Ectopic expression of Kip-related proteins restrains root-knot nematode-feeding site expansion

Authors

  • Paulo Vieira,

    1. Institut National de la Recherche Agronomique, UMR 1355 ISA/Centre National de la Recherche Scientifique, UMR 7254 ISA/Université de Nice-Sophia Antipolis, UMR ISA, Sophia-Antipolis, France
    Current affiliation:
    1. NemaLab/ICAAM - Instituto de Ciências Agrárias e Ambientais Mediterrânicas, Universidade de Évora, Núcleo da Mitra, Évora, Portugal
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  • Carmen Escudero,

    1. Institut National de la Recherche Agronomique, UMR 1355 ISA/Centre National de la Recherche Scientifique, UMR 7254 ISA/Université de Nice-Sophia Antipolis, UMR ISA, Sophia-Antipolis, France
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  • Natalia Rodiuc,

    1. Institut National de la Recherche Agronomique, UMR 1355 ISA/Centre National de la Recherche Scientifique, UMR 7254 ISA/Université de Nice-Sophia Antipolis, UMR ISA, Sophia-Antipolis, France
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  • Joanna Boruc,

    1. Department of Plant Systems Biology, VIB, Gent, Belgium
    2. Department of Plant Biotechnology and Bioinformatics, Ghent University, Gent, Belgium
    Current affiliation:
    1. Department of Molecular Genetics, The Ohio State University, USA
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  • Eugenia Russinova,

    1. Department of Plant Systems Biology, VIB, Gent, Belgium
    2. Department of Plant Biotechnology and Bioinformatics, Ghent University, Gent, Belgium
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  • Nathalie Glab,

    1. UMR8618, CNRS Université Paris-Sud 11, Orsay, France
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  • Manuel Mota,

    1. NemaLab/ICAAM – Instituto de Ciências Agrárias e Ambientais Mediterrânicas, Universidade de Évora, Núcleo da Mitra, Évora, Portugal
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  • Lieven De Veylder,

    1. Department of Plant Systems Biology, VIB, Gent, Belgium
    2. Department of Plant Biotechnology and Bioinformatics, Ghent University, Gent, Belgium
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  • Pierre Abad,

    1. Institut National de la Recherche Agronomique, UMR 1355 ISA/Centre National de la Recherche Scientifique, UMR 7254 ISA/Université de Nice-Sophia Antipolis, UMR ISA, Sophia-Antipolis, France
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  • Gilbert Engler,

    1. Institut National de la Recherche Agronomique, UMR 1355 ISA/Centre National de la Recherche Scientifique, UMR 7254 ISA/Université de Nice-Sophia Antipolis, UMR ISA, Sophia-Antipolis, France
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  • Janice de Almeida Engler

    Corresponding author
    • Institut National de la Recherche Agronomique, UMR 1355 ISA/Centre National de la Recherche Scientifique, UMR 7254 ISA/Université de Nice-Sophia Antipolis, UMR ISA, Sophia-Antipolis, France
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Author for correspondence:

Janice de Almeida Engler

Tel: +33 492 386 459

Email: janice.almeida-engler@sophia.inra.fr

Summary

  • The development of nematode feeding sites induced by root-knot nematodes involves the synchronized activation of cell cycle processes such as acytokinetic mitoses and DNA amplification. A number of key cell cycle genes are reported to be critical for nematode feeding site development. However, it remains unknown whether plant cyclin-dependent kinase (CDK) inhibitors such as the Arabidopsis interactor/inhibitor of CDK (ICK)/Kip-related protein (KRP) family are involved in nematode feeding site development. This study demonstrates the involvement of Arabidopsis ICK2/KRP2 and ICK1/KRP1 in the control of mitosis to endoreduplication in galls induced by the root-knot nematode Meloidogyne incognita.
  • Using ICK/KRP promoter-GUS fusions and mRNA in situ hybridizations, we showed that ICK2/KRP2, ICK3/KRP5 and ICK4/KRP6 are expressed in galls after nematode infection. Loss-of-function mutants have minor effects on gall development and nematode reproduction. Conversely, overexpression of both ICK1/KRP1 and ICK2/KRP2 impaired mitosis in giant cells and blocked neighboring cell proliferation, resulting in a drastic reduction of gall size.
  • Studying the dynamics of protein expression demonstrated that protein levels of ICK2/KRP2 are tightly regulated during giant cell development and reliant on the presence of the nematode.
  • This work demonstrates that impeding cell cycle progression by means of ICK1/KRP1 and ICK2/KRP2 overexpression severely restricts gall development, leading to a marked limitation of root-knot nematode development and reduced numbers of offspring.

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