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Feeding Cells Induced by Phytoparasitic Nematodes Require γ-Tubulin Ring Complex for Microtubule Reorganization

Reorganization of the microtubule network is important for the fast isodiametric expansion of giant-feeding cells induced by root-knot nematodes. The efficiency of microtubule reorganization depends on the nucleation of new microtubules, their elongation rate and activity of microtubule severing fac...

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Autores principales: Banora, Mohamed Youssef, Rodiuc, Natalia, Baldacci-Cresp, Fabien, Smertenko, Andrei, Bleve-Zacheo, Teresa, Mellilo, Maria Teresa, Karimi, Mansour, Hilson, Pierre, Evrard, Jean-Luc, Favery, Bruno, Engler, Gilbert, Abad, Pierre, de Almeida Engler, Janice
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2011
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3228788/
https://www.ncbi.nlm.nih.gov/pubmed/22144887
http://dx.doi.org/10.1371/journal.ppat.1002343
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author Banora, Mohamed Youssef
Rodiuc, Natalia
Baldacci-Cresp, Fabien
Smertenko, Andrei
Bleve-Zacheo, Teresa
Mellilo, Maria Teresa
Karimi, Mansour
Hilson, Pierre
Evrard, Jean-Luc
Favery, Bruno
Engler, Gilbert
Abad, Pierre
de Almeida Engler, Janice
author_facet Banora, Mohamed Youssef
Rodiuc, Natalia
Baldacci-Cresp, Fabien
Smertenko, Andrei
Bleve-Zacheo, Teresa
Mellilo, Maria Teresa
Karimi, Mansour
Hilson, Pierre
Evrard, Jean-Luc
Favery, Bruno
Engler, Gilbert
Abad, Pierre
de Almeida Engler, Janice
author_sort Banora, Mohamed Youssef
collection PubMed
description Reorganization of the microtubule network is important for the fast isodiametric expansion of giant-feeding cells induced by root-knot nematodes. The efficiency of microtubule reorganization depends on the nucleation of new microtubules, their elongation rate and activity of microtubule severing factors. New microtubules in plants are nucleated by cytoplasmic or microtubule-bound γ-tubulin ring complexes. Here we investigate the requirement of γ-tubulin complexes for giant feeding cells development using the interaction between Arabidopsis and Meloidogyne spp. as a model system. Immunocytochemical analyses demonstrate that γ-tubulin localizes to both cortical cytoplasm and mitotic microtubule arrays of the giant cells where it can associate with microtubules. The transcripts of two Arabidopsis γ-tubulin (TUBG1 and TUBG2) and two γ-tubulin complex proteins genes (GCP3 and GCP4) are upregulated in galls. Electron microscopy demonstrates association of GCP3 and γ-tubulin as part of a complex in the cytoplasm of giant cells. Knockout of either or both γ-tubulin genes results in the gene dose-dependent alteration of the morphology of feeding site and failure of nematode life cycle completion. We conclude that the γ-tubulin complex is essential for the control of microtubular network remodelling in the course of initiation and development of giant-feeding cells, and for the successful reproduction of nematodes in their plant hosts.
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spelling pubmed-32287882011-12-05 Feeding Cells Induced by Phytoparasitic Nematodes Require γ-Tubulin Ring Complex for Microtubule Reorganization Banora, Mohamed Youssef Rodiuc, Natalia Baldacci-Cresp, Fabien Smertenko, Andrei Bleve-Zacheo, Teresa Mellilo, Maria Teresa Karimi, Mansour Hilson, Pierre Evrard, Jean-Luc Favery, Bruno Engler, Gilbert Abad, Pierre de Almeida Engler, Janice PLoS Pathog Research Article Reorganization of the microtubule network is important for the fast isodiametric expansion of giant-feeding cells induced by root-knot nematodes. The efficiency of microtubule reorganization depends on the nucleation of new microtubules, their elongation rate and activity of microtubule severing factors. New microtubules in plants are nucleated by cytoplasmic or microtubule-bound γ-tubulin ring complexes. Here we investigate the requirement of γ-tubulin complexes for giant feeding cells development using the interaction between Arabidopsis and Meloidogyne spp. as a model system. Immunocytochemical analyses demonstrate that γ-tubulin localizes to both cortical cytoplasm and mitotic microtubule arrays of the giant cells where it can associate with microtubules. The transcripts of two Arabidopsis γ-tubulin (TUBG1 and TUBG2) and two γ-tubulin complex proteins genes (GCP3 and GCP4) are upregulated in galls. Electron microscopy demonstrates association of GCP3 and γ-tubulin as part of a complex in the cytoplasm of giant cells. Knockout of either or both γ-tubulin genes results in the gene dose-dependent alteration of the morphology of feeding site and failure of nematode life cycle completion. We conclude that the γ-tubulin complex is essential for the control of microtubular network remodelling in the course of initiation and development of giant-feeding cells, and for the successful reproduction of nematodes in their plant hosts. Public Library of Science 2011-12-01 /pmc/articles/PMC3228788/ /pubmed/22144887 http://dx.doi.org/10.1371/journal.ppat.1002343 Text en Youssef Banora et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Banora, Mohamed Youssef
Rodiuc, Natalia
Baldacci-Cresp, Fabien
Smertenko, Andrei
Bleve-Zacheo, Teresa
Mellilo, Maria Teresa
Karimi, Mansour
Hilson, Pierre
Evrard, Jean-Luc
Favery, Bruno
Engler, Gilbert
Abad, Pierre
de Almeida Engler, Janice
Feeding Cells Induced by Phytoparasitic Nematodes Require γ-Tubulin Ring Complex for Microtubule Reorganization
title Feeding Cells Induced by Phytoparasitic Nematodes Require γ-Tubulin Ring Complex for Microtubule Reorganization
title_full Feeding Cells Induced by Phytoparasitic Nematodes Require γ-Tubulin Ring Complex for Microtubule Reorganization
title_fullStr Feeding Cells Induced by Phytoparasitic Nematodes Require γ-Tubulin Ring Complex for Microtubule Reorganization
title_full_unstemmed Feeding Cells Induced by Phytoparasitic Nematodes Require γ-Tubulin Ring Complex for Microtubule Reorganization
title_short Feeding Cells Induced by Phytoparasitic Nematodes Require γ-Tubulin Ring Complex for Microtubule Reorganization
title_sort feeding cells induced by phytoparasitic nematodes require γ-tubulin ring complex for microtubule reorganization
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3228788/
https://www.ncbi.nlm.nih.gov/pubmed/22144887
http://dx.doi.org/10.1371/journal.ppat.1002343
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