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Feeding cells induced by phytoparasitic nematodes require gamma-tubulin ring complex for microtubule reorganization

Banora, M.Y.; Rodiuc, N.; Baldacci-Cresp, F.; Smertenko, A.; Bleve-Zacheo, T.; Mellilo, M.T.; Karimi, M.; Hilson, P.; J.-l., Evrard; Favery, B.; Engler, G.; Abad, P.; de Almeida-Engler, J.

Feeding cells induced by phytoparasitic nematodes require gamma-tubulin ring complex for microtubule reorganization Thumbnail


Authors

M.Y. Banora

N. Rodiuc

F. Baldacci-Cresp

A. Smertenko

T. Bleve-Zacheo

M.T. Mellilo

M. Karimi

P. Hilson

Evrard J.-l.

B. Favery

G. Engler

P. Abad

J. de Almeida-Engler



Abstract

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.

Citation

Banora, M., Rodiuc, N., Baldacci-Cresp, F., Smertenko, A., Bleve-Zacheo, T., Mellilo, M., …de Almeida-Engler, J. (2011). Feeding cells induced by phytoparasitic nematodes require gamma-tubulin ring complex for microtubule reorganization. PLoS Pathogens, 7(12), Article e1002343. https://doi.org/10.1371/journal.ppat.1002343

Journal Article Type Article
Publication Date Dec 1, 2011
Deposit Date Mar 12, 2012
Publicly Available Date Mar 29, 2024
Journal PLoS Pathogens
Print ISSN 1553-7366
Electronic ISSN 1553-7374
Publisher Public Library of Science
Peer Reviewed Peer Reviewed
Volume 7
Issue 12
Article Number e1002343
DOI https://doi.org/10.1371/journal.ppat.1002343

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Copyright Statement
Copyright: © 2011 Youssef Banora et al. 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 credited.




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