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Research Groups Group VIP Molecular interactions between viruses and their insect vectors

Molecular interactions between viruses and their insect vectors
Leader of the project: Marilyne Uzest
All non-circulative viruses transmitted by aphids are retained in their insect mouthparts (stylets). This project aims at identifying Caulimo-, Poty- and Cucumovirus receptors in the stylets to thoroughly characterize virus/vector interactions. A second objective is to decipher the role of the acrostyle – organ which bears some receptors – in plant-insect interactions.

Staff involved in the project

Maryline Uzest
Researcher – Leader of the project
Bastien Cayrol
Maelle Deshoux
M. Thillier (2013, Master 2, Univ. Montpellier, France)
M. Deshoux (2015, Master 2, Univ. Montpellier, France)
F. Delicque (2016, Master 2, Univ. Montpellier, France)

M. Deshoux (2016-2019, Thèse, Montpellier, France)

Major collaboration
G. Le Trionnaire (Chargé de Recherche, Inra, Rennes, France)
P. Bron (Directeur de recherche, INSERM, Montpellier, France)
P. Bulet (Directeur de recherche, CNRS, Montpellier, France)
A. Fereres (Professeur, CSIC, Madrid, Espagne)
Y. Rahbé (Directeur de recherche, INRA, Lyon, France)
L. David (Professeur, Université Lyon, France)


Aphids are sap-feeding insects. They are serious pests in agriculture and provoke significant losses, with large economic and social consequences. They transmit numerous plant viruses causing diseases in almost all important crops.
The majority of viruses are acquired after feeding on an infected plant and retained on the aphid’s mouthparts, the stylets (see figure 1). Most often, viruses are both acquired from infected plants and inoculated to healthy ones with a single probing puncture of a few seconds, thereby promoting viral outbreaks. Chemical treatments are expensive and have been proven inefficient at preventing non-circulative viral spread.

A better understanding of virus-vector interactions should help to define future alternative ‘environmentally safe’ strategies, limiting viral transmission by targeting and disrupting specifically the molecules involved in the interactions. The most challenging will be to identify receptors in insect mouthparts.

Figure 1: Attachment of viruses in aphid maxillary stylets (mx), either directly to receptor molecules (R) through the capsid – Cucumovirus – or indirectly through a protein encoded by the virus, the helper component (HC-Pro for Potyviruses, P2 for the CaMV), which makes a molecular link between the receptor and the virus – Potyvirus et Caulimovirus .

State of the art and current results

We set up in vitro interaction assays on aphid individualized dissected stylets. This approach allowed us to show that the Cauliflower mosaic virus (CaMV) receptors are located at the tip of aphid maxillary stylets in the common salivary-food canal (see figure 2). The receptors are non glycosylated cuticular proteins with one domain embedded in the chitin and one domain exposed at the surface. The viral ligand P2 from CaMV binds to a surface exposed domain.

Transmission and scanning electron microscopy studies of the tip of aphid maxillary stylets allowed to discover the acrostyle, organ located in the common canal (see figure 3). The acrostyle is 3 to 4 µm long, 250 nm width L’acrostyle est un organe de 3 à 4 µm de long, maximum 250 nm width. It bears the CaMV receptors. It seems to be conserved among aphid species also at the molecular level (found in all aphid species tested so far, principally in the APhidinae and Calaphidinae family).

Figure 2 : Localisation of the CaMV receptor. The viral protein P2 fused to GFP (green) is retained in the common canal at the tip of aphid maxillary stylets (orange). Here the aphid species is Acyrthosiphon pisum. Observation under epifluorescence microscope. From Uzest et al 2007.

We developed a library of antibodies specific of peptides of aphids’ cuticular proteins to identify the proteins of the acrostyle. Immunolabeling of the stylets allowed to identify several peptides at the tip of maxillary stylets and in the acrostyle belonging to cuticular proteins from the CPR family. A comprehensive study is ongoing to identify precisely the proteins of the acrostyle with domains accessible at the surface of the organ.
Figure 3 : Acrostyle, organ at the tip of aphid maxillary stylets. Transversal cross-section of a stylet bundle of an aphid fed on a CaMV-infected plant visualized under transmission electron microcopy. We can observe at the distal tip 2 virus particles (white arrow) in the common canal of the maxillary stylet. A region dense to the electron is clearly visible at the surface of the common canal (black arrows) (A). Maxillary stylet observed under scanning electron microscopy. Black arrows delineate the acrostyle (B). Ma: mandibular stylet, mx: maxillary stylet, FC: food canal, SC: salivary canal, CC:common canal. From Uzest et al 2008, 2010.

We are currently developping a program to address three main issues :

- Establish the exhaustive repertoire of the proteins of the acrostyle and the motifs exposed at the surface to identify CaMV receptors.

- Characterise and identify receptors of other non-circulative viruses transmitted by aphids, especially Potyvirus and Cucumovirus highly damaging to important crops. The CaMV receptors are the only ones that have been characterized to date. However, some published studies suggested that those viruses should be located in the common canal. We will have to define whether all non-circulative viruses use a generic receptor or if they use different molecules. This is an important issue to define future alternative strategies to limit viral spread.

- Define the role of the acrostyle apart from virus transmission. At the confluence of the salivary and food canals, the acrostyle could retain and release key compounds involved in the aphid feeding process leading to plant-insect compatible interactions.


This project is currently funded by ANR (ANR-StylHook project) et by the Bill & Melinda Gates Foundation (2nd Phase of the Grand Challenge Exploration)

Publication list of the PI : Marilyne Uzest


Jimenez J, Webster CG, Moreno A, Almeida RPP, Blanc S, Fereres A, Uzest. M. Fasting alters aphid probing behaviour but does not universally increase the transmission rate of non-circulative viruses. J Gen Virol. 2017 Nov 14. doi: 10.1099/jgv.0.000971

Chesnais Q, Couty A, Uzest M, Brault V, Ameline A. Plant infection by two different viruses induce contrasting changes of vectors fitness and behavior. Insect Sci. 2017 Jul 21. doi: 10.1111/1744-7917.12508.

Webster CG, Thillier M, Pirolles E, Cayrol B, Blanc S, Uzest M. Proteomic composition of the acrostyle: Novel approaches to identify cuticular proteins involved in virus-insect interactions. Insect Sci. 2017 Apr 19. doi: 10.1111/1744-7917.12469.

Mathers TC, Chen Y, Kaithakottil G, et al. Rapid transcriptional plasticity of duplicated gene clusters enables a clonally reproducing aphid to colonise diverse plant species. Genome Biol. 2017 Apr 4;18(1):63. doi: 10.1186/s13059-017-1202-6.


Marilyne Uzest & Stéphane Blanc (2016). Molecular Mechanisms Involved in Non-circulative Virus–Vector Interactions. In Brown J., (ed.). Vector-Mediated Transmission of Plant Pathogens. San Diego, USA: Academic Press. p59-72

Filloux D., Murrell S., Koohapitagtam M., Golden M., Julian C., Galzi S., Uzest M., Rodier-Goud M., D'Hont A., Vernerey M.S., Wilkin P., Peterschmitt M., Winter S., Murrell B., Martin D.P., Roumagnac P. 2015. The genomes of many yam species contain transcriptionally active endogenous geminiviral sequences that may be functionally expressed. Virus Evolution, 1 (1): 17 p. http://dx.doi.org/10.1093/ve/vev002

Blanc, S. ; Drucker, M. ; Uzest,M. (2014). Localizing Viruses in Their Insect Vectors. Annu. Rev. Phytopathol. 52:403–25

Blanc, S., Uzest, M., Drucker, M. (2011). New research horizons in vector-transmission of plant viruses. Curr Opin Microbiol. 14:483–491
M. Uzest, M., Drucker, M., Blanc, S. (2011). La transmission d’un complexe : pas si simple. Cas du virus de la mosaïque du chou-fleur.Virologie 15 (3), 192-204

Hoh, F., Uzest, M.*, Drucker, M., Plisson-Chastang, C., Bron, P., Blanc, S. & Dumas, C. (2010). Structural insights into the molecular mechanisms of cauliflower mosaic virus transmission by its insect vector. J Virol 84, 4706-13.

Uzest, M., Gargani, D., Dombrovsky, A., Cazevieille, C., Cot, D. & Blanc, S. (2010). The "acrostyle": a newly described anatomical structure in aphid stylets. Arthropod Struct Dev 39, 221-9.

Brault, V., Uzest, M., Monsion, B., Jacquot, E. & Blanc, S. (2010). Aphids as transport devices for plant viruses. C R Biol 333, 524-38.

Martinière, A., Gargani, D., Uzest, M., Lautredou, N., Blanc, S. & Drucker, M. (2009). A Role for Plant Microtubules in the Formation of Transmission-specific inclusion bodies of Cauliflower mosaic virus. Plant J 58, 135-146.

S. Blanc, M. Uzest, T. Candresse, M. Drucker, A. Fereres, D. Gargani, E. Garzo, H. Hébrard. (2008). Une protéine clé pour la transmission d'un virus de plante à la pointe des stylets de l'insecte vecteur.Virologie 12 (1), 70-2

Uzest, M., Gargani, D., Drucker, M., Hebrard, E., Garzo, E., Candresse, T., Fereres, A. & Blanc, S. (2007). A protein key to plant virus transmission at the tip of the insect vector stylet. Proc Natl Acad Sci U S A 104, 17959-64.

Moreno, A., Hebrard, E., Uzest, M., Blanc, S. & Fereres, A. (2005). A single amino acid position in the helper component of cauliflower mosaic virus can change the spectrum of transmitting vector species. J Virol 79, 13587-93.

Froissart, R., Roze, D., Uzest, M., Galibert, L., Blanc, S. & Michalakis, Y. (2005). Recombination every day: abundant recombination in a virus during a single multi-cellular host infection. PLoS Biol 3, e89

Plisson, C., Uzest, M.*, Drucker, M., Froissart, R., Dumas, C., Conway, J., Thomas, D., Blanc, S. & Bron, P. (2005). Structure of the mature P3-virus particle complex of cauliflower mosaic virus revealed by cryo-electron microscopy. J Mol Biol 346, 267-77.

Froissart, R., Uzest, M., Ruiz-Ferrer, V., Drucker, M., Hebrard, E., Hohn, T. & Blanc, S. (2004). Splicing of Cauliflower mosaic virus 35S RNA serves to downregulate a toxic gene product. J Gen Virol 85, 2719-26.

Drucker, M., Froissart, R., Hebrard, E., Uzest, M., Ravallec, M., Esperandieu, P., Mani, J. C., Pugniere, M., Roquet, F., Fereres, A. & Blanc, S. (2002). Intracellular distribution of viral gene products regulates a complex mechanism of cauliflower mosaic virus acquisition by its aphid vector. Proc Natl Acad Sci U S A 99, 2422-2427.

Hébrard, E., Drucker, M., Leclerc, D., Hohn, T., Uzest, M., Froissart, R., Strub, J.-M., Sanglier, S., van Dorsselaer, A., Padilla, A., Labesse, G. & Blanc, S. (2001). Biochemical Characterization of the Helper Component of Cauliflower Mosaic Virus. J. Virol. 75, 8538-8546.

Michel, B., Ehrlich, S. D. & Uzest, M. (1997). DNA double-strand breaks caused by replication arrest. EMBO J 16, 430-8.

Uzest, M., Ehrlich, S. D. & Michel, B. (1995). Lethality of rep recB and rep recC double mutants of Escherichia coli. Mol Microbiol 17, 1177-88

d'Alencon, E., Petranovic, M., Michel, B., Noirot, P., Aucouturier, A., Uzest, M. & Ehrlich, S. D. (1994). Copy-choice illegitimate DNA recombination revisited. EMBO J 13, 2725-34.

Vilette, D., Uzest, M., Ehrlich, S. D. & Michel, B. (1992). DNA transcription and repressor binding affect deletion formation in Escherichia coli plasmids. EMBO J 11, 3629-34.

Uzest, M., Ehrlich, S. D. & Michel, B. (1991). The Escherichia coli terB sequence affects maintenance of a plasmid with the M13 phage replication origin. J Bacteriol 173, 7695-7.