Wheat streak mosaic virus alters the transcriptome of its vector, wheat curl mite (Aceria tosichella Keifer), to enhance mite development and population expansion

Authors: GUPTAR, ADARSH - University Of Nebraska; Scully, Erin; Palmer, Nathan - Nate; Geib, Scott; Sarath, Gautam; HEIN, GARY - University Of Nebraska; Tatineni, Satyanarayana - Ts

Submitted to: Journal of General Virology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/14/2019
Publication Date: 5/1/2019
Citation: Guptar, A.K., Scully, E.D., Palmer, N.A., Geib, S.M., Sarath, G., Hein, G.L., Tatineni, S. 2019. Wheat streak mosaic virus alters the transcriptome of its vector, wheat curl mite (Aceria tosichella Keifer), to enhance mite development and population expansion. Journal of General Virology. 100(5):889-910. https://doi.org/10.1099/jgv.0.001256.
DOI: https://doi.org/10.1099/jgv.0.001256

Interpretive Summary: Wheat streak mosaic virus (WSMV) is one of the most damaging pathogens to wheat in the Great Plains as it can cause yield losses up to 100%. This virus is transmitted exclusively by the wheat curl mite (WCM, Aceria tosichella Keifer), which can reach quickly high population densities in the field and can transmit many other viruses in addition to WSMV, such as High Plains wheat mosaic emaravirus, Brome streak mosaic rymovirus, and Triticum mosaic poacevirus. In the case of WSMV, acquisition of this virus directly alters the biology and behavior of WCM in order to facilitate and expedite viral transmission by increasing reproduction and population levels, expediting maturation to adulthood, and increasing feeding rates. In order understand how WSMV alters the physiology of WCM, we compared gene expression levels in infected and uninfected mites. Overall, lower expression levels of genes linked to development and immunity were observed in infected WCMs. This study allows us to determine how WSMV manipulates WCM to increase viral transmission rates and will ultimately allow us to design better prevention and control tactics to reduce wheat infection rates and yield losses in the field.

Technical Abstract: Wheat streak mosaic virus (WSMV; genus Tritimovirus; family Potyviridae) is an economically important virus on wheat transmitted by the wheat curl mite (WCM), Aceria tosichella Keifer, in a persistent propagative manner. Viral persistence and virus-vector coevolution may potentially influence vector gene expression in order to prolong viral association and thus, increase its transmission efficiency. In order to understand the transcriptomic responses of WCM to WSMV, RNA sequencing was performed using Illumina HiSeq sequencing platform to generate differential transcriptomes of WSMV-viruliferous and aviruliferous mites. Among 7,785 de novo-assembled unigenes, 1,513 were differentially-expressed in viruliferous WCMs and were categorized into 251 different gene ontology terms. The majority of these unigenes were downregulated in viruliferous mites in comparison to only a few unigenes that were upregulated. PFAM and KEGG enrichment analyses revealed that the majority of the downregulated unigenes coded for enzymes and proteins linked to stress-response, immunity, and development, such as juvenile hormone binding protein, heat shock proteins, glutathione S-transferases, trypsins, aspartyl proteases, cuticle proteins, and cathepsin propeptide inhibitors. Overall, these transcriptional changes may inhibit WCM immune response to prolong viral association and alter WCM development to expedite population expansion, both of which could enhance viral transmission.