The Capsid Protein of Satellite Panicum Mosaic Virus Contributes to Systemic Invasion and Interacts with Its Helper Virus

Abstract

Satellite panicum mosaic virus (SPMV) depends on its helper Panicum mosaic virus (PMV) for replication and spread in host plants. The SPMV RNA encodes a 17-kDa capsid protein (CP) that is essential for formation of its 16-nm virions. The results of this study indicate that in addition to the expression of the full-length SPMV CP from the 5-proximal AUG start codon, SPMV RNA also expresses a 9.4-kDa C-terminal protein from the third in-frame start codon. Differences in solubility between the full-length protein and its C-terminal product were observed. Subcellular fractionation of infected plant tissues showed that SPMV CP accumulates in the cytosol, cell wall-, and membrane-enriched fractions. However, the 9.4-kDa protein exclusively cofractionated with cell wall-and membrane-enriched fractions. Earlier studies revealed that the 5-untranslated region (5-UTR) from nucleotides 63 to 104 was associated with systemic infection in a host-specific manner in millet plants. This study shows that nucleotide deletions and insertions in the 5-UTR plus simultaneous truncation of the N-terminal part of the CP impaired SPMV spread in foxtail millet, but not in proso millet plants. In contrast, the expression of the full-length version of SPMV CP efficiently compensated the negative effect of the 5-UTR deletions in foxtail millet. Finally, immunoprecipitation assays revealed the presence of a specific interaction between the capsid proteins of SPMV and its helper virus (PMV). Our findings show that the SPMV CP has several biological functions, including facilitating efficient satellite virus infection and movement in millet plants.Satellite viruses and satellite nucleic acids (satellite RNAs and satellite DNAs) represent a group of subviral nucleic acid molecules that require a helper virus for replication and movement (30, 31). Satellite viruses differ from satellite RNAs and satellite DNAs in their capacity to direct translation of a cognate coat protein (capsid protein [CP]), a structural component required for RNA packaging via virion assembly. Satellite viruses do not share significant sequence similarity with their helper virus. However, specific recognition by the helper virusencoded proteins, such as the replicase and movement proteins, necessarily dictates the involvement of cis-acting elements on satellite virus RNA; secondary structures are possibly responsible for such interactions. To date, four satellite viruses have been characterized in plants in pair-specific relationships with a helper virus (8,30,31). A satellite virus in an invertebrate host has recently been reported as a coinfection with the virus of Macrobrachium rosenbergii, a nodavirus (36).Satellite panicum mosaic virus (SPMV) is completely dependent on its helper Panicum mosaic virus (PMV) (genus Panicovirus; family Tombusviridae) for replication as well as local and systemic spread in plants (29,33,34). There is no significant sequence similarity between SPMV and PMV (34). PMV virions encapsidate the positive-sense, single-stranded genomic RNA (3,19...

Characterization of a Viral Synergism in the MonocotBrachypodium distachyonReveals Distinctly Altered Host Molecular Processes Associated with Disease

“…The earlier detection of PMV CP in the mixed infections (E) is associated with SPMV enhancement of either PMV replication or movement, which is a component of the working definition of the SPMV-associated synergism (Scholthof, 1999). The asterisks represent lower molecular weight CPs, possibly produced from leaky scanning (Omarov et al, 2005) or posttranslational modifications. The Ponceau S-stained nitrocellulose membranes serve to indicate approximately equal protein loading among the sample lanes.…”

“…Our previous genetic and molecular characterization of PMV and SPMV in millets revealed multiple determinants of the synergism Turina et al, 2000;Scholthof, 2001, 2004;Omarov et al, 2005;Batten et al, 2006aBatten et al, , 2006bEverett et al, 2010). In the case of PMV+SPMV mixed infections, SPMV has the unusual feature of enhancing PMV accumulation in host plants, with a simultaneous increase in accumulation of PMV movement protein (P8) and exacerbation of symptoms on systemically infected (noninoculated) leaves compared with infections of PMV alone (Scholthof, 1999;Supplemental Fig.…”

Plant Immune Responses Against Viruses: How Does a Virus Cause Disease?

“…A peculiar feature of PMV is that it supports the replication of a satellite virus, SPMV, resulting in a viral synergism (Scholthof, 1999;Mandadi and Scholthof, 2012). As a complex, PMV+SPMV causes disease in the host plants characterized by exacerbated symptoms relative to those produced by PMV alone (Scholthof, 1999;Omarov et al, 2005). We are using this unique panicovirus complex as a foundational tool for fundamental advances in host-virus interactions, as well as potential translation to the field due to the distribution of PMV on agriculturally important crop hosts.…”

Mimicry of molecular pretenders: The terminal structures of satellites associated with plant RNA viruses

“…Many studies have been done on satellite panicum mosaic virus (SPMV) in recent years. The CP of SPMV has been shown to play a multifunctional role in the infection cycles of SPMV and Panicum mosaic virus (PMV), [76][77][78][79] and has been applied in the development of plant virus-based vectors to enhance the expression level of foreign genes. 80 The crystal structures of PMV and SPMV virions have also been resolved through X-ray crystallography analysis, 81,82 including the RNA structures within the SPMV virion.…”