Dynamic cytoskeleton rearrangements in giant cells and syncytia of nematode-infected roots

Authors

  • Janice De Almeida Engler,

    1. Department of Plant Systems Biology, Flanders Interuniversity Institute for Biotechnology (VIB), Ghent University, B-9052 Gent, Belgium,
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      Present address: Institute National de la Recherche Agronomique, UMR Interactions Plantes-Microorganismes et Santé Végétale, B.P. 167, F-06903 Sophia Antipolis, France.
  • Kris Van Poucke,

    1. Department of Plant Systems Biology, Flanders Interuniversity Institute for Biotechnology (VIB), Ghent University, B-9052 Gent, Belgium,
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  • Mansour Karimi,

    1. Department of Plant Systems Biology, Flanders Interuniversity Institute for Biotechnology (VIB), Ghent University, B-9052 Gent, Belgium,
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  • Ruth De Groodt,

    1. Department of Plant Systems Biology, Flanders Interuniversity Institute for Biotechnology (VIB), Ghent University, B-9052 Gent, Belgium,
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  • Greetje Gheysen,

    1. Department of Plant Systems Biology, Flanders Interuniversity Institute for Biotechnology (VIB), Ghent University, B-9052 Gent, Belgium,
    2. Vakgroep Moleculaire Biotechnologie, Faculteit Landbouwkundige en Toegepaste Wetenschappen, Universiteit Gent, B-9000 Gent, Belgium, and
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  • Gilbert Engler,

    Corresponding author
    1. Laboratoire Associé de l'Institut National de la Recherche Agronomique (France), Universiteit Gent, B-9000 Gent, Belgium
      For correspondence (fax +33 493678955; e-mail
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      Present address: Institute National de la Recherche Agronomique, UMR Interactions Plantes-Microorganismes et Santé Végétale, B.P. 167, F-06903 Sophia Antipolis, France.
  • Godelieve Gheysen

    1. Department of Plant Systems Biology, Flanders Interuniversity Institute for Biotechnology (VIB), Ghent University, B-9052 Gent, Belgium,
    2. Vakgroep Moleculaire Biotechnologie, Faculteit Landbouwkundige en Toegepaste Wetenschappen, Universiteit Gent, B-9000 Gent, Belgium, and
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For correspondence (fax +33 493678955; e-mail gengler@antibes.inra.fr).
Present address: Institute National de la Recherche Agronomique, UMR Interactions Plantes-Microorganismes et Santé Végétale, B.P. 167, F-06903 Sophia Antipolis, France.

Summary

Giant cells induced by root knot nematodes and syncytia caused by cyst nematodes are large multinucleated feeding cells containing a dense cytoplasm generated during a complex host–parasite association in plant roots. To find out whether cytoskeleton changes occurred during feeding cell development, transcriptional activity of actin (ACT) and tubulin genes and organization of the ACT filaments and of the microtubules (MTs) were analyzed in situ. The importance of changes in the cytoskeleton architecture for the proper initiation and development of galls and syncytia was demonstrated by perturbing the cytoskeleton with chemical inhibitors. The expression levels of cytoskeletal components, such as tubulins and ACTs, are proposed to be upregulated to allow the assembly of a new cytoskeleton in expanding feeding cells. However, MTs and ACT filaments failed to properly organize and appeared partially depolymerized throughout feeding site development. Both the actin and tubulin cytoskeletons were strongly disrupted in syncytia and mitotic figures were never observed. In contrast, in giant cells, an ACT and cortical MT cytokeleton, although disturbed, was still visible. In addition, a functional mitotic apparatus was present that contained multiple large spindles and arrested phragmoplasts, but no pre-prophase bands. Chemical stabilization of the microtubular cytoskeleton with taxol blocked feeding site development. On the other hand, when the ACT or MT cytoskeleton of feeding cells was depolymerized by cytochalasin D or oryzalin, nematodes could complete their life cycle. Our data suggest that the cytoskeleton rearrangements and depolymerization induced by parasitic nematodes may be essential for a successful feeding process.

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