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Title: An eriophyid mite-transmitted plant virus contains eight genomic RNA segments with unusual heterogeneity in the nucleocapsid protein

Author
item Tatineni, Satyanarayana - Ts
item MCMECHAN, ANTHONY - University Of Nebraska
item WOSULA, EVERLYNE - University Of Nebraska
item WEGULO, STEPHEN - University Of Nebraska
item Graybosch, Robert
item French, Roy
item HEIN, GARY - University Of Nebraska

Submitted to: Journal of Virology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/28/2014
Publication Date: 10/18/2014
Citation: Tatineni, S., Mcmechan, A.J., Wosula, E.N., Wegulo, S.N., Graybosch, R.A., French, R.C., Hein, G.L. 2014. An eriophyid mite-transmitted plant virus contains eight genomic RNA segments with unusual heterogeneity in the nucleocapsid protein. Journal of Virology. Journal of Virology 88: 11834-11845.

Interpretive Summary: High Plains disease, an economically important disease of wheat and maize, was first described in the Great Plains region of the United States in 1993-94. Disease diagnosis, tracking and control are difficult as Wheat mosaic virus (WMoV), the causal organism of High Plains disease, has been incompletely characterized. To date, complete genome sequence has not been available. In this study, we determined the complete genome sequence of WMoV and found it consists of eight genomic RNA molecules packaged together within one viral protein coat. Significant sequence polymorphism was found in the RNA encoding the nucleocapsid (coat) protein but not in the additional genomic RNA segments. These findings suggest that nucleocapsid protein-based diagnostic methods will be unreliable. Immunological - or nucleic acid PCR-based diagnostic methods using information from other proteins or genomic RNAs will be necessary for reliable detection of WMoV isolates. Additionally, heterogeneity in the coat-protein coding RNA 3 molecule suggests that WMoV isolates may easily overcome coat-protein-based resistance strategies. The availability of WMoV genome sequence facilitates the examination of gene function and virus diversity and the development of effective diagnostic methods and management strategies for an economically important but poorly understood virus.

Technical Abstract: Eriophyid mite-transmitted, multipartite, negative-sense plant RNA viruses with membrane-bound spherical virions are classified in the genus Emaravirus. The relatively dissimilar emaraviruses evolved with 4 to 6 genomic RNAs with one open reading frame (ORF) in each genomic RNA segment. We report here the eriophyid mite-transmitted Wheat mosaic virus (WMoV), the causal agent of High Plains disease of wheat and maize, encodes eight genomic RNA segments, the largest number of genomic RNAs in a known negative-sense RNA plant virus. Remarkably, two RNA 3 consensus sequences, encoding the nucleocapsid protein, were found with 12.5% sequence divergence, while no heterogeneity was found in the consensus sequences of the additional genomic RNA segments. The RNA-dependent RNA polymerase, glycoprotein precursor, nucleocapsid and P4 proteins of WMoV exhibited limited sequence homology with the ortholog proteins of other emaraviruses, while proteins encoded by additional genomic RNA segments displayed no significant homology with reported proteins in GenBank, suggesting that the Emaravirus genus further evolved with a divergent octapartite genome. Furthermore, the virus- and virus complementary (vc)-sense genomic RNAs of WMoV were accumulated asymmetrically in infected wheat with 10- to 20-fold more accumulation of virus-sense genomic RNAs compared to those of vc-sense RNAs. These data further confirming the octapartite negative-sense polarity nature of the WMoV genome. In WMoV-infected wheat, subgenomic-length mRNAs of vc-sense were detected for the genomic RNAs 3, 4, 7 and 8 but not for other RNA species, suggesting that the ORFs present in the vc-sense genomic RNAs are expressed through genomic- or subgenomic-length vc-sense mRNAs.