Reduction in Fecundity and Shifts in Cellular Processes by a Native Virus on an Invasive Insect

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.

Shifts inBuchnera aphidicoladensity in soybean aphids (Aphis glycines) feeding on virus-infected soybean

“…While the factors governing the temporal differences in the onset of diminished fecundity between the virus‐infected treatments are unknown, a potential molecular signature could be observed in the aphid transcriptional profiles of Cassone et al . (). In that study, the downregulation of the transcriptome and associated significant reduction in fecundity were detected considerably earlier in the BPMV treatment.…”

“…We initially hypothesized that aphid host feeding on BPMV‐infected soybean detrimentally impacted Buchnera , which in turn altered aphid fecundity. Our previous study indicated Buchnera density was lower in aphids fed on both BPMV‐infected and SMV‐infected soybean but decreased fecundity was only detected in the BPMV treatment (Cassone et al ., ); however, by extending the fitness assays to include an additional 10‐day period, reductions in fecundity were also evident in the aphids feeding on SMV‐infected plants. While the factors governing the temporal differences in the onset of diminished fecundity between the virus‐infected treatments are unknown, a potential molecular signature could be observed in the aphid transcriptional profiles of Cassone et al .…”

“…The 2‐day feeding period on healthy soybean was sufficient to clear the insect gut of either virus (Cassone et al . ). The collections were carried out identically to the method used by Cassone et al .…”

“…The collections were carried out identically to the method used by Cassone et al . (). Briefly, 480 newborn apterous aphids (<12 h old) were randomly selected in equal numbers from four maintenance cages.…”

“…This includes changes to the phloem sap components, such as the nutritional substances, toxins and miRNAs (Tu et al, 2013). In turn, feeding on virusinfected plants can dramatically alter the fitness of their phloem-sucking insect pests (Rubinstein and Czosnek 1997;Guo et al, 2010;Cassone et al, 2014a;Xu et al, 2014). Given the integral role some symbionts play in nutrient synthesis for their insect hosts, including Buchnera in aphids, modifications to the phloem sap components of virus-infected plants could dramatically impact the insect host symbiont profiles and in turn affect host plant utilization.…”