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

Authors: CASSONE, B - The Ohio State University; MICHEL, A - The Ohio State University; Stewart, Lucy; BANSAL, R - The Ohio State University; Mian, Rouf; Redinbaugh, Margaret

Submitted to: Genome Biology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/20/2014
Publication Date: 4/6/2014
Publication URL: http://handle.nal.usda.gov/10113/59742
Citation: Cassone, B.J., Michel, A.P., Stewart, L.R., Bansal, R., Mian, R.M., Redinbaugh, M.G. 2014. Reduction in fecundity and shifts in cellular processes by a native virus on an invasive insect. Genome Biology and Evolution. 6(4):873-885.

Interpretive Summary: Virus diseases are most frequently transmitted to crops by insects, and aphids are among the most important insect vectors of viruses. The soybean aphid, a recently introduced and important pest of soybeans, can transmit several economically important viruses. By understanding interactions between the aphid, soybeans and viruses, we hope to identify critical mechanisms that can be disrupted for disease control. In this set of experiments we tested the response of soybean aphid to two viruses: one that the aphid transmits called Soybean mosaic virus (SMV); and, one that it can't transmit called Bean pod mottle virus (BPMV). Surprisingly, we found that aphids feeding on BPMV-infected soybeans reproduced at a lower rate than aphids feeding on healthy or SMV-infected soybean. Interestingly, gene expression changed much more dramatically in aphids feeding on BPMV-infected soybeans than on healthy or SMV-infected soybeans. The changes in gene expression in the aphids fed on BPMV-infected soybeans suggested the insects were decreasing their normal cellular activities and that they were defending themselves against an intracellular pathogen. However, we could not detect any multiplication of BPMV in the insect. Our results suggest that the soybean aphid is responding to something in the BPMV-infected plant. Because aphid reproduction is inhibited on BPMV-infected plants, further research to identify this component might allow development of unique pest control strategies.

Technical Abstract: Pathogens and their vectors have co-evolutionary histories that are intricately intertwined with their ecologies, environments and genetic interactions. The majority of non-persistently transmitted plant viruses are transmitted by aphid species. One important aphid vector in soybean-growing regions of North America is the soybean aphid, Aphis glycines, which transmits at least thirteen plant viruses. In this study we carried out fitness bioassays to examine any impacts on A. glycines survival and fecundity that were conferred by feeding on soybean infected with a virus it transmits (Soybean mosaic potyvirus) and does that it not transmit (Bean pod mottle comovirus). The genetic underpinnings of any observable changes in fitness phenotype were explored using RNA-Seq. Strikingly, feeding on BPMV-infected soybean elicited a large and persistent downregulation of A. glycines transcripts involved in regular cellular activities, and was coupled with significant reductions in aphid fecundity. Although molecular signatures suggested a Small Regulatory RNA pathway defense response is inactivated in aphids feeding on infected plants, BPMV is apparently not replicating in the vector. These results suggest a trade-off between the high energetic cost of parthenogenic reproduction versus the survival benefits of reducing reproduction and other core cellular processes in A. glycines fed on BPMV-infected plants. Ultimately, the inability of A. glycines to adapt to BPMV-infected plants may reflect the short tritrophic evolutionary histories between the insect, plant and virus.