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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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Transcriptional responses in three Myzus persicae genotypes (S, SR and MR) subjected to a pirimicarb.Volcano plots for each genotype show the log2 fold change (x axis) and the statistical significance (y axis) between the controls and treatments. Vertical lines indicate 2-fold expression difference in either direction (−1>log2FC>1). Horizontal line indicates significance threshold (P<0.05). Statistical analysis is based on a Bayesian inference using a lineal model, and reflects both biological and technical replications. Genes showing both 2-fold differential expression and a significant P value are colored. Not all labels appear in the S, SR and MR volcano plot in order to preserve readability (see Table 2 and supporting material for a full listing of significantly over-expressed genes). Gene abbreviations: 1, glutathione s-transferase; 2, cytochrome p450 family CYP6CYP3; 3, carboxylesterase type FE4; 4, cathepsin b; 5, cytochrome p450 family CYP6; 6, cuticle protein; 7, salivary peptide; 8, ABC transporter; 9, glucose transporter; 10, cytochrome p450; 11, heat shock protein 70; 12, heterotrimeric guanine nucleotide-binding protein; 13, histone h3 methyltransferase, 14, eukaryotic initiation factor; 15, unknown protein.
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pone-0036366-g001: Transcriptional responses in three Myzus persicae genotypes (S, SR and MR) subjected to a pirimicarb.Volcano plots for each genotype show the log2 fold change (x axis) and the statistical significance (y axis) between the controls and treatments. Vertical lines indicate 2-fold expression difference in either direction (−1>log2FC>1). Horizontal line indicates significance threshold (P<0.05). Statistical analysis is based on a Bayesian inference using a lineal model, and reflects both biological and technical replications. Genes showing both 2-fold differential expression and a significant P value are colored. Not all labels appear in the S, SR and MR volcano plot in order to preserve readability (see Table 2 and supporting material for a full listing of significantly over-expressed genes). Gene abbreviations: 1, glutathione s-transferase; 2, cytochrome p450 family CYP6CYP3; 3, carboxylesterase type FE4; 4, cathepsin b; 5, cytochrome p450 family CYP6; 6, cuticle protein; 7, salivary peptide; 8, ABC transporter; 9, glucose transporter; 10, cytochrome p450; 11, heat shock protein 70; 12, heterotrimeric guanine nucleotide-binding protein; 13, histone h3 methyltransferase, 14, eukaryotic initiation factor; 15, unknown protein.

Mentions: Microarray experiments were performed in order to study the transcriptome responses in three M. persicae genotypes (S, SR and MR) subjected to a dose of pirimicarb. Microarray analysis detected a high variation in transcriptional responses among genotypes. Global gene expression changes are shown in Figure 1 in the form of volcano plots, with threshold of 2-fold-change and a significance threshold of p<0.05. Thus, 183, 17 and 7 genes were significantly up-regulated in S, SR and RM genotypes, respectively. (see Table S1 for the full list of up-regulated genes). Interestingly, the number of down-regulated genes was inverse to the number of up-regulated genes in each genotype. Thus, 17, 28 and 78 genes were significantly down-regulated in S, SR and RM genotypes, respectively. Of the 183 up-regulated genes found in S genotype, 151 had known functions and 51 are potential candidates for being involved in insecticide resistance, including genes encoding for abc transporters, heat shock proteins, cathepsins, cuticle proteins, cytochrome P450s, a carboxylesterase E4/FE4 and glutathione-S-transferases, among others (see some of these genes in Table 2). Of the 17 up-regulated genes in the SR genotype, 12 have known functions and are potentially involved in insecticide resistance, including heat shock proteins, cathepsins, cuticle proteins and cytochrome P450s (Table 3). Finally, of the 7 up-regulated genes in the MR genotype, 3 have unknown functions while the other 4 genes included a histone h3 methyltransferase and a guanine nucleotide-binding protein (Table 4).


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)

Transcriptional responses in three Myzus persicae genotypes (S, SR and MR) subjected to a pirimicarb.Volcano plots for each genotype show the log2 fold change (x axis) and the statistical significance (y axis) between the controls and treatments. Vertical lines indicate 2-fold expression difference in either direction (−1>log2FC>1). Horizontal line indicates significance threshold (P<0.05). Statistical analysis is based on a Bayesian inference using a lineal model, and reflects both biological and technical replications. Genes showing both 2-fold differential expression and a significant P value are colored. Not all labels appear in the S, SR and MR volcano plot in order to preserve readability (see Table 2 and supporting material for a full listing of significantly over-expressed genes). Gene abbreviations: 1, glutathione s-transferase; 2, cytochrome p450 family CYP6CYP3; 3, carboxylesterase type FE4; 4, cathepsin b; 5, cytochrome p450 family CYP6; 6, cuticle protein; 7, salivary peptide; 8, ABC transporter; 9, glucose transporter; 10, cytochrome p450; 11, heat shock protein 70; 12, heterotrimeric guanine nucleotide-binding protein; 13, histone h3 methyltransferase, 14, eukaryotic initiation factor; 15, unknown protein.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0036366-g001: Transcriptional responses in three Myzus persicae genotypes (S, SR and MR) subjected to a pirimicarb.Volcano plots for each genotype show the log2 fold change (x axis) and the statistical significance (y axis) between the controls and treatments. Vertical lines indicate 2-fold expression difference in either direction (−1>log2FC>1). Horizontal line indicates significance threshold (P<0.05). Statistical analysis is based on a Bayesian inference using a lineal model, and reflects both biological and technical replications. Genes showing both 2-fold differential expression and a significant P value are colored. Not all labels appear in the S, SR and MR volcano plot in order to preserve readability (see Table 2 and supporting material for a full listing of significantly over-expressed genes). Gene abbreviations: 1, glutathione s-transferase; 2, cytochrome p450 family CYP6CYP3; 3, carboxylesterase type FE4; 4, cathepsin b; 5, cytochrome p450 family CYP6; 6, cuticle protein; 7, salivary peptide; 8, ABC transporter; 9, glucose transporter; 10, cytochrome p450; 11, heat shock protein 70; 12, heterotrimeric guanine nucleotide-binding protein; 13, histone h3 methyltransferase, 14, eukaryotic initiation factor; 15, unknown protein.
Mentions: Microarray experiments were performed in order to study the transcriptome responses in three M. persicae genotypes (S, SR and MR) subjected to a dose of pirimicarb. Microarray analysis detected a high variation in transcriptional responses among genotypes. Global gene expression changes are shown in Figure 1 in the form of volcano plots, with threshold of 2-fold-change and a significance threshold of p<0.05. Thus, 183, 17 and 7 genes were significantly up-regulated in S, SR and RM genotypes, respectively. (see Table S1 for the full list of up-regulated genes). Interestingly, the number of down-regulated genes was inverse to the number of up-regulated genes in each genotype. Thus, 17, 28 and 78 genes were significantly down-regulated in S, SR and RM genotypes, respectively. Of the 183 up-regulated genes found in S genotype, 151 had known functions and 51 are potential candidates for being involved in insecticide resistance, including genes encoding for abc transporters, heat shock proteins, cathepsins, cuticle proteins, cytochrome P450s, a carboxylesterase E4/FE4 and glutathione-S-transferases, among others (see some of these genes in Table 2). Of the 17 up-regulated genes in the SR genotype, 12 have known functions and are potentially involved in insecticide resistance, including heat shock proteins, cathepsins, cuticle proteins and cytochrome P450s (Table 3). Finally, of the 7 up-regulated genes in the MR genotype, 3 have unknown functions while the other 4 genes included a histone h3 methyltransferase and a guanine nucleotide-binding protein (Table 4).

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