A Single Amino Acid Position in the Helper Component of Cauliflower Mosaic Virus Can Change the Spectrum of Transmitting Vector Species

Moreno, Aránzazu; Hébrard, Eugénie; Uzest, Marilyne; Blanc, Stéphane; Fereres, Alberto

doi:10.1128/jvi.79.21.13587-13593.2005

Cited by 29 publications

(23 citation statements)

References 38 publications

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“…Although poorly efficient CaMV vector species have been reported, none of Ͼ30 aphid species tested thus far are strict CaMV nontransmitters (5,(10)(11)(12). While surveying P2-GFP binding to additional aphid species, a total absence of labeling was observed on 31 maxillary stylets from Acyrthosiphon lactucae (Fig.…”

Section: P2 Binding At the Tip Of The Maxillary Stylets Is Required Fmentioning

confidence: 99%

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A protein key to plant virus transmission at the tip of the insect vector stylet

Uzest

Gargani

Drucker

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

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174

136

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aphid ͉ receptor N early all plant viruses that cause extensive agricultural damage use specific vectors to spread between hosts. The most common vectors are arthropods, especially aphids (1), and the most widely adopted strategy for virus-vector interaction is noncirculative transmission, in which the virus is taken up by a vector feeding on an infected plant, adsorbed somewhere on the cuticle lining the inner part of the feeding apparatus, and subsequently released to inoculate a new host plant. The viral components involved in this interaction are relatively well established, in particular for the genus Cucumovirus, where domains of the coat protein directly recognize unknown retention sites in the vector mouthparts (capsid strategy), and for the genera Potyvirus and Caulimovirus, where a nonstructural viral protein, HC (helper component), creates the link between virion and vector (helper strategy) (reviewed in refs. 2 and 3). However, no putative binding sites for viral components in the insect vector have ever been chemically characterized or even precisely localized. This question is of major importance, because numerous noncirculative viruses may use the same vector attachment sites, and identification of putative receptor molecules could lead to new strategies to combat viral spread.A distinguishing feature of noncirculative transmission is that several virus species can be transmitted by the same vector, and, conversely, several vector species can transmit the same virus. Hence, although some degree of noncirculative virus/vector specificity exists (4, 5), it is often so broad that the very existence of actual viral receptors remains questionable, because their existence has never been directly demonstrated.Here we report evidence for the existence, precise location, and chemical nature of the receptor for a noncirculative virus, cauliflower mosaic virus (CaMV), in its insect vector. A novel in vitro system allowed rapid visualization of the interaction between dissected aphid stylets and the HC of CaMV. The CaMV retention sites are concentrated exclusively in a tiny and previously unknown anatomical zone located at the extreme tip of the aphid maxillary stylets. Virus/vector binding at this specific zone is mandatory for successful CaMV transmission. Pretreatment of dissected stylets with various chemicals and enzymes demonstrated that the molecule used by CaMV as a specific receptor for vector transmission is a nonglycosylated protein deeply embedded in the chitin matrix.

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Section: P2 Binding At the Tip Of The Maxillary Stylets Is Required Fmentioning

confidence: 99%

“…Hence, although some degree of noncirculative virus/vector specificity exists (4,5), it is often so broad that the very existence of actual viral receptors remains questionable, because their existence has never been directly demonstrated.…”

mentioning

confidence: 99%

A protein key to plant virus transmission at the tip of the insect vector stylet

Uzest

Gargani

Drucker

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

174

136

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“…From there, infectious CaMV units are simply released and inoculated into a new, healthy plant after movement of the vector, with no requirement for replication, or even cycling of the virus, within the vector body. The attachment of CaMV to the aphid is mediated by P2, the N-terminal domain of which specifically recognizes a cuticular protein receptor located at the extreme tip of the maxillary stylets (32,47), whereas the Cterminal ␣-helix binds, via predicted coiled-coil structures, to the ectodomain of the P3 decorating the virions (16,25,37).…”

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confidence: 99%

Structural Insights into the Molecular Mechanisms of Cauliflower Mosaic Virus Transmission by Its Insect Vector

Hoh

Uzest

Drucker

et al. 2010

J Virol

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Cauliflower mosaic virus (CaMV) is transmitted from plant to plant through a seemingly simple interaction with insect vectors. This process involves an aphid receptor and two viral proteins, P2 and P3. P2 binds to both the aphid receptor and P3, itself tightly associated with the virus particle, with the ensemble forming a transmissible viral complex. Here, we describe the conformations of both unliganded CaMV P3 protein and its virion-associated form. X-ray crystallography revealed that the N-terminal domain of unliganded P3 is a tetrameric parallel coiled coil with a unique organization showing two successive four-stranded subdomains with opposite supercoiling handedness stabilized by a ring of interchain disulfide bridges. A structural model of virus-liganded P3 proteins, folding as an antiparallel coiled-coil network coating the virus surface, was derived from molecular modeling. Our results highlight the structural and biological versatility of this coiled-coil structure and provide new insights into the molecular mechanisms involved in CaMV acquisition and transmission by the insect vector.Cauliflower mosaic virus (CaMV) is the type member of the plant virus family Caulimoviridae. This family is grouped together with hepadnaviruses into the pararetrovirus group due to its mode of replication via reverse transcription of a pregenomic RNA intermediate (17). The CaMV genome is a double-stranded circular DNA of approximately 8,000 bp, comprising seven major open reading frames (ORFs), only six of which have clearly identified biological functions. The product of ORF VI (P6) is expressed early in infection from the monocistronic 19S RNA. In addition to its recently reported role in the suppression of RNA silencing (14), P6 rapidly self-aggregates into the so-called electron-dense inclusion bodies, demonstrated to be the viral factory (17). Within these structures, P6 then trans-activates the translation of ORFs I to V from the polycistronic pregenomic 35S RNA according to a complex reinitiation process (39). ORFs I to V encode the major capsid protein (P4, encoded by ORF IV), reverse transcriptase (P5, encoded by ORF V), and three auxiliary proteins: P1 (ORF I) is involved in cell-to-cell and long-distance within-plant movement, P2 (ORF II) is involved in aphid transmission, and P3 (ORF III) is tightly associated with the virus particles and has a complex regulatory function in the virus infection cycle, particularly during plant-to-plant vector transmission.The CaMV viral particle is roughly spherical, 520 Å in diameter, with an icosahedral T7 symmetry. It is constituted of three concentric shells, built from 420 capsid protein subunits, surrounding a large inner cavity with a diameter of approximately 250 Å (4, 37). The physical association between P3 and viral particles has been consistently demonstrated in mature CaMV virions by copurification, immunolabeling experiments, and in vitro interactions (7,(23)(24)(25). Recently, cryoelectron microscopy (cryo-EM) image reconstruction further showed that P3 molecu...

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“…The amino acid motifs DAG located near the N terminus of the CP, KITC located near the N terminus of the HC-Pro, and PTK located into the central part of the HC-Pro are essential for transmission (35). For Cauliflower mosaic virus (CaMV; genus Caulimovirus, family Caulimoviridae), a single amino acid change in protein P2, which acts as HC, is sufficient to abolish aphid transmission (24). In the case of nematode-transmitted viruses, a single mutation in the HC protein 2b of Pea early-browning virus (PEBV; genus Tobravirus, unassigned family) is sufficient to prevent transmission (38).…”

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A Stretch of 11 Amino Acids in the βB-βC Loop of the Coat Protein of Grapevine Fanleaf Virus Is Essential for Transmission by the Nematode Xiphinema index

Schellenberger

Andret-Link

Schmitt-Keichinger

et al. 2010

J Virol

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Grapevine fanleaf virus (GFLV) and Arabis mosaic virus (ArMV) from the genus Nepovirus, family Secoviridae, cause a severe degeneration of grapevines. GFLV and ArMV have a bipartite RNA genome and are transmitted specifically by the ectoparasitic nematodes Xiphinema index and Xiphinema diversicaudatum, respectively. The transmission specificity of both viruses maps to their respective RNA2-encoded coat protein (CP). To further delineate the GFLV CP determinants of transmission specificity, three-dimensional (3D) homology structure models of virions and CP subunits were constructed based on the crystal structure of Tobacco ringspot virus, the type member of the genus Nepovirus. The 3D models were examined to predict amino acids that are exposed at the external virion surface, highly conserved among GFLV isolates but divergent between GFLV and ArMV. Five short amino acid stretches that matched these topographical and sequence conservation criteria were selected and substituted in single and multiple combinations by their ArMV counterparts in a GFLV RNA2 cDNA clone. Among the 21 chimeric RNA2 molecules engineered, transcripts of only three of them induced systemic plant infection in the presence of GFLV RNA1. Nematode transmission assays of the three viable recombinant viruses showed that swapping a stretch of (i) 11 residues in the ␤B-␤C loop near the icosahedral 3-fold axis abolished transmission by X. index but was insufficient to restore transmission by X. diversicaudatum and (ii) 7 residues in the ␤E-␣B loop did not interfere with transmission by the two Xiphinema species. This study provides new insights into GFLV CP determinants of nematode transmission.

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A Single Amino Acid Position in the Helper Component of Cauliflower Mosaic Virus Can Change the Spectrum of Transmitting Vector Species

Cited by 29 publications

References 38 publications

A protein key to plant virus transmission at the tip of the insect vector stylet

A protein key to plant virus transmission at the tip of the insect vector stylet

Structural Insights into the Molecular Mechanisms of Cauliflower Mosaic Virus Transmission by Its Insect Vector

A Stretch of 11 Amino Acids in the βB-βC Loop of the Coat Protein of Grapevine Fanleaf Virus Is Essential for Transmission by the Nematode Xiphinema index

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