Martin Drucker

French National Institute for Agricultural Research, Lutetia Parisorum, Île-de-France, France

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Publications (30)98.61 Total impact

  • Martin Drucker · Christiane Then
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    ABSTRACT: Many viruses are transmitted by arthropod vectors. An important mode of transmission is the noncirculative or mechanical transmission where viruses attach to the vector mouthparts for transport to a new host. It has long been assumed that noncirculative transmission is an unsophisticated mode of viral spread, and in the simplest case mere contamination of the vector mouthparts. However, emerging evidence strongly suggests that noncirculative transmission, like other transmission strategies, results from specific interactions between pathogens, hosts, and vectors. Recently, new insights into this concept have been obtained, by demonstrating that a plant virus responds instantly to the presence of its aphid vector on the host by forming transmission morphs. This novel concept, named Transmission Activation (TA), where viruses respond directly or via the host to the outside world, opens new research horizons. Copyright © 2015 Elsevier B.V. All rights reserved.
    No preview · Article · Aug 2015

  • No preview · Article · Jul 2014 · Virologie
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    ABSTRACT: Many viruses form inclusion bodies in infected plant and mamma- lian cells. Their formation often requires membrane rearrangement of various organelles, but some inclusions form in the cytoplasm independently of the endo- membrane system. In the latter case, they may resemble aggresomes or stress bodies but many inclusions do not seem to be related to any cellular structures. Synthesis, composition and size of these inclusions change with virus species. The best characterized inclusions create a “viral organelle” protecting viruses from host defenses and optimizing viral replication and assembly. These inclusions are also called viral factories. Recently, more complex and original functions were described for viral factories. This is exemplified here for Cauliflower mosaic virus (CaMV) factories. Unexpectedly, besides replication, CaMV factories also participate in another crucial step of the viral cycle: vector-transmission by aphids.
    Full-text · Article · Jul 2014 · Virologie
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    Stéphane Blanc · Martin Drucker · Marilyne Uzest
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    ABSTRACT: The mechanisms and impacts of the transmission of plant viruses by insect vectors have been studied for more than a century. The virus route within the insect vector is amply documented in many cases, but the identity, the biochemical properties, and the structure of the actual molecules (or molecule domains) ensuring compatibility between them remain obscure. Increased efforts are required both to identify receptors of plant viruses at various sites in the vector body and to design competing compounds capable of hindering transmission. Recent trends in the field are opening questions on the diversity and sophistication of viral adaptations that optimize transmission, from the manipulation of plants and vectors ultimately increasing the chances of acquisition and inoculation, to specific "sensing" of the vector by the virus while still in the host plant and the subsequent transition to a transmission-enhanced state. Expected final online publication date for the Annual Review of Phytopathology Volume 52 is August 04, 2014. Please see http://www.annualreviews.org/catalog/pubdates.aspx for revised estimates.
    Full-text · Article · Jun 2014 · Annual Review of Phytopathology
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    ABSTRACT: Cauliflower mosaic virus (CaMV) forms two types of inclusion bodies within infected plant cells: numerous virus factories, which are the sites for viral replication and virion assembly, and a single transmission body (TB), which is specialized for virus transmission by aphid vectors. The TB reacts within seconds to aphid feeding on the host plant by total disruption and redistribution of its principal component, the viral transmission helper protein P2, onto microtubules throughout the cell. At the same time, virions also associate with microtubules. This redistribution of P2 and virions facilitates transmission and is reversible: the TB reforms within minutes after vector departure. Although some virions are present in the TB before disruption, their subsequent massive accumulation on the microtubule network suggests that they may also be released from virus factories. Using drug treatments, mutant viruses, and exogenous supply of viral components to infected protoplasts, we show that virions can rapidly exit virus factories and, once in the cytoplasm, accumulate together with the helper protein P2 onto the microtubule network. Moreover, we show that during reversion of this phenomenon, virions from the microtubule network can either be incorporated in the reverted TB or return to the virus factories. Our results suggest that CaMV virus factories are dynamic structures that participate in vector transmission by controlled release and uptake of virions during TB reaction.
    Full-text · Article · Sep 2013 · Journal of Virology
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    ABSTRACT: Aphids infest many plants and cause damage by depriving them of nutrients and by transmitting many viral diseases. Aphid infestation and arbovirus transmission are controlled by establishment (or not) of a compatible reaction between the insects and the plants. This reaction is the result of defense reactions of the plant and counter-defense reactions of the parasite. Contrarily to plant-bacteria, plant-fungi and plant-herbivorous insects pathosystems, the plant-aphid pathosystem is understudied, although recent advances have begun to uncover some of its details. Especially the very early steps in plant-aphid interactions are hardly known. We here resume the present knowledge of these interactions. We discuss further how an aphid-transmitted plant virus that is transmitted during the first moments of the plant-aphid encounter, might help to study the very early plant aphid interactions.
    Full-text · Article · Mar 2013 · Plant signaling & behavior
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    ABSTRACT: Many plant and animal viruses are spread by insect vectors. Cauliflower mosaic virus (CaMV) is aphid-transmitted, with the virus being taken up from specialized transmission bodies (TB) formed within infected plant cells. However, the precise events during TB-mediated virus acquisition by aphids are unknown. Here, we show that TBs react instantly to the presence of the vector by ultra-rapid and reversible redistribution of their key components onto microtubules throughout the cell. Enhancing or inhibiting this TB reaction pharmacologically or by using a mutant virus enhanced or inhibited transmission, respectively, confirming its requirement for efficient virus-acquisition. Our results suggest that CaMV can perceive aphid vectors, either directly or indirectly by sharing the host perception. This novel concept in virology, where viruses respond directly or via the host to the outside world, opens new research horizons, that is, investigating the impact of ‘perceptive behaviors’ on other steps of the infection cycle. DOI: http://dx.doi.org/10.7554/eLife.00183.001
    Full-text · Article · Jan 2013 · eLife Sciences
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    ABSTRACT: Mechanical vector-less transmission of viruses, as well as vector-mediated non-circulative virus transmission, where the virus attaches only to the exterior of the vector during the passage to a new host, are apparently simple processes: the viruses are carried along with the wind, the food or by the vector to a new host. We discuss here, using the examples of the non-circulatively transmitted Cauliflower mosaic virus that binds to its aphid vector's exterior mouthparts, and that of the mechanically (during feeding activity) transmitted Autographa californica multicapsid nucleopolyhedrovirus, that transmission of these viruses is not so simple as previously thought. Rather, these viruses prepare their transmission carefully and long before the actual acquisition event. Host-virus interactions play a pivotal and specialised role in the future encounter with the vector or the new host. This ensures optimal propagation and enlarges the tremendous bottleneck transmission presents for viruses and other pathogens.
    Full-text · Article · Oct 2011 · Protoplasma
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    ABSTRACT: Host-to-host transmission--a key step in plant virus infection cycles--is ensured predominantly by vectors, especially aphids and related insects. A deeper understanding of the mechanisms of virus acquisition, which is critical to vector-transmission, might help to design future virus control strategies, because any newly discovered molecular or cellular process is a potential target for hampering viral spread within host populations. With this aim in mind, an aphid membrane-feeding assay was developed where aphids transmitted two non-circulative viruses [cauliflower mosaic virus (CaMV) and turnip mosaic virus] from infected protoplasts. In this assay, virus acquisition occurs exclusively from living cells. Most interestingly, we also show that CaMV is less efficiently transmitted by aphids in the presence of oryzalin--a microtubule-depolymerising drug. The example presented here demonstrates that our technically simple "virus-acquisition phenotyping assay" (VAPA) provides a first opportunity to implement correlative studies relating the physiological state of infected plant cells to vector-transmission efficiency.
    Full-text · Article · Aug 2011 · PLoS ONE
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    Stéphane Blanc · Marilyne Uzest · Martin Drucker
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    ABSTRACT: Understanding the mechanisms controlling vector-transmission of plant viruses requires integrating information from at least three different viewpoints: virus-vector interactions, plant-vector interactions and virus-plant interactions. While some of these aspects have been covered by past and present investigations, others have been bypassed completely, because of technical bottlenecks or conceptual lacunas. Here, we highlight recent advances and needs in hitherto poorly documented aspects of vector transmission, such as characterization of the vector molecules responsible for initial viral recognition, and the role of vector saliva in inoculation and initial onset of infection in a new plant. We also propose and discuss some novel conceptual and complementary questions that are opening up fascinating new horizons in this field. We explore the possible existence of viral morphs with specific properties that facilitate acquisition by vectors, and discuss the dynamics/genetics of such viral subpopulations, which could differentiate and specialize in different host compartments.
    Full-text · Article · Aug 2011 · Current opinion in microbiology
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    Marilyne Uzest · Martin Drucker · Stephane Blanc
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    ABSTRACT: Transmission by a vector is a common feature among viruses, especially plant viruses. While animal arboviruses infect literally their vector ("biological transmission"), plant viruses are mostly transmitted "mechanically". This mode of transmission is seemingly quite simple - the virus contaminates the vector mouthparts and subsequently is mechanically inoculated into new healthy hosts. In fact, the process involves astonishingly complicated virus-vector interactions that have been the focus of many studies. Nowadays, this phenomenon is considered far from being purely "mechanical" and has been renamed "non-circulative" transmission. In addition to specific ligand/receptor-like interactions between the virus and the vector, sophisticated regulatory mechanisms occur between the host cell and the virus, which seem to be dedicated exclusively to successful virus transmission. The aim of this review is to illustrate, using Cauliflower mosaic virus as a model, the remarkable intricacy of the noncirculative mode of transmission, and possibly instigate analogous research for animal viruses.
    Full-text · Article · May 2011 · Virologie
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    ABSTRACT: 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.
    Full-text · Article · Feb 2010 · Journal of Virology
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    ABSTRACT: Though the duration of a single round of replication is an important biological parameter, it has been determined for only few viruses. Here, this parameter was determined for Cauliflower mosaic virus (CaMV) in transfected protoplasts from different hosts: the highly susceptible Arabidopsis and turnip, and Nicotiana benthamiana, where CaMV accumulates only slowly. Four methods of differing sensitivity were employed: labelling of (1) progeny DNA and (2) capsid protein, (3) immunocapture PCR,, and (4) progeny-specific PCR. The first progeny virus was detected about 21 h after transfection. This value was confirmed by all methods, indicating that our estimate was not biased by the sensitivity of the detection method, and approximated the actual time required for one round of CaMV replication. Unexpectedly, the replication kinetics were similar in the three hosts; suggesting that slow accumulation of CaMV in Nicotiana plants is determined by non-optimal interactions in other steps of the infection cycle.
    Full-text · Article · Nov 2009 · Virology
  • Alexandre Martinière · Anouk Zancarini · Martin Drucker
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    ABSTRACT: Transmission of plant viruses is the result of interactions between a given virus, the host plant, and the vector. Most research has focused on molecular and cellular virus-vector interactions, and the host has only been regarded as a reservoir from which the virus is acquired by the vector more or less accidentally. However, a growing body of evidence suggests that the host can play a crucial role in transmission. Indeed, at least one virus, Cauliflower mosaic virus, exploits the host's cellular pathways to form specialized intracellular structures that optimize virus uptake by the vector and hence transmission.
    No preview · Article · Jun 2009 · Plant signaling & behavior
  • Alexandre Martinière · Anouk Zancarini · Martin Drucker
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    ABSTRACT: Transmission of plant viruses is the result of interactions between a given virus, the host plant, and the vector. Most research has focused on molecular and cellular virus-vector interactions, and the host has only been regarded as a reservoir from which the virus is acquired by the vector more or less accidentally. However, a growing body of evidence suggests that the host can play a crucial role in transmission. Indeed, at least one virus, Cauliflower mosaic virus, exploits the host's cellular pathways to form specialized intracellular structures that optimize virus uptake by the vector and hence transmission.
    No preview · Article · Jun 2009 · Plant signaling & behavior
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    ABSTRACT: Interactions between microtubules and viruses play important roles in viral infection. The best-characterized examples involve transport of animal viruses by microtubules to the nucleus or other intracellular destinations. In plant viruses, most work to date has focused on interaction between viral movement proteins and the cytoskeleton, which is thought to be involved in viral cell-to-cell spread. We show here, in Cauliflower mosaic virus (CaMV)-infected plant cells, that viral electron-lucent inclusion bodies (ELIBs), whose only known function is vector transmission, require intact microtubules for their efficient formation. The kinetics of the formation of CaMV-related inclusion bodies in transfected protoplasts showed that ELIBs represent newly emerging structures, appearing at late stages of the intracellular viral life cycle. Viral proteins P2 and P3 are first produced in multiple electron-dense inclusion bodies, and are later specifically exported to transiently co-localize with microtubules, before concentrating in a single, massive ELIB in each infected cell. Treatments with cytoskeleton-affecting drugs suggested that P2 and P3 might be actively transported on microtubules, by as yet unknown motors. In addition to providing information on the intracellular life cycle of CaMV, our results show that specific interactions between host cell and virus may be dedicated to a later role in vector transmission. More generally, they indicate a new unexpected function for plant cell microtubules in the virus life cycle, demonstrating that microtubules act not only on immediate intracellular or intra-host phenomena, but also on processes ultimately controlling inter-host transmission.
    Full-text · Article · Apr 2009 · The Plant Journal
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    Full-text · Article · Jan 2008 · Virologie
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    ABSTRACT: Du fait de l'immobilité de leurs hôtes, l'immense majorité des virus de plante utilisent des vecteurs spécifiques pour passer d'un hôte à un autre. Ces "véhicules de transport" sont principalement des arthropodes et en grande majorité des pucerons, qui sont des insectes de type piqueur-suceur. Pour les interactions virus-vecteur, la stratégie la plus communément utilisée par les virus de plante est la transmission dite non circulante, où les particules virales prélevées lors d'un repas dans les cellules infectées seront retenues au niveau de sites d'attachement dans les pièces buccales antérieures de l'insecte sans effectuer de passage à l'intérieur de son organisme. Ces particules virales seront ensuite relarguées de ces sites d'attachement lors de piqûres sur de nouvelles cellules hôtes et induiront ainsi l'infection dans de nouvelles plantes. Si les mécanismes moléculaires de la transmission non circulante sont bien documentés en ce qui concerne le partenaire viral, les sites d'attachement correspondants dans les stylets du vecteur demeurent la principale "boîte noire" pour laquelle aucune donnée n'est disponible. Malgré l'importance de ce mode de transmission, l'existence même d'un récepteur spécifique n'a jamais été prouvée pour aucun virus. Dans une étude très récemment publiée, nous avons localisé précisément le récepteur du Caulifower mosaic virus (CaMV) et déterminé sa nature chimique.
    Full-text · Article · Jan 2008 · Virologie
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    ABSTRACT: Hundreds of species of plant viruses, many of them economically important, are transmitted by noncirculative vector transmission (acquisition by attachment of virions to vector mouthparts and inoculation by subsequent release), but virus receptors within the vector remain elusive. Here we report evidence for the existence, precise location, and chemical nature of the first receptor for a noncirculative virus, cauliflower mosaic virus, in its insect vector. Electron microscopy revealed virus-like particles in a previously undescribed anatomical zone at the extreme tip of the aphid maxillary stylets. A novel in vitro interaction assay characterized binding of cauliflower mosaic virus protein P2 (which mediates virus-vector interaction) to dissected aphid stylets. A P2-GFP fusion exclusively labeled a tiny cuticular domain located in the bottom-bed of the common food/salivary duct. No binding to stylets of a non-vector species was observed, and a point mutation abolishing P2 transmission activity correlated with impaired stylet binding. The novel receptor appears to be a nonglycosylated protein deeply embedded in the chitin matrix. Insight into such insect receptor molecules will begin to open the major black box of this scientific field and might lead to new strategies to combat viral spread.
    Full-text · Article · Dec 2007 · Proceedings of the National Academy of Sciences
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    ABSTRACT: Cauliflower mosaic virus (CaMV) is transmitted by aphids. For acquisition by the vector, a transmissible complex must form, composed of the virus particle, the viral coat-associated protein P3 and the helper protein P2. However, the components of the transmissible complex are largely separated in infected plant cells: most P3 virions are confined in electron-dense inclusion bodies, whereas P2 is sequestered in electron-lucent inclusion bodies (elIBs). This spatial separation controls virus acquisition by favouring the binding of virus-free P2 to the vector first, rendering the vector competent for later uptake of P3 virions. Consequently, sequential acquisition of virus from different cells or tissues is possible, with important implications for the biology of CaMV transmission. CaMV strains Campbell and CM1841 contain a single amino acid mutation (G94R) in the helper protein P2, rendering them non-transmissible from plant to plant. However, the mutant P2-94 protein supports aphid transmission when expressed heterologously and supplied to P3-CaMV complexes in vitro. The non-transmissibility of P2-94 was re-examined in vivo and it is shown here that the non-transmissibility of this P2 mutant is not due to low accumulation levels in infected plants, as suggested previously, but more specifically to the failure to form elIBs within infected plant cells. This demonstrates that elIBs are complex viral structures specialized for aphid transmission and suggests that viral inclusion bodies other than viral factories, most often considered as 'garbage cans', can in fact exhibit specific functions.
    Full-text · Article · Nov 2007 · Journal of General Virology

Publication Stats

586 Citations
98.61 Total Impact Points

Institutions

  • 2007-2013
    • French National Institute for Agricultural Research
      • Biologie et Génétique des Interactions Plantes-parasites pour la Protection Intégrée
      Lutetia Parisorum, Île-de-France, France
  • 2009-2011
    • Montpellier SupAgro
      Montpelhièr, Languedoc-Roussillon, France
  • 2002-2010
    • French National Centre for Scientific Research
      • Laboratoire de Biologie Moléculaire Eucaryote (LBME)
      Lutetia Parisorum, Île-de-France, France
    • Spanish National Research Council
      Madrid, Madrid, Spain
  • 2005
    • Université de Montpellier 1
      • Centre de Biochimie Structurale (CBS)
      Montpelhièr, Languedoc-Roussillon, France