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

Janice de Almeida Engler UGent, Kris Van Poucke UGent, Mansour Karimi UGent, Ruth De Groodt, Godelieve Gheysen UGent and Gilbert Engler UGent (2004) PLANT JOURNAL. 38(1). p.12-26
abstract
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.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
cytoskeleton, galls, inhibitors, nematodes, syncytia, IN-SITU HYBRIDIZATION, TUBULIN GENE FAMILY, PLANT ACTIN GENE, ALPHA-TUBULIN, ARABIDOPSIS-THALIANA, MELOIDOGYNE-INCOGNITA, EXPRESSION, MICROTUBULE, HETERODERA-SCHACHTII, SMALL GENOME
journal title
PLANT JOURNAL
Plant J.
volume
38
issue
1
pages
12 - 26
Web of Science type
Article
Web of Science id
000220521800002
JCR category
PLANT SCIENCES
JCR impact factor
6.367 (2004)
JCR rank
6/137 (2004)
JCR quartile
1 (2004)
ISSN
0960-7412
DOI
10.1111/j.1365-313X.2004.02019.x
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
215165
handle
http://hdl.handle.net/1854/LU-215165
date created
2004-05-10 12:06:00
date last changed
2016-12-19 15:38:01
@article{215165,
  abstract     = {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.},
  author       = {de Almeida Engler, Janice and Van Poucke, Kris and Karimi, Mansour and De Groodt, Ruth and Gheysen, Godelieve and Engler, Gilbert},
  issn         = {0960-7412},
  journal      = {PLANT JOURNAL},
  keyword      = {cytoskeleton,galls,inhibitors,nematodes,syncytia,IN-SITU HYBRIDIZATION,TUBULIN GENE FAMILY,PLANT ACTIN GENE,ALPHA-TUBULIN,ARABIDOPSIS-THALIANA,MELOIDOGYNE-INCOGNITA,EXPRESSION,MICROTUBULE,HETERODERA-SCHACHTII,SMALL GENOME},
  language     = {eng},
  number       = {1},
  pages        = {12--26},
  title        = {Dynamic cytoskeleton rearrangements in giant cells and syncytia of nematode-infected roots},
  url          = {http://dx.doi.org/10.1111/j.1365-313X.2004.02019.x},
  volume       = {38},
  year         = {2004},
}

Chicago
de Almeida Engler, Janice, Kris Van Poucke, Mansour Karimi, Ruth De Groodt, Godelieve Gheysen, and Gilbert Engler. 2004. “Dynamic Cytoskeleton Rearrangements in Giant Cells and Syncytia of Nematode-infected Roots.” Plant Journal 38 (1): 12–26.
APA
de Almeida Engler, J., Van Poucke, K., Karimi, M., De Groodt, R., Gheysen, G., & Engler, G. (2004). Dynamic cytoskeleton rearrangements in giant cells and syncytia of nematode-infected roots. PLANT JOURNAL, 38(1), 12–26.
Vancouver
1.
de Almeida Engler J, Van Poucke K, Karimi M, De Groodt R, Gheysen G, Engler G. Dynamic cytoskeleton rearrangements in giant cells and syncytia of nematode-infected roots. PLANT JOURNAL. 2004;38(1):12–26.
MLA
de Almeida Engler, Janice, Kris Van Poucke, Mansour Karimi, et al. “Dynamic Cytoskeleton Rearrangements in Giant Cells and Syncytia of Nematode-infected Roots.” PLANT JOURNAL 38.1 (2004): 12–26. Print.