Reorganization of the plant cytoskeleton is thought to play an important role during nodule ontogeny. In situ immunolocalisation of tubulin reveals that important cytoskeletal changes, implying a transient disorganization followed by a newly patterned reorganization, occur in indeterminate and determinate nodules. In alfalfa nodules, cytoskeletal changes closely parallel the symbiotic differentiation features related to cell infection, bacterial release, endopolyploidization, cell enlargement, cell spatial organization and organelle ultrastructure and positioning. Moreover, the fact that microtubule disorganization can be correlated with Nod factor internalization in central infected cells suggests that Nod factors are possibly involved in the control of cytoskeletal changes which direct the differentiation of bacteria-containing cells.
REFERENCES
REFERENCES
Ardourel
M.
, Demont
N.
, Debelle
F.
, Maillet
F.
, De Billy
F.
, Prome
J.-C.
, Denarie
J.
, Truchet
G.
(1994
) Rhizobium meliloti lipooligosaccharide nodulation factors: different structural requirements for bacterial entry into target root hair cells and induction of plant symbiotic developmental responses.
Plant Cell
6
, 1357
–1374
Bakhuizen
R.
, Van Spronsen
P. C.
, Sluiman-Den Hertog
F. A. J.
, Venverloo
C. J.
, Goosen-De Roo
L.
(1985
) Nuclear envelope radiating microtubules in plant cells during interphase mitosis transition.
Protoplasma
128
, 43
–51
Baluska
F.
, Parker
J. S.
, Barlow
P. W.
(1992
). Specific patterns of cortical and endoplasmic microtubules associated with cell growth and tissue differentiation in roots of maize (Zea mays L.).
J. Cell Sci
103
, 191
–200
Bershadsky
A.
, Chausovsky
A.
, Becker
E.
, Lyubimova
A.
, Geiger
B.
(1996
) Involvement of microtubules in the control of adhesion-dependent signal transduction.
Curr. Biol
6
, 1279
–1289
Blanchard
V.
, Raisman-Vozari
R.
, Savasta
M.
, Hirsch
E.
, Javoy-Agid
F.
, Feuerstein
C.
, Agid
Y.
(1993
) Cellular quantification of tyrosine hydroxylase in the rat brain by immunoautoradiography.
J. Neurochem
61
, 617
–626
Bono
J.-J.
, Riond
J.
, Nicolaou
K. C.
, Bockovich
N. J.
, Estevez
V. A.
, Cullimore
J. V.
, Ranjeva
R.
(1995
) Characterization of a binding site for chemically synthesized lipo-oligosaccharidic NodRm factors in particulate fractions prepared from roots.
Plant J
7
, 253
–260
Brewin
N. J.
(1991
) Development of the legume root nodule.
Ann.Rev. Cell Biol
7
, 191
–226
Brown
R. C.
, Lemmon
B. E.
, Olsen
O.-A.
(1994
) Endosperm development in barley: microtubule involvement in the morphogenetic pathway.
Plant Cell
6
, 1241
–1252
Callaham
D. A.
, Torrey
J. G.
(1981
) The structural basis for infection of root hairs of Trifolium repens by Rhizobium.
Can. J. Bot
59
, 1647
–1664
Cole
N. B.
, Lippincott-Schwartz
J.
(1995
) Organization of organelles and membrane traffic by microtubules.
Curr. Opin. Cell Biol
7
, 55
–64
Crossin
K. L.
, Carney
D. H.
(1981
) Evidence that microtubule depolymerization early in the cell cycle is sufficient to initiate DNA synthesis.
Cell
23
, 61
–71
Cyr
R. J.
(1994
) Microtubules in plant morphogenesis: role of the cortical array.
Ann. Rev. Cell Biol
10
, 153
–180
Cyr
R. J.
, Palevitz
B. A.
(1995
) Organization of cortical microtubules in plant cells.
Curr. Opin. Cell Biol
7
, 65
–71
Denarie
J.
, Debelle
F.
, Prome
J.-C.
(1996
) Rhizobium lipo-chitooligosaccharide nodulation factors: Signaling molecules mediating recognition and morphogenesis.
Ann. Rev. Biochem
65
, 503
–535
Djordjevic
M. A.
, Schofield
P. R.
, Rolfe
B. G.
(1985
) Tn5 mutagenesis of Rhizobium trifolii host-specific nodulation genes result in mutants with altered host-range ability.
Mol. Gen. Genet
200
, 463
–471
Ehrhardt
D. W.
, Atkinson
E. M.
, Long
S. R.
(1992
) Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors.
Science
256
, 998
–1000
Ehrhardt
D. W.
, Wais
R.
, Long
S. R.
(1996
) Calcium spiking in plant root hairs responding to Rhizobium nodulation signals.
Cell
85
, 673
–681
Engvall
E.
, Perlmann
P.
(1971
) Enzyme-linked immunosorbent assay (ELISA).
Quantitative assay of immunoglobulin G. Immunochem
8
, 871
–874
Felle
H. H.
, Kondorosi
E.
, Kondorosi
A.
(1995
) Nod-signal induced plasma membrane potential changes in alfalfa root hairs are differentially sensitive to structural modifications of the lipochito-oligosaccharide.
Plant J
7
, 939
–947
Foussard
M.
, Garnerone
A.-M.
, Ni
F.
, Soupene
E.
, Boistard
P.
, Batut
J.
(1997
) Negative autoregulation of the Rhizobium meliloti fixK gene is indirect and requires a newly identified regulator, FixT.
Mol. Microbiol
25
, 27
–37
Goddard
R. H.
, Wick
S. W.
, Silflow
C. D.
, Sunstad
D. P.
(1994
) Microtubule components of the plant cell cytoskeleton.
Plant Physiol
104
, 1
–6
Lambert
A.-M.
(1993
) Microtubule-organizing centers in higher plants.
Curr. Opin. Cell Biol
5
, 116
–122
Leigh
J. A.
, Signer
E. R.
, Walker
G. C.
(1985
) Exopolysaccharide-deficient mutants of Rhizobium meliloti that form ineffective nodules.
Proc. Natl. Acad. Sci. USA
82
, 6231
–6235
Liu
B.
, Joshi
H. C.
, Wilson
T. J.
, Silflow
C. D.
, Palevitz
B. A.
, Snustad
D. P.
(1994
) -Tubulin in Arabidopsis : Gene sequence, immunoblot, and immunofluorescence studies.
Plant Cell
6
, 303
–314
Panteris
E.
, Apostolakos
P.
, Galatis
B.
(1995
) Telophase-interphase transition in taxol-treated Triticum root cells: cortical microtubules appearwithout the prior presence of a radial perinuclear array.
Protoplasma
188
, 78
–84
Philip-Hollingsworth
S.
, Dazzo
F. B.
, Hollingsworth
R.
(1997
) Structural requirements of Rhizobium chitolipooligosaccharides for uptake and bioactivity in legume roots as revealed by synthetic analogs and fluorescent probes.
J. Lipid Res
38
, 1229
–1241
Roche
P.
, Debelle
F.
, Maillet
F.
, Lerouge
P.
, Faucher
C.
, Truchet
G.
, Denarie
J.
, Prome
J.-C.
(1991
) Molecular basis of symbiotic host specificity in Rhizobium meliloti: nodH and nodPQ genes encode the sulfation of lipo-oligosaccharide signals.
Cell
67
, 1131
–1143
Roth
L. E.
, Stacey
G.
(1989
) Bacterium release into host cells of nitrogen-fixing soybean nodules: The symbiosome membrane comes from three sources.
Eur. J. Cell Biol
49
, 13
–23
Schlaman
H. R. M.
, Horvath
B.
, Vijgenboom
E.
, Okker
R. J. H.
, Lugtenberg
B. J. J.
(1991
) Suppression of nodulation gene expression in bacteroids of Rhizobium leguminosarum bv. viciae.
J. Bacteriol
173
, 4277
–4287
Schultze
M.
, Kondorosi
A.
(1996
) The role of lipooligosaccharides in root nodule organogenesis and plant cell growth.
Curr. Opin. Genet. Devel
6
, 631
–638
Truchet
G.
, Barker
D. G.
, Camut
S.
, De Billy
F.
, Vasse
J.
, Huguet
T.
(1989
) Alfalfa nodulation in the absence of Rhizobium.
Mol. Gen. Genet
219
, 65
–68
Truchet
G.
, Coulomb
P.
(1973
). Mise en evidence et evolution du systeme phytolysosomal dans les cellules des differentes zones de nodules radiculaires de pois (Pisum sativum L.). Notion d'heterophagie.
J. Ultrastruct. Res
43
, 36
–57
Truchet
G.
, Roche
P.
, Lerouge
P.
, Vasse
J.
, Camut
S.
, De Billy
F.
, Prome
J.-C.
, Denarie
J.
(1991
) Sulfated lipo-oligosaccharide signals ofRhizobium meliloti elicit root nodule organogenesis in alfalfa.
Nature
351
, 670
–673
Van Brussel
A. A. N.
, Bakhuizen
R.
, Van Spronsen
P. C.
, Spaink
H. P.
, Tak
T.
, Lugtenberg
B. J. J.
, Kijne
J. W.
(1992
) Induction of preinfection thread structures in the leguminous host plant by mitogenic lipooligosaccharides of Rhizobium.
Science
2547
, 70
–72
Van Brussel
A. A. N.
, Zaat
S. A. J.
, Canter Cremers
H. C. J.
, Wijfellman
C. A.
, Pees
E.
, Tak
T.
, Lugtenberg
B. J. J.
(1986
) Role of plant root exudate and Sym plasmid-localized nodulation genes in the synthesis by Rhizobium leguminosarum of Tsr factor, which causes thick and short roots on common vetch.
J. Bacteriol
165
, 517
–522
Van Spronsen
P. C.
, Van Brussel
A. A. N.
, Kijne
J. W.
(1995
) Nod factors produced by Rhizobium leguminosarum biovar viciae induce ethylene-related changes in root cortical cells of Vicia sativa ssp. nigra.
Eur. J. Cell Biol
68
, 463
–469
Vasse
J.
, de Billy
F.
, Camut
S.
, Truchet
G.
(1990
) Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules.
J. Bacteriol
172
, 4295
–4306
Warren
G.
, Wickner
W.
(1996
) Organelle inheritance.
Cell
84
, 395
–400
Williamson
R. E.
(1991
) Orientation of cortical microtubules in interphase plant cells.
Int. Rev. Cytol
129
, 135
–206
Yaffe
M. P.
, Harata
D.
, Verde
F.
, Eddison
M.
, Toda
T.
, Nurse
P.
(1996
) Microtubules mediate mitochondrial distribution in fission yeast.
Proc. Natl. Acad. Sci. USA
93
, 11664
–11668
Yang
W.-C.
, De Blank
C.
, Meskiene
I.
, Hirt
H.
, Bakker
J.
, Van Kammen
A.
, Franssen
H.
, Bisseling
T.
(1994
) Rhizobium Nod factors reactivate the cell cycle during infection and nodule primordium formation, but the cycle is only completed in primordium formation.
Plant Cell
6
, 1415
–1426
This content is only available via PDF.
© 1998 by Company of Biologists
1998
