Disruption of arabinogalactan proteins disorganizes cortical microtubules in the root of Arabidopsis thaliana

Nguema‐Ona, Eric; Bannigan, Alex; Chevalier, Laurence; Baskin, Tobias I.; Driouich, Azeddine

doi:10.1111/j.1365-313x.2007.03224.x

Disruption of arabinogalactan proteins disorganizes cortical microtubules in the root of Arabidopsis thaliana

Journal Article · Tue Aug 21 00:00:00 EDT 2007 · The Plant Journal

DOI:https://doi.org/10.1111/j.1365-313x.2007.03224.x· OSTI ID:2483293

Nguema‐Ona, Eric ^[1]; Bannigan, Alex ^[2]; Chevalier, Laurence ^[1]; Baskin, Tobias I. ^[2]; Driouich, Azeddine ^[1]

Université de Rouen (France)
University of Massachusetts, Amherst, MA (United States)

The cortical array of microtubules inside the cell and arabinogalactan proteins on the external surface of the cell are each implicated in plant morphogenesis. To determine whether the cortical array is influenced by arabinogalactan proteins, we first treated Arabidopsis roots with a Yariv reagent that binds arabinogalactan proteins. Cortical microtubules were markedly disorganized by 1 μmβ-d-glucosyl (active) Yariv but not by up to 10 μmβ-d-mannosyl (inactive) Yariv. This was observed for 24-h treatments in wild-type roots, fixed and stained with anti-tubulin antibodies, as well as in living roots expressing a green fluorescent protein (GFP) reporter for microtubules. Using the reporter line, microtubule disorganization was evident within 10 min of treatment with 5 μm active Yariv and extensive by 30 min. Active Yariv (5 μm) disorganized cortical microtubules after gadolinium pre-treatment, suggesting that this effect is independent of calcium influx across the plasma membrane. Similar effects on cortical microtubules, over a similar time scale, were induced by two anti-arabinogalactan-protein antibodies (JIM13 and JIM14) but not by antibodies recognizing pectin or xyloglucan epitopes. Active Yariv, JIM13, and JIM14 caused arabinogalactan proteins to aggregate rapidly, as assessed either in fixed wild-type roots or in the living cells of a line expressing a plasma membrane-anchored arabinogalactan protein from tomato fused to GFP. Finally, electron microscopy of roots prepared by high-pressure freezing showed that treatment with 5 μm active Yariv for 2 h significantly increased the distance between cortical microtubules and the plasma membrane. Furthermore, these findings demonstrate that cell surface arabinogalactan proteins influence the organization of cortical microtubules.

View Accepted Manuscript (DOE)

Research Organization:: University of Massachusetts, Amherst, MA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB)

Grant/Contract Number:: FG02-03ER15421

OSTI ID:: 2483293

Journal Information:: The Plant Journal, Journal Name: The Plant Journal Journal Issue: 2 Vol. 52; ISSN 0960-7412

Publisher:: Society for Experimental BiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (57)

Higher plant cortical microtubule array analyzed in vitro in the presence of the cell wall Tian, Guo‐Wei; Smith, Damien; Glück, Susanne Cell Motility, Vol. 57, Issue 1 https://doi.org/10.1002/cm.10153	journal	November 2003
Field emission scanning electron microscopy of microtubule arrays in higher plant cells Vesk, Peter A.; Vesk, Maret; Gunning, Brian E. S. Protoplasma, Vol. 195, Issue 1-4 https://doi.org/10.1007/BF01279195	journal	March 1996
On the alignment of cellulose microfibrils by cortical microtubules: A review and a model Baskin, Tobias I. Protoplasma, Vol. 215, Issue 1-4 https://doi.org/10.1007/BF01280311	journal	March 2001
Comparison of the ultrastructure of conventionally fixed and high pressure frozen/freeze substituted root tips ofNicotiana andArabidopsis Kiss, J. Z.; Giddings, Th. H.; Staehelin, L. A. Protoplasma, Vol. 157, Issue 1-3 https://doi.org/10.1007/BF01322639	journal	February 1990
Effects of Yariv phenylglycosides onRosa cell suspensions: Evidence for the involvement of arabinogalactan-proteins in cell proliferation Serpe, Marcelo D.; Nothnagel, Eugene A. Planta, Vol. 193, Issue 4 https://doi.org/10.1007/BF02411560	journal	May 1994
Spatiotemporal relationships between growth and microtubule orientation as revealed in living root cells ofArabidopsis thaliana transformed with green-fluorescent-protein gene constructGFP-MBD Granger, C. L.; Cyr, R. J. Protoplasma, Vol. 216, Issue 3-4 https://doi.org/10.1007/BF02673872	journal	September 2001
The reb1-1 mutation of Arabidopsis alters the morphology of trichoblasts, the expression of arabinogalactan-proteins and the organization of cortical microtubules Andème-Onzighi, Christine; Sivaguru, Mayandi; Judy-March, Jan Planta, Vol. 215, Issue 6 https://doi.org/10.1007/s00425-002-0836-z	journal	October 2002
A role for arabinogalactan-proteins in root epidermal cell expansion Ding, Lei; Zhu, Jian-Kang Planta, Vol. 203, Issue 3 https://doi.org/10.1007/s004250050194	journal	October 1997
Effects of Yariv phenylglycoside on cell wall assembly in the lily pollen tube Roy, Stéphane; Jauh, Guang Yuh; Hepler, Peter K. Planta, Vol. 204, Issue 4 https://doi.org/10.1007/s004250050279	journal	March 1998
Arabinogalactan proteins, pollen tube growth, and the reversible effects of Yariv phenylglycoside Mollet, Jean-Claude; Kim, Sunran; Jauh, Guang-Yuh Protoplasma, Vol. 219, Issue 1-2 https://doi.org/10.1007/s007090200009	journal	February 2002
Antibodies against a Gossypium hirsutum recombinant cellulose synthase (Ces A) specifically label cellulose synthase in Micrasterias denticulata Nakashima, Jin; Heathman, Amy; Brown, R. Malcolm Cellulose, Vol. 13, Issue 2 https://doi.org/10.1007/s10570-006-9059-y	journal	March 2006
The role of calcium in cell division Hepler, P. K. Cell Calcium, Vol. 16, Issue 4 https://doi.org/10.1016/0143-4160(94)90096-5	journal	October 1994
Proteoglycans and Related Components in Plant Cells Nothnagel, Eugene A. International Review of Cytology https://doi.org/10.1016/S0074-7696(08)62118-X	book	January 1997
WAKs; cell wall associated kinases Kohorn, Bruce D. Current Opinion in Cell Biology, Vol. 13, Issue 5 https://doi.org/10.1016/S0955-0674(00)00247-7	journal	October 2001
Galactose Biosynthesis in Arabidopsis Seifert, Georg J.; Barber, Christine; Wells, Brian Current Biology, Vol. 12, Issue 21 https://doi.org/10.1016/S0960-9822(02)01260-5	journal	October 2002
Delivering Force and Amplifying Signals in Plant Mechanosensing Pickard, Barbara G. Current Topics in Membranes https://doi.org/10.1016/S1063-5823(06)58014-7	book	January 2007
Progress in understanding the role of microtubules in plant cells Wasteneys, Geoffrey O. Current Opinion in Plant Biology, Vol. 7, Issue 6 https://doi.org/10.1016/j.pbi.2004.09.008	journal	December 2004
Biosynthesis of plant cell wall polysaccharides — a complex process Lerouxel, Olivier; Cavalier, David M.; Liepman, Aaron H. Current Opinion in Plant Biology, Vol. 9, Issue 6 https://doi.org/10.1016/j.pbi.2006.09.009	journal	December 2006
β-Glucosyl and α-Galactosyl Yariv Reagents Bind to Cellulose and Other Glucans Triplett, Barbara A.; Timpa, Judy D. Journal of Agricultural and Food Chemistry, Vol. 45, Issue 12 https://doi.org/10.1021/jf970390h	journal	December 1997
The complex structures of arabinogalactan-proteins and the journey towards understanding function Gaspar, Yolanda; Johnson, Kim L.; McKenna, James A. Plant Molecular Biology, Vol. 47, p. 161-176 https://doi.org/10.1023/A:1010683432529	journal	January 2001
Growth of the plant cell wall Cosgrove, Daniel J. Nature Reviews Molecular Cell Biology, Vol. 6, Issue 11, p. 850-861 https://doi.org/10.1038/nrm1746	journal	November 2005
The interaction of glycosides and saccharides with antibody to the corresponding phenylazo glycosides Yariv, J.; Rapport, Mm; Graf, L. Biochemical Journal, Vol. 85, Issue 2 https://doi.org/10.1042/bj0850383	journal	November 1962
Precipitation of arabic acid and some seed polysaccharides by glycosylphenylazo dyes Yariv, J.; Lis, H.; Katchalski, E. Biochemical Journal, Vol. 105, Issue 1 https://doi.org/10.1042/bj1050001C	journal	October 1967
A new approach for cryofixation by high-pressure freezing Studer, D.; Graber, W.; Al-Amoudi, A. Journal of Microscopy, Vol. 203, Issue 3 https://doi.org/10.1046/j.1365-2818.2001.00919.x	journal	September 2001
Developmentally regulated epitopes of cell surface arabinogalactan proteins and their relation to root tissue pattern formation Knox, J. P.; Linstead, P. J.; Cooper, J. Peart C. The Plant Journal, Vol. 1, Issue 3 https://doi.org/10.1046/j.1365-313X.1991.t01-9-00999.x	journal	November 1991
A role for arabinogalactan-proteins in plant cell expansion: evidence from studies on the interaction of beta-glucosyl Yariv reagent with seedlings of Arabidopsis thaliana Willats, William G. T.; Knox, J. Paul The Plant Journal, Vol. 9, Issue 6 https://doi.org/10.1046/j.1365-313X.1996.9060919.x	journal	June 1996
Uncoupling secretion and tip growth in lily pollen tubes: evidence for the role of calcium in exocytosis Roy, Stéphane J.; Holdaway‐Clarke, Terena L.; Hackett, Grant R. The Plant Journal, Vol. 19, Issue 4 https://doi.org/10.1046/j.1365-313X.1999.00515.x	journal	August 1999
Ca2+ pulsation in BY-2 cells and evidence for control of mechanosensory Ca2+-selective channels by the plasmalemmal reticulum Pickard, Barbara G.; Fujiki, Masaaki Functional Plant Biology, Vol. 32, Issue 10 https://doi.org/10.1071/FP05045	journal	January 2005
Alignment of Cortical Microtubules by Anisotropic Wall Stresses Williamson, Re Functional Plant Biology, Vol. 17, Issue 6 https://doi.org/10.1071/PP9900601	journal	January 1990
Root Morphology Mutants in Arabidopsis thaliana Baskin, Ti; Betzner, As; Hoggart, R. Functional Plant Biology, Vol. 19, Issue 4 https://doi.org/10.1071/PP9920427	journal	January 1992
Arabinogalactan-proteins from Nicotiana alata and Pyrus communis contain glycosylphosphatidylinositol membrane anchors Youl, Joelian J.; Bacic, Antony; Oxley, David Proceedings of the National Academy of Sciences, Vol. 95, Issue 14 https://doi.org/10.1073/pnas.95.14.7921	journal	July 1998
Structure of the glycosylphosphatidylinositol anchor of an arabinogalactan protein from Pyrus communis suspension-cultured cells Oxley, D.; Bacic, A. Proceedings of the National Academy of Sciences, Vol. 96, Issue 25 https://doi.org/10.1073/pnas.96.25.14246	journal	December 1999
Experimental evidence for a mechanical function of the cellulose microfibril angle in wood cell walls Reiterer, A.; Lichtenegger, H.; Tschegg, S. Philosophical Magazine A, Vol. 79, Issue 9 https://doi.org/10.1080/01418619908210415	journal	September 1999
Aluminum Rapidly Depolymerizes Cortical Microtubules and Depolarizes the Plasma Membrane: Evidence that these Responses are Mediated by a Glutamate Receptor Sivaguru, Mayandi; Pike, Sharon; Gassmann, Walter Plant and Cell Physiology, Vol. 44, Issue 7 https://doi.org/10.1093/pcp/pcg094	journal	July 2003
Isolation and Identification of Glycosylphosphatidylinositol-Anchored Arabinogalactan Proteins and Novel β-Glucosyl Yariv-Reactive Proteins from Seeds of Rice (Oryza sativa) Mashiguchi, Kiyoshi; Yamaguchi, Isomaro; Suzuki, Yoshihito Plant and Cell Physiology, Vol. 45, Issue 12 https://doi.org/10.1093/pcp/pch208	journal	December 2004
Cortical Microtubule Arrays Lose Uniform Alignment Between Cells and are Oryzalin Resistant in the Arabidopsis Mutant, radially swollen 6 Bannigan, Alex; Wiedemeier, Allison M. D.; Williamson, Richard E. Plant and Cell Physiology, Vol. 47, Issue 7 https://doi.org/10.1093/pcp/pcj067	journal	July 2006
Wall Ingrowths in Epidermal Transfer Cells of Vicia faba Cotyledons are Modified Primary Walls Marked by Localized Accumulations of Arabinogalactan Proteins Vaughn, K. C.; Talbot, M. J.; Offler, C. E. Plant and Cell Physiology, Vol. 48, Issue 1 https://doi.org/10.1093/pcp/pcl047	journal	December 2006
Using Genomic Resources to Guide Research Directions. The Arabinogalactan Protein Gene Family as a Test Case Schultz, Carolyn J.; Rumsewicz, Michael P.; Johnson, Kim L. Plant Physiology, Vol. 129, Issue 4 https://doi.org/10.1104/pp.003459	journal	August 2002
Disorganization of Cortical Microtubules Stimulates Tangential Expansion and Reduces the Uniformity of Cellulose Microfibril Alignment among Cells in the Root of Arabidopsis Baskin, Tobias I.; Beemster, Gerrit T. S.; Judy-March, Jan E. Plant Physiology, Vol. 135, Issue 4 https://doi.org/10.1104/pp.104.040493	journal	August 2004
Root Border-Like Cells of Arabidopsis. Microscopical Characterization and Role in the Interaction with Rhizobacteria Vicré, Maïté; Santaella, Catherine; Blanchet, Sandrine Plant Physiology, Vol. 138, Issue 2 https://doi.org/10.1104/pp.104.051813	journal	May 2005
Characterization of Synthetic Hydroxyproline-Rich Proteoglycans with Arabinogalactan Protein and Extensin Motifs in Arabidopsis Estévez, José M.; Kieliszewski, Marcia J.; Khitrov, Natalie Plant Physiology, Vol. 142, Issue 2 https://doi.org/10.1104/pp.106.084244	journal	August 2006
Molecular Interactions of Arabinogalactan Proteins with Cortical Microtubules and F-Actin in Bright Yellow-2 Tobacco Cultured Cells Sardar, Harjinder Singh; Yang, Jie; Showalter, Allan M. Plant Physiology, Vol. 142, Issue 4 https://doi.org/10.1104/pp.106.088716	journal	October 2006
Extending the Microtubule/Microfibril Paradigm: Cellulose Synthesis Is Required for Normal Cortical Microtubule Alignment in Elongating Cells Fisher, Deborah D.; Cyr, Richard J. Plant Physiology, Vol. 116, Issue 3 https://doi.org/10.1104/pp.116.3.1043	journal	March 1998
The Multiple Roles of Arabinogalactan Proteins in Plant Development Majewska-Sawka, Anna; Nothnagel, Eugene A. Plant Physiology, Vol. 122, Issue 1 https://doi.org/10.1104/pp.122.1.3	journal	January 2000
Mutation or Drug-Dependent Microtubule Disruption Causes Radial Swelling without Altering Parallel Cellulose Microfibril Deposition in Arabidopsis Root Cells Sugimoto, Keiko; Himmelspach, Regina; Williamson, Richard E. The Plant Cell, Vol. 15, Issue 6 https://doi.org/10.1105/tpc.011593	journal	May 2003
The Classical Arabinogalactan Protein Gene Family of Arabidopsis Schultz, Carolyn J.; Johnson, Kim L.; Currie, Graeme The Plant Cell, Vol. 12, Issue 9 https://doi.org/10.1105/tpc.12.9.1751	journal	September 2000
Isolation of a 90-kD Microtubule-Associated Protein from Tobacco Membranes. Marc, J.; Sharkey, D. E.; Durso, N. A. The Plant Cell https://doi.org/10.1105/tpc.8.11.2127	journal	November 1996
Mechanotransduction and the glycocalyx Tarbell, J. M.; Pahakis, M. Y. Journal of Internal Medicine, Vol. 259, Issue 4 https://doi.org/10.1111/j.1365-2796.2006.01620.x	journal	March 2006
Spatial variation in H₂O₂ response of Arabidopsis thaliana root epidermal Ca²⁺ flux and plasma membrane Ca²⁺ channels Demidchik, Vadim; Shabala, Sergey N.; Davies, Julia M. The Plant Journal, Vol. 49, Issue 3 https://doi.org/10.1111/j.1365-313X.2006.02971.x	journal	January 2007
Do microtubules orient plant cell wall microfibrils? Emons, A. M. C.; Derksen, J.; Sassen, M. M. A. Physiologia Plantarum, Vol. 84, Issue 3 https://doi.org/10.1111/j.1399-3054.1992.tb04695.x	journal	March 1992
Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development Demidchik, Vadim; Maathuis, Frans J. M. New Phytologist, Vol. 175, Issue 3 https://doi.org/10.1111/j.1469-8137.2007.02128.x	journal	June 2007
Visualization of Cellulose Synthase Demonstrates Functional Association with Microtubules Paredez, A. R. Science, Vol. 312, Issue 5779 https://doi.org/10.1126/science.1126551	journal	June 2006
Remodeling the Cytoskeleton for Growth and Form: An Overview with Some New Views Wasteneys, Geoffrey O.; Galway, Moira E. Annual Review of Plant Biology, Vol. 54, Issue 1 https://doi.org/10.1146/annurev.arplant.54.031902.134818	journal	June 2003
Anisotropic Expansion of the Plant cell wall Baskin, Tobias I. Annual Review of Cell and Developmental Biology, Vol. 21, Issue 1 https://doi.org/10.1146/annurev.cellbio.20.082503.103053	journal	November 2005
Organogenesis-A Biophysical View Green, P. B. Annual Review of Plant Physiology, Vol. 31, Issue 1 https://doi.org/10.1146/annurev.pp.31.060180.000411	journal	June 1980
Plant Hormone-Induced Changes in the Orientation of Cortical Microtubules: Alterations in the Cross-linking Between Microtubules and the Plasma Membrane Shibaoka, H. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 45, Issue 1 https://doi.org/10.1146/annurev.pp.45.060194.002523	journal	June 1994
Involvement of transmembrane proteins in the association of cortical microtubules with the plasma membrane in tobacco BY-2 cells Akashi, Tomohiro; Shibaoka, Hiroh Journal of Cell Science, Vol. 98, Issue 2 https://doi.org/10.1242/jcs.98.2.169	journal	February 1991

Similar Records

Intercourse between cell wall and cytoplasm exemplified by arabinogalactan proteins and cortical microtubules

Journal Article · Sun Nov 30 19:00:00 EST 2008 · American Journal of Botany · OSTI ID:2483295

Microtubule-dependent microtubule nucleation based on recruitment of γ-tubulin in higher plants

Journal Article · Sat Sep 03 20:00:00 EDT 2005 · Nature Cell Biology · OSTI ID:2483286

Imaging cellulose synthase motility during primary cell wall synthesis in the grass Brachypodium distachyon

Journal Article · Tue Nov 07 19:00:00 EST 2017 · Scientific Reports · OSTI ID:1507735

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
arabinogalactan protein
cell wall
cryofixation
microtubules
morphogenesis
root growth

Disruption of arabinogalactan proteins disorganizes cortical microtubules in the root of Arabidopsis thaliana

Citation Formats

References (57)

Similar Records

Related Subjects