Details of DPV and References
DPV NO: 422 July 2011
Species: Grapevine leafroll-associated virus 3 | Acronym: GLRaV-3
Grapevine leafroll-associated virus 3
Giovanni P. Martelli Department of Plant Protection and Applied Microbiology, University Aldo Moro Bari, Italy and Plant Virology Institute of the CNR, UOS Bari, Bari, Italy
Pasquale Saldarelli Plant Virology Institute of the CNR, UOS Bari, Bari, Italy
Angelantonio Minafra Plant Virology Institute of the CNR, UOS Bari, Bari, Italy
- Main Diseases
- Geographical Distribution
- Host Range and Symptomatology
- Transmission by Vectors
- Transmission through Seed
- Transmission by Grafting
- Transmission by Dodder
- Nucleic Acid Hybridization
- Stability in Sap
- Properties of Particles
- Particle Structure
- Particle Composition
- Properties of Infective Nucleic Acid
- Molecular Structure
- Genome Properties
- Relations with Cells and Tissues
- Ecology and Control
Described by Rosciglione & Gugerli (1986).
A virus with flexuous filamentous particles about 1800 x 12 nm in size that infects only Vitis species. It was first detected in Switzerland in grapevines showing reduced vigour, downward rolling of the leaf margins, and early season reddening of the inteveinal areas that soon expanded to the whole leaf blade (Rosciglione &Gugerli, 1986). GLRaV-3 is transmitted by grafting and by pseudococcid mealybugs and soft scale insects with a semipersistent modality, but is not transmitted by sap inoculation, through seeds or through dodder. Its genome is linear positive-sense, ssRNA and it is classified as the type species of the genus Ampelovirus, which currently contains eight species. The genus is grouped with two others (Closterovirus and Crinivirus) in the family Closteroviridae (Martelli et al., 2011).
GLRaV-3 is one of the viruses involved in the aetiology of leafroll disease of Vitis vinifera. American Vitis species and their hybrids used as rootstocks are infected but do not show symptoms (Krake et al., 1999; Martelli, 1993; Martelli & Boudon-Padieu, 2006; Walter et al., 2000).
The virus has a worldwide distribution (Martelli & Boudon-Padieu, 2006).
Host Range and Symptomatology
The virus has apparently no hosts other than Vitis species (Klaassen et al., 2011). Besides V. vinifera, natural infections of V. californica and V. vinifera x V. californica hybrids have been reported from California (Klaassen et al., 2011), and of V. labruscana (Concord) and V. labrusca (Niagara) from Washington State (Naidu et al., 2011). In red- and white-berried European grapevine cultivars natural GLRaV-3 infections result in reddening (Fig. 1) or yellowing of the leaves (Fig. 2), respectively. Discolourations usually appear in summer and progress from the base to the top of the canes as the season advances. Leaf blades become thick, brittle and show downwardly-rolled margins. Bunches mature late and irregularly. The quantity and quality of the grapes (sugar content, soluble solids, titratable acidity) is adversely affected, and the aromatic profile of musts modified (Martins et al., 1997). Symptomatic leaves have decreased chlorophyll and carotenoid pigments, rubisco, nitrate reductase, photosynthetic activity and thylakoid membrane proteins and senesce rapidly (Bertamini et al., 2005; Hristov & Abracheva, 2001) but have increased resveratrol (Bertazzon et al., 2009). Detrimental effects are similar on own-rooted vines (e.g. cv. Merlot) (Alabi et al., 2011). Virus elimination from different red-berried cultivars results in an overall improvement in vine performance, earlier and higher accumulation of anthocyanins in the berries, of soluble solids in the must, increased vegetative vigour and higher yields, (Guidoni et al., 1997; Mannini et al., 2006, 2009).
- Several red-berried V. vinifera cultivars (Cabernet sauvignon, Cabernet franc, Merlot, Mission, Pinot noir) are routinely used as indicators in indexing trials. They all react with typical symptoms (rolling and reddening of the leaves), usually within a few months from graft-inoculation in the field (Martelli, 1993) or within a glasshouse (Walter et al., 1990).
- The virus can be propagated in the above V. vinifera cultivars. Virus titre is higher in in vitro-propagated herbaceous cuttings than in field-grown source plants (Barba et al., 1989).
- Biological variants
- Two biologically distinct virus strains have been found in Australia in cv. Crimson Seedless. One (GLRaV-3-s) elicits severe symptoms, spreads naturally and is associated with poor quality grapes. By contrast, the symptoms induced by the other strain (GRLaV-3-m) are mild and the vines bear larger, crispier and heavier berries than those of a virus-free clone of the same variety (Habili et al., 2009).
- Serological variants.
- Virus isolates with differential immunoreactivity have been reported from New Zealand (Chooi et al., 2011).
- Molecular variants
- The virus is characterized by a wide molecular heterogeneity in different genomic regions. In a comparative study by single strand conformation polymorphism (SSCP) of 45 viral isolates from 14 countries, the highest genetic diversity level was found in the CP (0.0492), followed by HSP70h (0.0340) and RdRp genes (0.0295). Divergence in the former two genes was also due to recombination events (Turturo et al., 2005). A Spanish virus isolate from cv. Tempranillo diverged at the nucleotide level from other sequenced strains by 20% in the polymerase gene and by 30% in the intergenic fragment between ORF1b and ORF2 (Angelini et al., 2006). Five variant groups were identified in the US analysing the HSP70h gene (Fuchs et al., 2009a), and three groups were detected in South Africa by SSCP analysis of ORF5 sequences. The molecular variation of ORF5 correlated with that shown by the 5' NTR of a representative of each grouping (Jooste et al., 2010). Finally, five well-defined clusters of variants in the CP gene were found among 174 virus isolates from a Portuguese grapevine collection. Three of these clusters corresponded to the South African groups (Jooste et al., 2010) whereas cluster 4 comprised only vines of Portguese origin and cluster 5 the partially sequenced Chilean isolate Cl-817 (EU344894) (Gouveia et al., 2011).
Transmission by Vectors
The virus is not aphid-transmitted (Kuniyuki et al., 1994). Vectors are the pseudococcid mealybugs (Hemiptera:Pseudococcidae) Planococcus ficus, Pl. citri, Pseudococcus longispinus (Fig. 3), Ps. affinis, Ps.calceolariae, Ps. maritimus, Ps. viburni, Ps. comstocki, Heliococcus bohemicus, Phenacoccus aceris (Cabaleiro & Segura, 1997a; Golino et al., 1995; Ioannou et al., 1997; Petersen & Charles, 1997; Rosciglione & Gugerli, 1989; Sforza et al., 2003; Zorloni et al., 2004) and the soft scale insects (Hemiptera:Coccidae) Pulvinaria vitis, Neopulvinaria innumerabilis, Parthenolecanium corni, Coccus hesperidium, C. longulus, Saissetia sp., Parassaissetia nigra, and Ceroplastes rusci (Belli et al., 1994; Krüger & Douglas, 2009; Mahfoudhi et al., 2009; Sforza et al., 2003). Transmission is semi-persistent, i.e. acquisition and inoculation access periods in the range of 15-60 min and 30 min, respectively, retention of infectivity from 2 or 3 up to 8 days, absence of a latent period, lack of retention through moults and of transmission to the vector's progeny (Cabaleiro, 2009; Cabaleiro & Segura, 1997b; Krüger et al., 2006). The molecular bases of this mode of transmission are currently not understood. In particular, the localization of virions in viruliferous vectors has not been ultimately established, and the reasons for the long retention period are unknown. Although the apparent detection of GLRaV-3 particles in the salivary glands of Pl. citri (Cid et al., 2007) led to the suggestion that the virus could be transmitted in a persistent circulative manner, further experiments confirmed transmissibility with a semi-persistent modality (Tsai et al., 2008).
Transmission through Seed
None found (Kuniyuki et al., 1992).
Transmission by Grafting
The virus is readily transmitted by grafting from naturally infected V. vinifera to plants of the same or other Vitis species (Harmon & Snyder, 1946; Krake et al., 1999; Martelli, 1993; Scheu, 1935).
Transmission by Dodder
Positive transmission by Cuscuta campestris from grape to grape but not to herbaceous hosts (Woodham & Krake, 1983).
The virus is moderately immunogenic. Polyclonal antisera have been raised using partially purified virus (Gugerli et al.,1990; Tobias et al., 1996; Zee et al., 1987; Zimmermann et al., 1988), or recombinant CP subunits (Ling et al., 2000), or electrophoretically separated CP subunits (Gozsczynski et al., 1995, 1997). Monoclonal antibodies (MAbs) have also been produced to a number of isolates from different countries (Faggioli et al., 1991; Gugerli, 2009; Gugerli et al., 1990; Hu et al., 1990; Seddas et al., 2000; Zee et al., 1987; Zhou et al., 2003; Zimmermann et al., 1990a). Polyclonal antisera and MAbs decorate virus particles from purified preparations and leaf dips in immunoelectron microscopy tests, and are widely used with various ELISA protocols (Gugerli, 2009) or tissue blot immunoassays (Couceiro et al., 2006) for virus detection in field samples with home-made and commercial kits. MAbs have also been used for mapping epitopes on the viral CP (Zhou et al., 2003). A fully recombinant ELISA kit was developed, comprising a single-chain fragment variable antibody and a recombinant viral CP expressed in bacteria, thus avoiding problems associated with virus propagation and purification (Cogotzi et al., 2009). Leaf tissues (petioles and/or mid veins) collected in autumn and cortical scrapings of mature canes are good sources of antigen for routine serological detection of the virus from field samples (Martelli et al., 1997). Cortical scrapings from canes and roots, rather than leaf tissues, are recommended for virus detection in American Vitis hybrids used as rootstocks either by serology (Boscia et al., 1991; Credi & Santucci, 1991) or nucleic acid-based techniques (Beccavin et al., 2009). ELISA is more effective than indexing for virus detection (Rowhani et al., 1997).
Nucleic Acid Hybridization
GLRaV-3 has been detected by hybridization of total RNA extracts from infected vines with radioactive or digoxigenin-labelled molecular probes (Saldarelli et al., 1994a, 1994b). More recently, a range of diversified protocols based on RNA amplification with virus-specific or degenerate primers designed on different virus genes (CP or HSP70h) has been used for GLRaV-3 detection in naturally infected hosts, starting from different templates (dsRNAs, total nucleic acid extracts, crude tissues extracts), and in viruliferous mealybugs and soft scales (Douglas et al., 2009; Fuchs et al., 2009b; Minafra & Hadidi, 1994). These amplification procedures comprise conventional single-step and multiplex RT-PCR (Faggioli & La Starza, 2006; Minafra & Hadidi, 1994), spot RT-PCR (La Notte et al., 1997), ramped annealing nested RT-PCR (Dovas et al., 2006), immunocapture RT-PCR (Engel et al., 2006), qRT-PCR (Malan et al., 2009), TaqMan RT-PCR and TaqMan low density array (Osman et al., 2007, 2008, 2009).
The virus is serologically distantly related to Grapevine leafroll-associated virus 1 (GLRaV-1) with which it shares an antigenic determinant (Seddas et al., 2000). No cross reactions are detected with other ampeloviruses using extant polyclonal antisera or monoclonal antibodies. However, a recombinant single-chain fragment variable antibody to GLRaV-3 recognized GLRaV-1 and GLRaV-7, but not the more distantly related GLRaV-2 (Orecchia et al., 2008). In phylogenetic trees construced with sequences of different viral genes (polymerase, CP, HSP70h) GLRaV-3 and GLRaV-1 consistently group in the same clade, forming a subgroup (subgroup II or B), distinct from subgroup I (or A) which comprises all the other grapevine ampeloviruses (Maliogka et al., 2008; Martelli, 2009).
Method 1 (Gugerli et al., 1984; Zimmermann et al., 1990b). Leaf tissues from symptomatic grapevines are powdered in a mortar in the presence of liquid nitrogen and suspended in Tris-HCl buffer 0.5 M, pH 8.2 containing 4% Polyclar AT (polyvinylpyrrolidone, PVPP), 0.5% bentonite, 4% Triton X-100 and 0.2% 2-mercaptoethanol. All steps are carried out at 4 °C. After 30 min stirring, the homogenate is filtered through cheesecloth and clarified by slow-speed centrifugation (7,500 g for 15 min). The supernatant is layered on a 20% (w/v) sucrose cushion and centrifuged for 170 min at 85,000 g. Pellets are re-suspended overnight in a Tris-HCl 0.02 M, pH 8.2, MgCl 2 0.01M buffer. After a further low-speed centrifugation (7,500 g for 20 min) the supernatant is centrifuged again through a sucrose cushion as above. Re-suspended pellets constitute the concentrated semi-purified virus preparation.
Method 2 (Zee et al., 1987). Mature symptomatic grapevine leaves, used fresh or frozen at -80 °C, are powdered in liquid nitrogen with mortar and pestle, mixed with 5 vol. (1g/5ml) of 0.5 M Tris-HCl buffer, pH 8.2, containing 4% water insoluble PVPP, 0.5% bentonite, 0.2% 2-mercaptoethanol and 5% Triton X-100 and agitated for 30 min at 6 °C. The extract is squeezed through cheesecloth, clarified by centrifugation for 30 min at 6,000 g and concentrated by high-speed centrifugation (80,000 g for 2 h) over 5-ml pads of 20% sucrose dissolved in 0.1 M Tris-HCl, pH 8.2. Pellets are re-suspended in 0.1 M Tris-HCl buffer, pH 8.2, containing 0.01 M MgCl2 and centrifuged at 2,000 g for 5 min. The supernatant is layered over a 3-ml pad of 20% sucrose and centrifuged at 30,000 rpm for 2 h in a Beckman type 40 rotor. Pellets are dissolved in 0.1 M Tris-HCl buffer pH 8.2 with 0.01 M MgCl2, then layered over a 3-ml pad of 53% caesium sulphate and centrifuged in a Beckman SW-40 rotor for 18 h at 36,000 rpm. Fractions are recovered and checked electron microscopically.
Method 3 (Uyemoto et al., 1997). Source material consists of bark shavings from dormant canes. The outer skin is removed and the canes are submerged in iced water. Free moisture is removed from the canes and the cortical layer is scraped with a sharp knife into a mortar containing liquid nitrogen, to be powdered with a pestle and mixed with either one of three extraction buffers: (i) 0.5 M Tris-HCl pH 8.2, containing 4% PVPP, 5% Triton X-100, 0.1% 2-mercaptoethanol, 0.5% bentonite; (ii) Tris-HCl as above without bentonite; (iii) 0.5 M potassium phosphate pH 6.4, 0.2% urea, 0.5 sodium sulphite, 4% PPVV, 5% Triton X-100, 0.1% 2-mercaptoethanol. The homogenate is incubated at 4 °C for no less than 1 h, filtered through cheesecloth and centrifuged at 7,000 g for 10 min. The supernatant is filtered through miracloth and centrifuged at 118,000 g for 1.5 h. Pelletes are re-suspended in 0.1 M Tris-HCl, pH 8.2 with 0.01 M MgCl, for tissues extracted in Tris-HCl, or in 0.1 M Tris-HCl, pH 7.0, 0.01 M MgCl2 and 0.3% urea, for tissues extracted in phosphate buffer. Re-suspended pellets are centrifuged at 2,000 g for 5 min, the supernatant is overlaid on a 5-ml cushion of 20% sucrose in a single tube and virions are pelleted as above. Pellets are re-suspended in the appropriate buffer, clarified by a slow-speed centrifugation and subjected to isopycnic centrifugation (164,000 g for 18 h in a SW-40 rotor) in a caesium sulphate density gradient column.
Virus particles are very flexuous, about 1800 x 12 nm in size, show a distinct cross banding and, like those of all members of the family Closteroviridae, are helically constructed; the pitch of the primary helix is about 3.5 nm, and there are approximately 10 protein subunits per turn of the helix (Fig. 4). The 5' terminus (head) of the particle is likely to have the same complex structure as other members of the family Closteroviridae, made up of four different proteins (see Particle Composition) for which the names rattle snake, heterodimeric and bipolar have been coined (Martelli et al., 2011).
Viral nucleic acid is a monopartite, linear, single-stranded, positive-sense RNA molecule constituting about 5% of the particle weight. The 5'-end of the genome is likely to be capped and the 3'-end is not polyadenylated (Ling et al., 1998).
Dissociated CP preparations have a Mr of 43 kDa estimated electrophoretically (Gugerli et al., 1990; Zimmermann et al., 1990c). By analogy with other members of the family Closteroviridae, virions are likely to contain five structural proteins (Dolja et al., 2006). The major CP (34 kDa, estimated from the amino acid sequence), coats the whole length of the virion except for the 5' terminal part (about 100 nm), which is coated by the diverged copy of the CP (CPm, 50 kDa) and comprises also three additional proteins, HSP70h, 55 kDa (p55), and 20 kDa (p20A).
GLRaV-3 has the largest genome in the genus Ampelovirus, consisting of 12 open reading frames (ORFs) (Fig. 5). Seven viral isolates have been completely sequenced: (i) isolate NY-1 from the US, 17,919 nt in size (AF037268) (Ling et al., 1998, 2004); (ii) isolate Cl-766 from Chile, 17,919 nt in size (EU344893) (Engel et al., 2008); (iii) isolate GP18 from South Africa, 18,498 nt in size (EU259806) (Maree et al., 2008) (iv) isolate PL-20 from South Africa, 18,433 nt in size (GQ352633) (Jooste et al., 2010); (v) isolate 621 from South Africa, 18,498 nt in size (GQ352631) (Jooste et al., 2010); (vi) isolate 623 from South Africa, 18,498 nt in size (GQ352632) (Jooste et al., 2010); (vii) isolate WA-MR from the US, 18,498 nt in size (GU983863) (Jarugula et al., 2010). The difference in genome size between isolates NY-1/Cl-766 (17,919 nt) and the other five isolates (18,433-18,498 nts) depends on the length of the 5' NTR, which was determined to be 158 nt long in NY-1/Cl-766 and 737 nt long in four of the other virus isolates. The latter figure (737 nt) is thought to be the correct one (Jarugula et al., 2010). The 5' NTR of isolate WA-MR folds into a complex secondary structure with several substructural hairpins of variable length, differing from the less complex one of the South African isolates (Jarugula et al., 2010). By contrast, the 3' NTR of all isolates has the consistent length of 277 nts, is more conserved, and folds always into a secondary structure consisting of two principal hairpins, the 5' most of which contains four substructural hairpins (Jarugula et al., 2010).
In the 5'® 3' direction the viral genome encodes: (i) a polyprotein 245.3 kDa in size comprising the papain-like protease, methyl transferase, AlkB, and helicase domains (ORF1a), and the polymerase (ORF 1b); (ii) a 6 kDa hydrophobic protein with a putative transmembrane domain separated by an intergenic non coding region 228 nt long from ORF1b (ORF2); (iii) a 5 kDa hydrophobic protein (ORF3) separated from ORF 2 by an intergenic non coding region 1,065 nt in size; (iv) the HSP70h protein (ORF4); (v) a 55 kDa protein matching the comparable product encoded by all members of the family Closteroviridae (ORF5); (vi) the coat protein (CP) 34 kDa in size (ORF6); (vii) the minor coat protein (CPm) 50 kDa in size (ORF7); (viii) a 21 kDa protein (ORF8); (ix) two 20 kDa proteins (p20A and p20B) (ORFs 9 and 10); (x) two proteins 4 kDa and 7 kDa in size, respectively (ORFs 11 and 12) (Fig. 5). HSP70h is a multifunctional protein thought to be involved in cell-to-cell transport of infectivity through plasmodesmata, assembly of multi-subunit complexes for genome replication and/or subgenomic RNA synthesis, and assembly of virus particles, whereas the 55 kDa protein is required for incorporation of HSP70h and CPm to virion heads (Dolja et al., 2006). ORFs 3 to 7 constitute the so-called quintuple gene module, which is conserved in most members of the family Closteroviridae. Genome expression strategy encompasses: (i) direct translation and proteolytic processing of the polyprotein encoded by ORF1a; (ii) +1 ribosomal frameshift for the expression of the polymerase domain encoded by ORF1b; (iii) a set of eleven 3' co-terminal monocistronic subgenomic RNAs for the expression of proteins encoded by ORF 2 through 12 (Jarugula et al., 2010) (Fig. 5). Eight subgenomic RNAs with a size ranging from 9,497 to 1,233 nts were identified in infections by the South African virus isolate GP18 (Maree et al., 2009). Jarugula et al. (2010) reported that the subgenomic RNAs for CP, p21, p20A and p20B genes of the US virus isolate WA-MR are the most abundant, being 4,699, 2,226, 1,744 and 1,234 nt in size, respectively.
Relations with Cells and Tissues
The virus is unevenly distributed in tissues of European grapes and American rootstocks (Boscia et al., 1991; Credi & Santucci, 1991; Teliz et al., 1987; Rowhani et al., 1997) and is restricted to the phloem where it induces necrotic obliteration and hyperplastic proliferation of sieve tubes located in the abaxial vascular bundles (Faoro et al., 1992). Cytopathological modifications of differentiating sieve tubes, companion and phloem parenchyma cells can be rather extensive. The cytoplasm of infected cells contains: (i) inclusion bodies made up of clusters of membranous vesicles with fibrillar content originated from proliferation of the peripheral membrane of mitochondria (Fig. 6 and Fig. 7), which are released in the ground cytoplasm following disruption of these organelles; (ii) loose bundles to compact aggregates of virus particles (Fig. 8), sometimes surrounded by a bounding membrane (Fig. 9) and occasionally present in the nuclei; (iii) patches of granular electron-dense material containing many ribosomes (Faoro et al. 1991, 1992; Kim et al., 1989). Mitochondrial vesicles were experimentally shown to contain RNA and are thought to be sites of viral genome replication (Faoro & Carzaniga, 1995).
Ecology and Control
The extremely wide geographical distribution and the severity of the disease induced make GLRaV-3 a serious pathogen. The incidence of infections is quite variable, depending on the environmental conditions under which grapevines are grown and on vector efficiency (Douglas & Krüger, 2008). The virus invades the host plants systemically, where it persists, and is disseminated with propagative material over medium and long distances. Spreading at a site is mediated by vectors. Re-infection of vineyards newly established in areas with favourable environmental conditions for vector multiplication, in which the old plants supported mealybug populations, can be very quick, e.g. from 9.1 to 93.1% in 5 years in New Zealand (Jordan et al., 1993); from 22 to 56% in 5 years in Australia (Habili & Nutter, 1997); from 20 to 67% and from 33 to 73% in 5 years in two Cypriot localities (Ioannou et al., 1999); from 0 to 100% in 12 years, again in New Zealand (Goussard & Hunderhay, 2004); from 0 to 82% in 10 years to 94.7% in 13 years in Spain (Cabaleiro, 2009; Cabaleiro et al., 2008); from 23 to 66% in 5 years in the US (Golino et al. 2008). Slower spread (from 0 to 25% in 17 years) was registered in a vineyard planted with virus-free vines in Piedmont (northern Italy), where climatic conditions are less favourable to the vector (Bertin et al., 2009). Mealybug crawlers, the first nymphal instar stage in particular, are responsible for virus spread at a site as they move from vine to vine, but can also be passively transported by wind, contaminated agricultural implements and labourers' clothing (Pietersen, 2006). Mealybugs thriving on remnant roots following uprooting of vineyards were held responsible for the rapid reappearance of GLRaV-3 infections in replanted New Zealand vineyards (Bell et al., 2009). The virus can be eliminated from infected vines by heat therapy, but more efficiently by meristem tip culture (Savino et al., 1990), somatic embryogenesis (Gambino et al., 2006) and chemotherapy of in vitro-grown explants (Panattoni et al., 2007). Thus a complex strategy encompassing preventive measures for the establishment of sanitarily improved vineyards and restraining vector-mediated virus spread can envisaged, based on enforcement of fallow periods, elimination of volunteer vines and remnant roots, use of virus-free planting material, roguing of newly infected vines, judicious use of contact and systemic insecticides, sanitation of agricultural equipment and labourers' clothing (Pietersen, 2006; Spreet et al., 2006).
Genome structure and strategy of replication of GLRaV-3 [modified from Jarugula et al. (2010)].
Mitochondrion of a grapevine cell infected by GLRaV-3 in an early stage of vesiculation. Membranous vesicles containing filamentous material (Ve) are nested within the organelle's bounding membrane. White arrow points to residual cristae (Cr). Bar = 100 nm [from Faoro et al. (1992), by permission].
Mitochondria (M) in a GLRaV-3-infected grapevine parenchyma phloem cell in a late stage of vesiculation. The organelles are transformed into a mass of vesicles. CW = cell wall. Bar = 250 nm [from Faoro et al. (1992), by permission].
Bundles of virus particles (V) in a companion cell of a GLRaV-3-infected grapevine. The particles are labelled with colloidal gold-conjugated antibodies to GLRaV-3. Bar = 250 nm [from Faoro et al. (1992), by permission].
Membrane-bound compact aggregates of virus particles (V) in an GLRaV-3-infected grapevine parenchyma phloem cell. Bar = 250 nm [from Faoro et al. (1992), by permission].
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