, Figueroa CC - PLoS ONE (2012)

Bottom Line: Insecticide resistance is one of the best examples of rapid micro-evolution found in nature.Since the development of the first synthetic insecticide in 1939, humans have invested considerable effort to stay ahead of resistance phenotypes that repeatedly develop in insects.This study suggests strongly that insecticide resistance in M. persicae is more complex that has been described, with the participation of a broad array of resistance mechanisms.

View Article: PubMed Central - PubMed

Affiliation: Instituto de Ciencias Ambientales y Evolutivas, Facultad de Ciencias, Universidad Austral de Chile, Valdivia, Chile.

ABSTRACT

Background: Insecticide resistance is one of the best examples of rapid micro-evolution found in nature. Since the development of the first synthetic insecticide in 1939, humans have invested considerable effort to stay ahead of resistance phenotypes that repeatedly develop in insects. Aphids are a group of insects that have become global pests in agriculture and frequently exhibit insecticide resistance. The green peach aphid, Myzus persicae, has developed resistance to at least seventy different synthetic compounds, and different insecticide resistance mechanisms have been reported worldwide.

Methodology/principal findings: To further characterize this resistance, we analyzed genome-wide transcriptional responses in three genotypes of M. persicae, each exhibiting different resistance mechanisms, in response to an anti-cholinesterase insecticide. The sensitive genotype (exhibiting no resistance mechanism) responded to the insecticide by up-regulating 183 genes primarily ones related to energy metabolism, detoxifying enzymes, proteins of extracellular transport, peptidases and cuticular proteins. The second genotype (resistant through a kdr sodium channel mutation), up-regulated 17 genes coding for detoxifying enzymes, peptidase and cuticular proteins. Finally, a multiply resistant genotype (carrying kdr and a modified acetylcholinesterase), up-regulated only 7 genes, appears not to require induced insecticide detoxification, and instead down-regulated many genes.

Conclusions/significance: This study suggests strongly that insecticide resistance in M. persicae is more complex that has been described, with the participation of a broad array of resistance mechanisms. The sensitive genotype exhibited the highest transcriptional plasticity, accounting for the wide range of potential adaptations to insecticides that this species can evolve. In contrast, the multiply resistant genotype exhibited a low transcriptional plasticity, even for the expression of genes encoding enzymes involved in insecticide detoxification. Our results emphasize the value of microarray studies to search for regulated genes in insects, but also highlights the many ways those different genotypes can assemble resistant phenotypes depending on the environmental pressure.

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Quantification of relative expression in different genotypes of Myzus persicae exposed to pirimicarb.Graphs represent the relative mRNA expression in aphids sprayed with pirimicarb in comparison to control (water). Data were normalized for interclonal variation using GADPH expression levels. Green bars correspond to the genotype S (sensitive), Yellow corresponds to the genotype SR (simple resistant) and red bars correspond to the genotype MR (multiple resistant). Same color bars represent the time after insecticide spraying, with left bar = 20 hours and right bar = 30 hours. Data are shown as mean ± SE of two independent experiments, with three technical replicates in each case. *p<0.05 and **p<0.01 indicate a significant difference compared to 1, which was used as a reference value for no change in gene expression, using a t-test. Gene abbreviations: (A) cathepsin B–N, cathepsin B clade N; (B) HSP-70, heat shock protein 70; (C) G protein, Heterotrimeric guanine nucleotide-binding protein; (D) GST, glutathione S-transferase; (E) Esterase, carboxylesterase type E4/FE4; (F) CYP6CYP3, cytochrome p450 family CYP6CYP3; (G) CYP4, cytochrome p450 family CYP4.
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pone-0036366-g006: Quantification of relative expression in different genotypes of Myzus persicae exposed to pirimicarb.Graphs represent the relative mRNA expression in aphids sprayed with pirimicarb in comparison to control (water). Data were normalized for interclonal variation using GADPH expression levels. Green bars correspond to the genotype S (sensitive), Yellow corresponds to the genotype SR (simple resistant) and red bars correspond to the genotype MR (multiple resistant). Same color bars represent the time after insecticide spraying, with left bar = 20 hours and right bar = 30 hours. Data are shown as mean ± SE of two independent experiments, with three technical replicates in each case. *p<0.05 and **p<0.01 indicate a significant difference compared to 1, which was used as a reference value for no change in gene expression, using a t-test. Gene abbreviations: (A) cathepsin B–N, cathepsin B clade N; (B) HSP-70, heat shock protein 70; (C) G protein, Heterotrimeric guanine nucleotide-binding protein; (D) GST, glutathione S-transferase; (E) Esterase, carboxylesterase type E4/FE4; (F) CYP6CYP3, cytochrome p450 family CYP6CYP3; (G) CYP4, cytochrome p450 family CYP4.

Mentions: The Cathepsin B gene showed a significant up-regulation in the S and SR genotypes at 20 hours after insecticide application, while at 30 hours up-regulation remained significant only in the S genotype. Genotype MR showed no evidence of regulation for this gene (Figure 6A). The Heat Shock Protein 70 gene showed a significant up-regulation in S and SR genotypes at 20 and 30 hours after the application of the insecticide. In contrast, the MR genotype showed a down-regulation for this gene (Figure 6B). The Heterotrimeric G protein gene did not show a significantly different transcription between treatments in any of the studied genotypes (Figure 6C). In this case, we found transcriptional differences between the results obtained by the microarray analysis compared to the RT-qPCR, which can be explained by intra-clonal variation (see Discussion). The Glutathione-S-transferase gene showed a significantly higher transcription in S and SR genotypes at 20 and 30 hours after the application of insecticide (Figure 6D), while no changes were detected in the MR genotype. The Esterase gene only showed a significant up-regulation at 20 hours after application of insecticide in the S genotype (Figure 6E), while all other genotypes were unaffected. Two genes of the Cytochrome P450 gene family were assessed (CYP6CY3 and CYP4). The genotypes S and SR showed an up-regulation for both genes at 20 and 30 hours after application of insecticide (Figure 6E and 6G), while the genotype MR showed no changes.


Insecticide resistance mechanisms in the green peach aphid Myzus persicae (Hemiptera: Aphididae) I: A transcriptomic survey.

Silva AX, Jander G, Samaniego H, Ramsey JS, Figueroa CC - PLoS ONE (2012)

Quantification of relative expression in different genotypes of Myzus persicae exposed to pirimicarb.Graphs represent the relative mRNA expression in aphids sprayed with pirimicarb in comparison to control (water). Data were normalized for interclonal variation using GADPH expression levels. Green bars correspond to the genotype S (sensitive), Yellow corresponds to the genotype SR (simple resistant) and red bars correspond to the genotype MR (multiple resistant). Same color bars represent the time after insecticide spraying, with left bar = 20 hours and right bar = 30 hours. Data are shown as mean ± SE of two independent experiments, with three technical replicates in each case. *p<0.05 and **p<0.01 indicate a significant difference compared to 1, which was used as a reference value for no change in gene expression, using a t-test. Gene abbreviations: (A) cathepsin B–N, cathepsin B clade N; (B) HSP-70, heat shock protein 70; (C) G protein, Heterotrimeric guanine nucleotide-binding protein; (D) GST, glutathione S-transferase; (E) Esterase, carboxylesterase type E4/FE4; (F) CYP6CYP3, cytochrome p450 family CYP6CYP3; (G) CYP4, cytochrome p450 family CYP4.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3369866&req=5

pone-0036366-g006: Quantification of relative expression in different genotypes of Myzus persicae exposed to pirimicarb.Graphs represent the relative mRNA expression in aphids sprayed with pirimicarb in comparison to control (water). Data were normalized for interclonal variation using GADPH expression levels. Green bars correspond to the genotype S (sensitive), Yellow corresponds to the genotype SR (simple resistant) and red bars correspond to the genotype MR (multiple resistant). Same color bars represent the time after insecticide spraying, with left bar = 20 hours and right bar = 30 hours. Data are shown as mean ± SE of two independent experiments, with three technical replicates in each case. *p<0.05 and **p<0.01 indicate a significant difference compared to 1, which was used as a reference value for no change in gene expression, using a t-test. Gene abbreviations: (A) cathepsin B–N, cathepsin B clade N; (B) HSP-70, heat shock protein 70; (C) G protein, Heterotrimeric guanine nucleotide-binding protein; (D) GST, glutathione S-transferase; (E) Esterase, carboxylesterase type E4/FE4; (F) CYP6CYP3, cytochrome p450 family CYP6CYP3; (G) CYP4, cytochrome p450 family CYP4.
Mentions: The Cathepsin B gene showed a significant up-regulation in the S and SR genotypes at 20 hours after insecticide application, while at 30 hours up-regulation remained significant only in the S genotype. Genotype MR showed no evidence of regulation for this gene (Figure 6A). The Heat Shock Protein 70 gene showed a significant up-regulation in S and SR genotypes at 20 and 30 hours after the application of the insecticide. In contrast, the MR genotype showed a down-regulation for this gene (Figure 6B). The Heterotrimeric G protein gene did not show a significantly different transcription between treatments in any of the studied genotypes (Figure 6C). In this case, we found transcriptional differences between the results obtained by the microarray analysis compared to the RT-qPCR, which can be explained by intra-clonal variation (see Discussion). The Glutathione-S-transferase gene showed a significantly higher transcription in S and SR genotypes at 20 and 30 hours after the application of insecticide (Figure 6D), while no changes were detected in the MR genotype. The Esterase gene only showed a significant up-regulation at 20 hours after application of insecticide in the S genotype (Figure 6E), while all other genotypes were unaffected. Two genes of the Cytochrome P450 gene family were assessed (CYP6CY3 and CYP4). The genotypes S and SR showed an up-regulation for both genes at 20 and 30 hours after application of insecticide (Figure 6E and 6G), while the genotype MR showed no changes.

Bottom Line: Insecticide resistance is one of the best examples of rapid micro-evolution found in nature.Since the development of the first synthetic insecticide in 1939, humans have invested considerable effort to stay ahead of resistance phenotypes that repeatedly develop in insects.This study suggests strongly that insecticide resistance in M. persicae is more complex that has been described, with the participation of a broad array of resistance mechanisms.

View Article: PubMed Central - PubMed

Affiliation: Instituto de Ciencias Ambientales y Evolutivas, Facultad de Ciencias, Universidad Austral de Chile, Valdivia, Chile.

ABSTRACT

Background: Insecticide resistance is one of the best examples of rapid micro-evolution found in nature. Since the development of the first synthetic insecticide in 1939, humans have invested considerable effort to stay ahead of resistance phenotypes that repeatedly develop in insects. Aphids are a group of insects that have become global pests in agriculture and frequently exhibit insecticide resistance. The green peach aphid, Myzus persicae, has developed resistance to at least seventy different synthetic compounds, and different insecticide resistance mechanisms have been reported worldwide.

Methodology/principal findings: To further characterize this resistance, we analyzed genome-wide transcriptional responses in three genotypes of M. persicae, each exhibiting different resistance mechanisms, in response to an anti-cholinesterase insecticide. The sensitive genotype (exhibiting no resistance mechanism) responded to the insecticide by up-regulating 183 genes primarily ones related to energy metabolism, detoxifying enzymes, proteins of extracellular transport, peptidases and cuticular proteins. The second genotype (resistant through a kdr sodium channel mutation), up-regulated 17 genes coding for detoxifying enzymes, peptidase and cuticular proteins. Finally, a multiply resistant genotype (carrying kdr and a modified acetylcholinesterase), up-regulated only 7 genes, appears not to require induced insecticide detoxification, and instead down-regulated many genes.

Conclusions/significance: This study suggests strongly that insecticide resistance in M. persicae is more complex that has been described, with the participation of a broad array of resistance mechanisms. The sensitive genotype exhibited the highest transcriptional plasticity, accounting for the wide range of potential adaptations to insecticides that this species can evolve. In contrast, the multiply resistant genotype exhibited a low transcriptional plasticity, even for the expression of genes encoding enzymes involved in insecticide detoxification. Our results emphasize the value of microarray studies to search for regulated genes in insects, but also highlights the many ways those different genotypes can assemble resistant phenotypes depending on the environmental pressure.

Show MeSH
Related in: MedlinePlus