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Nucleotide Sequence and Infectivity of a Full-Length Cdna Clone of Panicum Mosaic Virus

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Nucleotide Sequence and Infectivity of a Full-Length Cdna Clone of Panicum Mosaic Virus VIROLOGY 241, 141±155 (1998) ARTICLE NO. VY978939 Nucleotide Sequence and Infectivity of a Full-Length cDNA Clone of Panicum Mosaic Virus Massimo Turina,1 Miko Maruoka,*,2 Judit Monis,*,3 A. O. Jackson,* and Karen-Beth G. Scholthof4 Department of Plant Pathology and Microbiology, Texas A&M University, College Station, Texas 77843; and *Department of Plant and Microbial Biology, University of California, Berkeley, California 94720 Received September 4, 1997; returned to author for revision October 2, 1997; accepted November 9, 1997 The sequence of an infectious cDNA clone of panicum mosaic virus (PMV) showed that the single-stranded RNA genome is 4326 nucleotides (nt) and a single highly abundant subgenomic (sg) RNA of 1475 nt was synthesized during PMV infection of pearl millet plants and protoplasts. Computer comparisons revealed strong similarities between the predicted amino acid sequences of the p48 and p112 open reading frames (ORFs) and replicase proteins of members of the Tombusviridae. The sgRNA has the potential to encode five proteins. Three small ORFs, p8, p8-FS, and/or p6.6 have similarity to ORFs of carmo-, necro-, and machlomoviruses thought to be involved in virus spread in plants. The sgRNA also has the potential to encode a 26-kDa capsid protein and a 15-kDa nested gene (p15) of unknown function. PMV transcripts also supported replication and movement of SPMV, the satellite virus. Genome organization, physicochemical properties, and biological features indicate that PMV is a member of the Tombusviridae family. However, PMV differs sufficiently from previously described members to warrant its placement in a new genus provisionally designated Panicovirus. © 1998 Academic Press INTRODUCTION reported on centipedegrass (Eremochloa ophiuroides)in Florida, Louisiana, Arkansas, Mississippi, North Caro- Panicum mosaic virus (PMV) is a 30-nm icosahedral lina, and South Carolina (Haygood and Barnett, 1992). monopartite plant virus composed of a plus sense sin- The causal agent was characterized as a mixed infection gle-stranded RNA genome of approximately 4300 nucle- of a strain of PMV and a satellite virus (SPMV) that otides (nt) and a 26-kilodalton (kDa) capsid protein (CP) depends on PMV for movement and replication, but en- (Buzen et al., 1984; Masuta et al., 1987). The host range codes its own capsid protein (Buzen et al., 1984; Niblett of PMV is restricted to a few grass species (Niblett and et al., 1977). Depending on the host plant, PMV or mixed Paulsen, 1975; Niblett et al., 1977; Sill and Pickett, 1957), infections of PMV and SPMV can elicit a chlorotic mottle, where it typically causes a systemic mosaic. PMV was stunting, and seed reductions in forage grasses. During first reported on switchgrass (Panicum virgatum)inKan- the warm summer months, severe symptoms develop in sas in 1953 (Sill and Pickett, 1957) and was recently infected St. Augustinegrass (Dale and McDaniel, 1982). confirmed in breeding plots in Oklahoma (K.-B. G. Thus far, a biological vector has not been identified, but Scholthof, unpublished observations). Several serologi- infections can be spread by virus-contaminated lawn- cal variants of PMV have been described on St. Au- mower blades and from infected St. Augustinegrass gustinegrass (Stenotaphrum secundatum) (Holcomb et plugs or sod (Haygood and Barnett, 1992; Holcomb et al., al., 1972). In the mid-1960s, a virus disease named ``St. 1989). In the laboratory and under natural field condi- Augustine decline'' became so severe in the Lower Rio tions, PMV can support the replication of SPMV (Buzen et Grande Valley that it limited the production, mainte- al., 1984; Masuta et al., 1987) and at least two satellite nance, and establishment of St. Augustinegrass in Texas RNAs (satRNAs). The complete nucleotide sequence of (McCoy et al., 1969). A similar disease has since been two strains of SPMV have previously been determined (Berger et al., 1994; Masuta et al., 1987). The taxonomy of small isometric viruses infecting the The nucleotide sequence data reported in this paper have been Poaceae is complex, and their characterization has been submitted to the GenBank nucleotide sequence database and as- based primarily on serological relationships. In addition signed Accession No. U55002. 1 Present address: Istituto di Patologia Vegetale, Via Filippo Re 8, to PMV isolates in North America, a serological analysis 40126 Bologna, Italy. of 17 isolates of monopartite single-stranded RNA vi- 2 Present address: Genentech, 1 DNA Way, South San Francisco, CA ruses with icosahedral particles from various species of 94080. Poaceae in Europe revealed that PMV and molinia streak 3 Present address: Agritope, 8505 SW Creekside Place, Beaverton, virus (MSV) are related (Huth et al., 1974; Paul et al., OR 97005. 4 To whom correspondence and reprint requests should be ad- 1980). Furthermore, MSV is able to support the replica- dressed. Fax: (409) 845-6483. E-mail: [email protected]. tion of SPMV (Buzen et al., 1984). The sequence analysis 0042-6822/98 $25.00 141 Copyright © 1998 by Academic Press All rights of reproduction in any form reserved. 142 TURINA ET AL. Analysis of the PMV RNA sequence The complete sequence of PMV reveals several un- usual features of the 4326-nt genome. Among these is that PMV RNA has the potential to encode seven pro- teins (Figs. 3 and 5). Sequence analyses of PMV cDNAs indicate that if all seven ORFs are expressed in vivo, the virus uses a variety of translational control mechanisms for the expression of its genes, including translational readthrough, a ribosomal frameshift, leaky scanning, a noncanonical translational start site, and possibly one or more internal ribosomal entry sites. FIG. 1. Alignment of the cDNA clones derived from PMV genomic RNA. The plasmids pHindIII-PMV-59, pM1, pPMV3, pPMV7, pPMV10, pPMV12, pPMV13, pPMV17, pPMV18, and pPMV21 are aligned along The 59 nontranslated leader sequence the 4326-nt PMV genome. Unique restriction enzymes sites on the PMV genome are indicated above the pPMV85 full-length infectious cDNA The 59 end of the genome was determined by primer clone which was constructed by ligation of pHindIII-PMV-59, pPMV12, extension of the genomic RNA using a 32P end-labeled and pPMV17. Open rectangles on pPMV85 indicate significant open DNA primer (MT30) complementary to a portion of the 59 reading frames. The transcriptional start site of the sgRNA at nucleo- proximal end of the virus RNA (Figs. 4A and 4B). The tide 2851 is indicated by an arrowhead (). primer extension products produced in the absence of dideoxynucleotides lacked the terminal G doublet nor- of a full-length infectious clone of PMV described in this mally associated with a capped RNA (Goldberg et al., study provides further justification for the contention that 1991). The 59 end of PMV RNA (59-GGGUAUU-39) (Figs. 3 PMV forms a new genus of plant viruses. and 4) is similar to the 59 termini of the genomic RNA of carnation mottle carmovirus (CarMV; 59-GGGUAAG-39) RESULTS AND DISCUSSION (Carrington et al., 1989), maize chlorotic mottle machlo- Construction and infectivity of full-length cDNA movirus (MCMV; 59-AGGUAAU-39) (Nutter et al., 1989) clones and cowpea mottle carmovirus (CPMoV; 59-NGGUAUC- 39)(Youet al., 1995). Comparisons of the predicted 59 To determine the primary sequence of PMV, 10 cDNA untranslated leaders of PMV and the tombusviruses clones (Fig. 1) were selected from viral RNA that had within the Tombusviridae revealed no obvious similari- been either polyadenylated and primed with an oligo(dT) ties between these RNAs. primer (pPMV10, pPMV13, and pPMV17), primed with One difference, a C instead ofaGatposition 8, was random oligonucleotides (pPMV3, pPMV7, pPMV12, detected within the untranslated leader sequence de- pPMV18, and pPMV21), or primed with specific oligonu- rived from the pPMV85 clone compared to the sequence cleotides complementary to internal regions of PMV RNA obtained from RNA sequencing (compare Figs. 3 and 4B (pM1 and pHindIII-PMV-59). Each cloned insert was se- with Fig. 4A). This variant was also observed in two of quenced on both strands and the sequence was con- three PCR-derived cDNA clones of pHindIII-PMV-59 and firmed on the full-length infectious cDNA clone after it one clone was identical to the wild-type RNA sequence. was constructed. Either PCR-associated error rates or the diversity of the Pearl millet plants inoculated with full-length tran- viral RNA population (Holland, 1993) could account for scripts derived from pPMV85 developed mild mosaic these differences. However, this difference did not result symptoms on the upper uninoculated leaves within 12 in any obvious change in replication, movement, or phe- days postinoculation. The mild symptoms were typical of notype on pearl millet plants compared to wild-type PMV those elicited by PMV lacking satellites. In contrast, co- infections (data not shown). inoculation of infectious PMV and SPMV transcripts re- sulted in a severe systemic mosaic within 2 weeks post- Relatedness of p48 and p112 to Tombusviridae inoculation which was indistinguishable from wild-type replicases mixed infections. RNA analysis of total RNA extracted from PMV- or PMV1SPMV-infected plants or protoplasts, The first AUG on PMV genomic RNA at nt 29±31 is the using a 32P-labeled probe to the 39 end of the PMV start codon of a putative 48-kDa protein (p48) which genome, revealed the presence of the genomic RNA terminates at an UAG codon at positions 1304±1306 (gRNA) and one sgRNA (Figs. 2A and 2C). Immunoblot (Figs. 3 and 5). A translational readthrough could extend assays of plants indicated that the 26-kDa PMV CP was the ORF to a second stop codon (UAA) at nt 3005±3007 present in the PMV infections and that in the mixed to generate a 112-kDa readthrough protein (p112). A infections, both the PMV and the 17-kDa SPMV capsid second in-frame AUG codon is present at nt 77±79 but proteins were present (Fig.
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