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Reduction in fecundity and shifts in cellular processes by a native virus on an invasive insect.

Cassone BJ, Michel AP, Stewart LR, Bansal R, Mian MA, Redinbaugh MG - Genome Biol Evol (2014)

Bottom Line: Pathogens and their vectors have coevolutionary histories that are intricately intertwined with their ecologies, environments, and genetic interactions.The genetic underpinnings of the observed changes in fitness phenotype were explored using RNA-Seq.These results suggest that incompatibilities with BPMV or the effects of BPMV infection on soybean caused A. glycines to allot available energy resources to survival rather than reproduction and other core cellular processes.

View Article: PubMed Central - PubMed

Affiliation: USDA, ARS Corn, Soybean and Wheat Quality Research Unit, Wooster, Ohio.

ABSTRACT
Pathogens and their vectors have coevolutionary histories that are intricately intertwined with their ecologies, environments, and genetic interactions. The soybean aphid, Aphis glycines, is native to East Asia but has quickly become one of the most important aphid pests in soybean-growing regions of North America. In this study, we used bioassays to examine the effects of feeding on soybean infected with a virus it vectors (Soybean mosaic virus [SMV]) and a virus it does not vector (Bean pod mottle virus [BPMV]) have on A. glycines survival and fecundity. The genetic underpinnings of the observed changes in fitness phenotype were explored using RNA-Seq. Aphids fed on SMV-infected soybean had transcriptome and fitness profiles that were similar to that of aphids fed on healthy control plants. Strikingly, a significant reduction in fecundity was seen in aphids fed on BPMV-infected soybean, concurrent with a large and persistent downregulation of A. glycines transcripts involved in regular cellular activities. Although molecular signatures suggested a small regulatory RNA pathway defense response was repressed in aphids feeding on infected plants, BPMV did not appear to be replicating in the vector. These results suggest that incompatibilities with BPMV or the effects of BPMV infection on soybean caused A. glycines to allot available energy resources to survival rather than reproduction and other core cellular processes. Ultimately, the detrimental impacts to A. glycines may reflect the short tritrophic evolutionary histories between the insect, plant, and virus.

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Survival (A) and fecundity (B) of Aphis glycines adult after feeding on BPMV-infected (white), SMV-infected (dark gray), or healthy control (light gray) soybean for 7 days. Error bars indicate standard deviation variation between ten replicates per treatment/fitness parameter.
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evu057-F1: Survival (A) and fecundity (B) of Aphis glycines adult after feeding on BPMV-infected (white), SMV-infected (dark gray), or healthy control (light gray) soybean for 7 days. Error bars indicate standard deviation variation between ten replicates per treatment/fitness parameter.

Mentions: Differences in survival rates and fecundity were assessed among A. glycines fed on SMV-infected, BPMV-infected, and healthy soybean for 7 days. A total of 300 aphids were bioassayed per treatment across ten biological replicates harvested from different cohorts (fig. 1). Fecundity was significantly lower in aphids fed on BPMV-infected soybean (P < 0.001) compared with aphids in the other treatments. No dead offspring were found on the enclosed trifoliates after 7 days for any treatment. Reduced fecundity in the BPMV treatment did not appear due to a smaller pool of aphids available to produce offspring, as adult survival was not significantly different between treatments (P > 0.05). Across all replicates, aphids feeding on BPMV-infected soybean produced about half as many viable offspring after 7 days as those feeding on SMV-infected or healthy plants.Fig. 1.—


Reduction in fecundity and shifts in cellular processes by a native virus on an invasive insect.

Cassone BJ, Michel AP, Stewart LR, Bansal R, Mian MA, Redinbaugh MG - Genome Biol Evol (2014)

Survival (A) and fecundity (B) of Aphis glycines adult after feeding on BPMV-infected (white), SMV-infected (dark gray), or healthy control (light gray) soybean for 7 days. Error bars indicate standard deviation variation between ten replicates per treatment/fitness parameter.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC4007533&req=5

evu057-F1: Survival (A) and fecundity (B) of Aphis glycines adult after feeding on BPMV-infected (white), SMV-infected (dark gray), or healthy control (light gray) soybean for 7 days. Error bars indicate standard deviation variation between ten replicates per treatment/fitness parameter.
Mentions: Differences in survival rates and fecundity were assessed among A. glycines fed on SMV-infected, BPMV-infected, and healthy soybean for 7 days. A total of 300 aphids were bioassayed per treatment across ten biological replicates harvested from different cohorts (fig. 1). Fecundity was significantly lower in aphids fed on BPMV-infected soybean (P < 0.001) compared with aphids in the other treatments. No dead offspring were found on the enclosed trifoliates after 7 days for any treatment. Reduced fecundity in the BPMV treatment did not appear due to a smaller pool of aphids available to produce offspring, as adult survival was not significantly different between treatments (P > 0.05). Across all replicates, aphids feeding on BPMV-infected soybean produced about half as many viable offspring after 7 days as those feeding on SMV-infected or healthy plants.Fig. 1.—

Bottom Line: Pathogens and their vectors have coevolutionary histories that are intricately intertwined with their ecologies, environments, and genetic interactions.The genetic underpinnings of the observed changes in fitness phenotype were explored using RNA-Seq.These results suggest that incompatibilities with BPMV or the effects of BPMV infection on soybean caused A. glycines to allot available energy resources to survival rather than reproduction and other core cellular processes.

View Article: PubMed Central - PubMed

Affiliation: USDA, ARS Corn, Soybean and Wheat Quality Research Unit, Wooster, Ohio.

ABSTRACT
Pathogens and their vectors have coevolutionary histories that are intricately intertwined with their ecologies, environments, and genetic interactions. The soybean aphid, Aphis glycines, is native to East Asia but has quickly become one of the most important aphid pests in soybean-growing regions of North America. In this study, we used bioassays to examine the effects of feeding on soybean infected with a virus it vectors (Soybean mosaic virus [SMV]) and a virus it does not vector (Bean pod mottle virus [BPMV]) have on A. glycines survival and fecundity. The genetic underpinnings of the observed changes in fitness phenotype were explored using RNA-Seq. Aphids fed on SMV-infected soybean had transcriptome and fitness profiles that were similar to that of aphids fed on healthy control plants. Strikingly, a significant reduction in fecundity was seen in aphids fed on BPMV-infected soybean, concurrent with a large and persistent downregulation of A. glycines transcripts involved in regular cellular activities. Although molecular signatures suggested a small regulatory RNA pathway defense response was repressed in aphids feeding on infected plants, BPMV did not appear to be replicating in the vector. These results suggest that incompatibilities with BPMV or the effects of BPMV infection on soybean caused A. glycines to allot available energy resources to survival rather than reproduction and other core cellular processes. Ultimately, the detrimental impacts to A. glycines may reflect the short tritrophic evolutionary histories between the insect, plant, and virus.

Show MeSH
Related in: MedlinePlus