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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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Related in: MedlinePlus

Distribution of GO IDs at the 2nd level.Based on their participation in biological processes (A) and molecular functions (B) of up-regulated ESTs (putative proteins) in a sensitive genotype (S) of Myzus persicae treated with pirimicarb. Out of 97 annotated EST sequences, 69 presented GO IDs for biological processes and 88 for molecular functions.
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pone-0036366-g003: Distribution of GO IDs at the 2nd level.Based on their participation in biological processes (A) and molecular functions (B) of up-regulated ESTs (putative proteins) in a sensitive genotype (S) of Myzus persicae treated with pirimicarb. Out of 97 annotated EST sequences, 69 presented GO IDs for biological processes and 88 for molecular functions.

Mentions: A total of 97 sequences of 183 up-regulated genes in the S genotype were annotated. Gene Ontology (GO) graphs were constructed using percentages of 2nd level GO terms and presented in Figure 3 under biological processes (BP) and molecular functions (MF). GO analysis revealed the participation of 69 putative proteins in 14 BP (Figure 3A). Among them, metabolic processes were the most represented with 49 gene products (25%) involved in primary metabolic processes (protein localization, carbohydrate and lipid biosynthetic and catabolic process, ATP and nucleotide biosynthetic process), cellular metabolic process (including the generation of precursors metabolites and energy) and oxidation reduction processes among others. The second largest represented group corresponded to putative proteins encoded by 40 genes (21%) and involved in cellular processes such as organelle organization, actin filament-based processes, microtubule-based processes, cell division, cytoplasm organization and cell communication. Under the category of molecular functions (MF), 88 gene products were involved in 6 different activities (some in more than one category) (Figure 3B). Most sequences (60 gene products) were related to catalytic activity; among them, the 44% corresponded to hydrolase activity (GO terms associated with esterase and cathepsins), 26% to transferase activity (GO terms associated with glutathione-S-transferase) and 16% to oxidoreductase activity (GO terms associated with cytochrome P450s).


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)

Distribution of GO IDs at the 2nd level.Based on their participation in biological processes (A) and molecular functions (B) of up-regulated ESTs (putative proteins) in a sensitive genotype (S) of Myzus persicae treated with pirimicarb. Out of 97 annotated EST sequences, 69 presented GO IDs for biological processes and 88 for molecular functions.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0036366-g003: Distribution of GO IDs at the 2nd level.Based on their participation in biological processes (A) and molecular functions (B) of up-regulated ESTs (putative proteins) in a sensitive genotype (S) of Myzus persicae treated with pirimicarb. Out of 97 annotated EST sequences, 69 presented GO IDs for biological processes and 88 for molecular functions.
Mentions: A total of 97 sequences of 183 up-regulated genes in the S genotype were annotated. Gene Ontology (GO) graphs were constructed using percentages of 2nd level GO terms and presented in Figure 3 under biological processes (BP) and molecular functions (MF). GO analysis revealed the participation of 69 putative proteins in 14 BP (Figure 3A). Among them, metabolic processes were the most represented with 49 gene products (25%) involved in primary metabolic processes (protein localization, carbohydrate and lipid biosynthetic and catabolic process, ATP and nucleotide biosynthetic process), cellular metabolic process (including the generation of precursors metabolites and energy) and oxidation reduction processes among others. The second largest represented group corresponded to putative proteins encoded by 40 genes (21%) and involved in cellular processes such as organelle organization, actin filament-based processes, microtubule-based processes, cell division, cytoplasm organization and cell communication. Under the category of molecular functions (MF), 88 gene products were involved in 6 different activities (some in more than one category) (Figure 3B). Most sequences (60 gene products) were related to catalytic activity; among them, the 44% corresponded to hydrolase activity (GO terms associated with esterase and cathepsins), 26% to transferase activity (GO terms associated with glutathione-S-transferase) and 16% to oxidoreductase activity (GO terms associated with cytochrome P450s).

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