An Eriophyid Mite-Transmitted Plant Virus Contains Eight Genomic RNA Segments with Unusual Heterogeneity in the Nucleocapsid Protein

Abstract

Eriophyid mite-transmitted, multipartite, negative-sense RNA plant viruses with membrane-bound spherical virions are classified in the genus Emaravirus. We report here that the eriophyid mite-transmitted Wheat mosaic virus (WMoV), an Emaravirus, contains eight genomic RNA segments, the most 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 observed in the consensus sequences of additional genomic RNA segments. The RNA-dependent RNA polymerase, glycoprotein precursor, nucleocapsid, and P4 proteins of WMoV exhibited limited sequence homology with the orthologous proteins of other emaraviruses, while proteins encoded by additional genomic RNA segments displayed no significant homology with proteins reported in GenBank, suggesting that the genus Emaravirus evolved further with a divergent octapartite genome. Phylogenetic analyses revealed that WMoV formed an evolutionary link between members of the Emaravirus genus and the family Bunyaviridae. Furthermore, genomic-length virus-and virus-complementary (vc)-sense strands of all WMoV genomic RNAs accumulated asymmetrically in infected wheat, with 10-to 20-fold more virus-sense genomic RNAs than vc-sense RNAs. These data further confirm the octapartite negative-sense polarity of the WMoV genome. In WMoV-infected wheat, subgenomic-length mRNAs of vc sense were detected for genomic RNAs 3, 4, 7, and 8 but not for other RNA species, suggesting that the open reading frames present in the complementary sense of genomic RNAs are expressed through subgenomic-or near-genomic-length vc-sense mRNAs. IMPORTANCEWheat mosaic virus (WMoV), an Emaravirus, is the causal agent of High Plains disease of wheat and maize. In this study, we demonstrated that the genome of WMoV comprises eight negative-sense RNA segments with an unusual sequence polymorphism in an RNA encoding the nucleocapsid protein but not in the additional genomic RNA segments. WMoV proteins displayed weak or no homology with reported emaraviruses, suggesting that the genus Emaravirus further evolved with a divergent octapartite genome. The current study also examined the profile of WMoV RNA accumulation in wheat and provided evidence for the synthesis of subgenomic-length mRNAs of virus complementary sense. This is the first report to demonstrate that emaraviruses produce subgenomic-length mRNAs that are most likely utilized for genome expression. Importantly, this study facilitates the examination of gene functions and virus diversity and the development of effective diagnostic methods and management strategies for an economically important but poorly understood virus. E riophyid mite-transmitted, multipartite single-stranded RNA plant viruses with negative polarity recently were classified in the genus Emaravirus (1). The Emaravirus virions are membranebound particles of 80 to 200 nm in diameter, resembling those of Tospovirus. Members of the genus Emaravirus possess four...

Newly identified RNAs of raspberry leaf blotch virus encoding a related group of proteins

“…RLBV, FMV, PPSMV, PPSMV 2 and HPWMoV have been shown to encode a 'P5' protein of between 55 and 59 kDa, and HPWMoV P6 is also of this size. Indeed, HPWMoV P5 has low but detectable amino acid sequence similarity to the RLBV, FMV and PPSMV P5 proteins (Tatineni et al, 2014); however, their sequences provide no information about the possible function of any of these proteins.…”

“…Other, tentative, members of the genus Emaravirus are Pigeonpea sterility mosaic virus (PPSMV), Pigeonpea sterility mosaic virus 2 (PPSMV 2), Redbud yellow ringspot-associated virus (RYRSaV), High Plains wheat mosaic virus (HPWMoV), Wooly burdock yellow vein virus (WBYVV), Viburnum line pattern-associated virus (VibLPaV) and Blackberry leaf mottle-associated virus (BLMaV). Although not all of these viruses have been studied in the same detail, they all have multi-segmented genomes of (probably) negative-strand RNA, some are known to have roughly spherical particles enclosed in a double-membrane envelope and all have similarity in the amino acid sequences of some of their encoded proteins (Ebrahim-Nesbat & Izadpanah, 1992;Elbeaino et al, 2009Elbeaino et al, , 2014Elbeaino et al, , 2015Laney et al, 2011;Sabanadzovic & Abou Ghanem-Sabanadzovic, 2011;Bi et al, 2012;Ishikawa et al, 2012;Tatineni et al, 2014). Other shared attributes are their transmission between plants by eriophyid mites (Mielke-Ehret & Mühlbach, 2012), and the presence of short conserved, imperfectly repeated nucleotide sequences at the 59 and 39 termini of the viral RNAs.…”

“…Currently, HPWMoV has the largest known emaravirus genome, comprising eight RNAs (RNA1-8) together with an additional variant version of RNA3 (3B), encoding a NC protein with 11 % amino acid differences to the NC encoded by RNA3A (Tatineni et al, 2014). Six RNAs have been reported for FMV and PPSMV 2, five for PPSMV, and four for RRV, although it is likely that more RNAs remain to be discovered for these viruses.…”

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Differential Transmission of Two Isolates ofWheat streak mosaic virusby Five Wheat Curl Mite Populations

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