Unité Mixte de Recherche - Biologie et Génétique des Interactions Plante-Parasite
Cirad - Inra - Montpellier SupAgro

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Group 2 : Interactions Virus Insect Plant (VIP) Research interest
Cellular virus-host interaction regulating the uptake of the virus by its insect vector
Project leader: Martin Drucker

Many parasites form during their life cycle specific cellular structures (morphs) that are dedicated to transmission. This project studies such morphs, formed by plant viruses in response to arrival, installation and feeding of their arthropod vectors on infected plants.

Staff involved in the project

M. Drucker
Project Leader
J.L. Macia
E. Berthelot

Research project

Background and state of the art

We want to understand the cellular and molecular interactions between plant viruses and their plant hosts that allow for their acquisition and subsequent transmission by insect vectors.
Confocal projections showing CaMV-infected leaf tissue immunolabelled for P2 aphid transmission factor (green). Left: Epidermis and mesophyll cells displaying P2 in standby transmission bodies. Cell walls are counterstained in cyan and chloroplasts in red. Middle: Epidermis cells displaying P2-labelled mixed-networks. Chloroplasts are counterstained in red. Right: P2-labelled mixed-networks close to a stylet sheath (bluish tube-like structure) in leaf mesophyll. During puncturing, aphids secrete continuously gelling saliva that hardens around the stylet track to form a stylet sheath. When the stylets are withdrawn, the sheaths are left behind and document the stylet track. Chloroplasts are counterstained in red and nuclei in white.

We want to understand the cellular and molecular interactions between plant viruses and their plant hosts that allow for their acquisition and subsequent transmission by insect vectors.

For this, we study Cauliflower mosaic virus (CaMV) and (since more recently) Turnip mosaic virus (TuMV), two entirely unrelated viruses that are transmitted by aphids using similar molecular strategies: both viruses bind – like hundreds of other plant viruses – to the aphid stylets (their needle-like mouthparts) when aphids puncture infected plant cells. They are then transported, immobilised in the stylets, to other plants and are inoculated into them when aphids resume testing and feeding punctures.

It has been assumed for a long time that virus acquisition is simple contamination of the stylets occurring during aphid feeding and an active role of the virus has rarely been considered. Our research has rendered obsolete this view by the discovery of an unexpected phenomenon: the model virus CaMV forms precisely at the arrival of the aphid vector specific transmission morphs that dissociate after aphid take-off (Martinière et al., 2013). Thus, this virus is transmission-competent only during the presence of vectors on the plant and when transmission is possible and can attribute cellular resources to other steps of the infection cycle (replication, movement etc.) for the remaining time (Figure 1).

All our projects deal with this phenomenon that we have named 'transmission activation'. We work mostly on two research axes. First, we want to explore the cellular and molecular details of CaMV transmission activation, and second, we want to know whether (and how) other viruses activate their transmission.

Answering these two question will have great impact on plant virology and pathology and possibly also on agriculture (Drucker & Then, 2015). Effectively, elucidating the different steps in transmission activation might reveal weak points that might be used to design novel virus control strategies. Finally, testing other viruses will inform whether transmission activation is a universal mechanism in plant and – why not – animal virology.

Figure 1: The CaMV transmissible complex and a model of CaMV transmission activation. (A) CaMV transmission requires formation of a transmissible complex, composed of the icosahedric virus particle (in blue and yellow) and the viral protein P2 (red), which as the aphid transmission factor binds the virus particle to a receptor in the aphid stylet tips. (B) Model of CaMV transmission activation. (1) Schema of an infected plant cell in the absence of aphids. The cell displays virus factories (VF) containing most virus particles (blue and yellow circles), embedded in a matrix of viral protein P6 (grey). This cell contains also another viral structure, the transmission body (TB). The TB is in a stand-by state in the absence of aphids and contains all of a cell's P2 protein (red), associated with P3 (blue) and some virus particles. The microtubules are shown in green. (2) After alighting on an infected plant, the aphid inserts its stylets into the tissue for probing punctures. This causes mechanical and/or chemical stress, induced by the stylets' movement or a unknown saliva or other compound. The plant immediately senses the stress (symbolised by the yellow flashes), which will eventually trigger a defence response. The TB reacts also to the aphid stress, probably in relation with the initial defence response. Tubulin (green) floods within seconds the TB, transforming it into an 'activated' TB. (3) Equally rapid, the TB dissociates and P2 as well as virus particles (from virus factories) relocalise on microtubules to form 'mixed networks' (Martinière et al., 2013 ; Bak et al., 2013). The mixed networks display transmissible complexes and a surplus of P2, allowing direct and sequential virus acquisition by the vector (Drucker et al., 2002). (4) After take-off of the aphid, which retains free P2 and transmissible complexes in the stylets, a new TB forms and the remaining virus particles are shuttled back to the virus factories, to be ready for another. round of transmission. Modified after Drucker & Then (2015).


Agence National de la Recherche (ANR) projet 12-BSV7-005-01 «VIP»
Human Frontiers Science Program (HFSP) projet RGP0013/2015 «Cellular and biophysical mechanisms of virus-vector interactions mediating disease transmission»

Selected publications

Drucker, M., and Then, C. (2015). Transmission activation in non-circulative virus transmission: a general concept? Curr Opin Virol 15, 63–68.

Bak, A., Blanc, S., Gargani, D., Martinière, A., and Drucker, M. (2014). Multiples fonctions des usines virales?: l’exemple du virus de la mosaïque du chou-fleur (cauliflower mosaic virus). Virologie 18, 201–210.

Blanc, S., Drucker, M., and Uzest, M. (2014). Localizing viruses in their insect vectors. Annu Rev Phytopathol 52, 403–425.

Bak, A., Martinière, A., Blanc, S., and Drucker, M. (2013). Early interactions during the encounter of plants, aphids and arboviruses. Plant Signal Behav 8, e24225.

Bak, A., Gargani, D., Macia, J.-L., Malouvet, E., Vernerey, M.-S., Blanc, S., and Drucker, M. (2013). Virus factories of cauliflower mosaic virus are virion reservoirs that engage actively in vector transmission. J Virol 87, 12207–12215.

Martinière, A., Bak, A., Macia, J.-L., Lautredou, N., Gargani, D., Doumayrou, J., Garzo, E., Moreno, A., Fereres, A., Blanc, S., and Drucker, M. (2013). A virus responds instantly to the presence of the vector on the host and forms transmission morphs. eLife 2, e00183.

Bak, A., Irons, S.L., Martinière, A., Blanc, S., and Drucker, M. (2012). Host cell processes to accomplish mechanical and non-circulative virus transmission. Protoplasma 249, 529–539.

Blanc, S., Uzest, M., and Drucker, M. (2011). New research horizons in vector-transmission of plant viruses. Curr Opin Microbiol 14, 483–491.

Martinière, A., Macia, J.-L., Bagnolini, G., Jridi, C., Bak, A., Blanc, S., and Drucker, M. (2011). VAPA, an innovative “virus-acquisition phenotyping assay” opens new horizons in research into the vector-transmission of plant viruses. PloS One 6, e23241.

Uzest, M., Drucker, M., and Blanc, S. (2011). La transmission d’un complexe?: pas si simple. Cas du virus de la mosaïque du chou-fleur. Virologie 15, 192–204.

Hoh, F., Uzest, M., Drucker, M., Plisson-Chastang, C., Bron, P., Blanc, S., and Dumas, C. (2010). Structural insights into the molecular mechanisms of cauliflower mosaic virus transmission by its insect vector. J Virol 84, 4706–4713.

Martinière, A., Zancarini, A., and Drucker, M. (2009). Aphid transmission of cauliflower mosaic virus: the role of the host plant. Plant Signal Behav 4, 548–550.

Martinière, A., Gargani, D., Uzest, M., Lautredou, N., Blanc, S., and 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.

Khelifa, M., Journou, S., Krishnan, K., Gargani, D., Espérandieu, P., Blanc, S., and Drucker, M. (2007). Electron-lucent inclusion bodies are structures specialized for aphid transmission of cauliflower mosaic virus. J Gen Virol 88, 2872–2880.

Drucker, M., Froissart, R., Hébrard, E., Uzest, M., Ravallec, M., Espérandieu, P., Mani, J.C., Pugnière, M., Roquet, F., Fereres, A., and 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.

Palacios, I., Drucker, M., Blanc, S., Leite, S., Moreno, A., and Fereres, A. (2002). Cauliflower mosaic virus is preferentially acquired from the phloem by its aphid vectors. J Gen Virol 83, 3163–3171.