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Deciphering the route of Ralstonia solanacearum colonization in Arabidopsis thaliana roots during a compatible interaction: focus at the plant cell wall

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Abstract

The compatible interaction between the model plant, Arabidopsis thaliana, and the GMI1000 strain of the phytopathogenic bacterium, Ralstonia solanacearum, was investigated in an in vitro pathosystem. We describe the progression of the bacteria in the root from penetration at the root surface to the xylem vessels and the cell type-specific, cell wall-associated modifications that accompanies bacterial colonization. Within 6 days post inoculation, R. solanacearum provoked a rapid plasmolysis of the epidermal, cortical, and endodermal cells, including those not directly in contact with the bacteria. Plasmolysis was accompanied by a global degradation of pectic homogalacturonanes as shown by the loss of JIM7 and JIM5 antibody signal in the cell wall of these cell types. As indicated by immunolabeling with Rsol-I antibodies that specifically recognize R. solanacearum, the bacteria progresses through the root in a highly directed, centripetal manner to the xylem poles, without extensive multiplication in the intercellular spaces along its path. Entry into the vascular cylinder was facilitated by cell collapse of the two pericycle cells located at the xylem poles. Once the bacteria reached the xylem vessels, they multiplied abundantly and moved from vessel to vessel by digesting the pit membrane between adjacent vessels. The degradation of the secondary walls of xylem vessels was not a prerequisite for vessel colonization as LM10 antibodies strongly labeled xylem cell walls, even at very late stages in disease development. Finally, the capacity of R. solanacearum to specifically degrade certain cell wall components and not others could be correlated with the arsenal of cell wall hydrolytic enzymes identified in the bacterial genome.

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Abbreviations

dpi:

Days post-inoculation

HG:

Homogalacturonan

PEL:

Pectate lyase

PG:

Polygalacturonase

PL:

Pectin lyase

PME:

Pectin methylesterase

TEM:

Transmission electron microscopy

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Acknowledgments

The authors would like to thank Stéphane Genin and Alice Guidot (LIPM, Toulouse, France) for helpful discussions, and Françoise Poliakoff, Corrine Audusseau and Carène Rivoal (ANSES-Laboratoire de la Santé des Végétaux, Angers, France) for the generous gift of Rsol-I antibody. This work was funded by the French National Agency for Research (WALLTALK: ANR-07-GPLA-014).

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Authors and Affiliations

  1. Université de Toulouse, UPS, UMR 5546, Laboratoire de Recherche en Sciences Végétales, BP 42617, 31326, Castanet-Tolosan, France

    Catherine Digonnet, Nicolas Denancé, Marine Chasseray, Philippe Ranocha & Deborah Goffner

  2. Centre National de la Recherche Scientifique, CNRS, UMR 5546, Laboratoire de Recherche en Sciences Végétales, BP 42617, 31326, Castanet-Tolosan, France

    Catherine Digonnet, Nicolas Denancé, Marine Chasseray, Philippe Ranocha & Deborah Goffner

  3. Centre National de la Recherche Scientifique, CNRS, Plateforme Imagerie-Microscopie, Fédération de Recherche FR3450, 24 Chemin de Borde Rouge, 31326, Castanet-Tolosan, France

    Yves Martinez & Alain Jauneau

  4. Institut National de la Recherche Agronomique, INRA, UMR 441, Laboratoire des Interactions Plantes Microorganismes, 24 Chemin de Borde Rouge, 31326, Castanet-Tolosan, France

    Patrick Dabos & Yves Marco

  5. Centre National de la Recherche Scientifique, CNRS, UMR 2594, Laboratoire des Interactions Plantes Microorganismes, 24 Chemin de Borde Rouge, 31326, Castanet-Tolosan, France

    Patrick Dabos & Yves Marco

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  1. Catherine Digonnet
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  2. Yves Martinez
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  3. Nicolas Denancé
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  9. Deborah Goffner
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Correspondence to Deborah Goffner.

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C. Digonnet and Y. Martinez contributed equally to this work.

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Digonnet, C., Martinez, Y., Denancé, N. et al. Deciphering the route of Ralstonia solanacearum colonization in Arabidopsis thaliana roots during a compatible interaction: focus at the plant cell wall. Planta 236, 1419–1431 (2012). https://doi.org/10.1007/s00425-012-1694-y

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