Insight into molecular basis of plant-infecting arbovirus persistence in the vector

Read full article on ScienceDirect.

Conserved responses to viruses in insects

Text by Dorith Rotenberg, Kathleen Martin, and Anna Whitfield

Viruses that complete their replication cycles in two different eukaryotic hosts – culminating into vastly different physiological responses to infection – offer enticing questions about the nature of pathogenicity and immunity. One such plant virus, Maize mosaic rhabdovirus (MMV), depletes farmers’ pocketbooks in the tropical and subtropical regions of the globe. MMV relies exclusively on the corn planthopper, Peregrinus maidis, for transmission to plants. While MMV replicates in sensory-nervous, digestive and muscular systems, the virus has no apparent negative effect on vector health. To gain insight into host response and virus persistence in the insect, we deep-sequenced the transcriptomes of infected and non-infected adults and performed comparative sequence analyses with published data sets of other hopper-propagative plant virus systems. Our data revealed unique P. maidis responses to MMV and a core set of virus-responsive hopper genes, including those predicted to be transposable elements (TE), reverse transcriptases (RT), and innate immune genes (see figure).

The perturbation of TEs and RTs in response to MMV and other propagative hopper plant viruses like SRBSDV and MFSV, may point to the role of these proteins in maintaining persistent, non-pathogenic levels of plant viruses in their arthropod vectors. This hypothesis is not too unreasonable given that, in Aedes mosquitos that transmit dengue or chikungunya viruses, there is accumulating evidence that TEs and RTs generate virus-derived DNAs (Goic et al., 2016) that may be precursors to insect genome-incorporated viral sequence and subsequent production of small-interfering RNAs that keep virus levels in check. In the case of MMV, we postulate that virus persistence in the corn planthopper with no negative effect on fitness would increase the vector’s capacity to transmit virus to the primary host, the plant. Future work will focus on functional analysis of these exciting genes in planthoppers and leafhoppers infected with their virus partners.

Teasing out tripartite interactions, whether at the ecological or molecular level, is not without its challenges. In our experience with virus-vector molecular interaction studies, quality and age of virus inoculum (source plants), insect age, stage of development, sex, and time of virus exposure, can influence insect-to-insect variation in virus acquisition, accumulation, and inoculation efficiencies. Experimental and/or natural biological variation can be magnified with the sensitivity of quantitative RNA sequencing tools. This variation more than likely contributes to disconcordant repetitions of a transcriptome experiment, often resulting in messy data that is difficult to extract meaning from. To circumvent these lurking variables in our –omics research reported here, we conducted seven bio-repetitions of the acquisition step for drilling down on three for RNA sequencing, effectively choosing repetitions comprised of the same insect age, female-male sex ratio, and relative virus abundance. Reducing noise in the system to better resolve the influence of one variable on a particular response continues to motivate scientific rigor, however painstaking and lengthy the process.

Rotenberg blog figure square

 

Figure legend

Virus-responsive transcripts unique to Peregrinus maidis or shared with other virus-infected planthopper [Sogatella furcifera – Southern rice black-streaked dwarf virus (SRBSDV)] and leafhopper [Graminella nigrifrons – Maize fine streak virus (MFSV)] species. Indicated are the number and percentage of the 144 P. maidis transcripts that were differentially-expressed under infection with Maize mosaic rhabdovirus (MMV), and the number provisionally annotated as transposable element-related sequences and innate immunity-associated proteins. Peregrinus maidis photo taken by Ken Chamberlain at Ohio State Research and Development Center, courtesy of Margaret Redinbaugh, USDA-ARS CSWQRU.

Citation

Goic, B., Stapleford, K.A., Frangeul, L., Doucet, A.J., Gausson, V., Blanc, H., Schemmel-Jofre, N., Cristofari, G., Lambrechts, L., Vignuzzi, M., Saleh, M.C., 2016. Virus derived DNA drives mosquito vector tolerance to arboviral infection. Nat. Commun.7, 12410.

Introducing the authors

Authors_Rosenberg

Pictured (left to right) are Dorith Rotenberg (Associate Professor), Kathleen Martin (Postdoctoral Associate), and Anna Whitfield (Professor) at the Department of Entomology and Plant Pathology, North Carolina State University, USA.

About the research

Transcriptomic response of the insect vector, Peregrinus maidis, to Maize mosaic rhabdovirus and identification of conserved responses to propagative viruses in hopper vectors

Kathleen M. Martin, Karen Barandoc-Alviar, Derek J. Schneweis, Catherine L. Stewart, Dorith Rotenberg, Anna E. Whitfield

Virology, Volume 509, September 2017, Pages 71-81