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

Driouich, Azeddine; Baskin, Tobias I.

doi:10.3732/ajb.0800277

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

Journal Article · Mon Dec 01 00:00:00 EST 2008 · American Journal of Botany

DOI:https://doi.org/10.3732/ajb.0800277· OSTI ID:2483295

Driouich, Azeddine ^[1]; Baskin, Tobias I. ^[2]

Plateforme de Recherche en Imagerie Cellulaire de Haute Normandie (PRIMACEN)–Université de Rouen, Mont Saint Aignan (France)
University of Massachusetts, Amherst, MA (United States)

How does a plant cell sense and respond to the status of its cell wall? Intercourse between cell wall and cytoplasm has long been supposed to involve arabinogalactan proteins, in part because many of them are anchored to the plasma membrane. Disrupting arabinogalactan proteins has recently been shown to disrupt the array of cortical microtubules present just inside the plasma membrane, implying that microtubules and arabinogalactan proteins interact. In this article, we assess possibilities for how this interaction might be mediated. First, we consider microdomains in the plasma membrane (lipid rafts), which have been alleged to link internal and external regions of the plasma membrane; however, the characteristics and even the existence of these domains remains controversial. Next, we point out that disrupting the synthesis of cellulose also can disrupt microtubules and consider whether arabinogalactan proteins are part of a network linking microtubules and nascent microfibrils. Finally, we outline several signaling cascades that could transmit information from arabinogalactan proteins to microtubules through channels of cellular communication. Furthermore, these diverse possibilities highlight the work that remains to be done before we can understand how plant cells communicate across their membranes.

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:: 2483295

Journal Information:: American Journal of Botany, Journal Name: American Journal of Botany Journal Issue: 12 Vol. 95; ISSN 0002-9122

Publisher:: Wiley - Botanical Society of AmericaCopyright Statement

Country of Publication:: United States

Language:: English

References (53)

Cytoskeletal elements of chick embryo fibroblasts revealed by detergent extraction Brown, Susan; Levinson, Warren; Spudich, James A. Journal of Supramolecular Structure, Vol. 5, Issue 2 https://doi.org/10.1002/jss.400050203	journal	January 1976
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
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
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
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
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
Lipid Rafts Munro, Sean Cell, Vol. 115, Issue 4 https://doi.org/10.1016/S0092-8674(03)00882-1	journal	November 2003
Nanoscale Organization of Multiple GPI-Anchored Proteins in Living Cell Membranes Sharma, Pranav; Varma, Rajat; Sarasij, R. C. Cell, Vol. 116, Issue 4 https://doi.org/10.1016/S0092-8674(04)00167-9	journal	February 2004
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
A Receptor-like Kinase Mediates the Response of Arabidopsis Cells to the Inhibition of Cellulose Synthesis Hématy, Kian; Sado, Pierre-Etienne; Van Tuinen, Ageeth Current Biology, Vol. 17, Issue 11 https://doi.org/10.1016/j.cub.2007.05.018	journal	June 2007
Nucleotide sugar interconversions and cell wall biosynthesis: how to bring the inside to the outside Seifert, Georg J. Current Opinion in Plant Biology, Vol. 7, Issue 3 https://doi.org/10.1016/j.pbi.2004.03.004	journal	June 2004
A proteoglycan mediates inductive interaction during plant vascular development Motose, Hiroyasu; Sugiyama, Munetaka; Fukuda, Hiroo Nature, Vol. 429, Issue 6994 https://doi.org/10.1038/nature02613	journal	June 2004
Lipid rafts: at a crossroad between cell biology and physics Jacobson, Ken; Mouritsen, Ole G.; Anderson, Richard G. W. Nature Cell Biology, Vol. 9, Issue 1 https://doi.org/10.1038/ncb0107-7	journal	January 2007
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
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
Yariv reagent treatment induces programmed cell death in Arabidopsis cell cultures and implicates arabinogalactan protein involvement Gao, Minggeng; Showalter, Allan M. The Plant Journal, Vol. 19, Issue 3 https://doi.org/10.1046/j.1365-313X.1999.00544.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
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
Morlin, an inhibitor of cortical microtubule dynamics and cellulose synthase movement DeBolt, S.; Gutierrez, R.; Ehrhardt, D. W. Proceedings of the National Academy of Sciences, Vol. 104, Issue 14 https://doi.org/10.1073/pnas.0700789104	journal	March 2007
Lipid Rafts in Higher Plant Cells: PURIFICATION AND CHARACTERIZATION OF TRITON X-100-INSOLUBLE MICRODOMAINS FROM TOBACCO PLASMA MEMBRANE Mongrand, Sébastien; Morel, Johanne; Laroche, Jeanny Journal of Biological Chemistry, Vol. 279, Issue 35 https://doi.org/10.1074/jbc.M403440200	journal	June 2004
A "Microtubule" in Plant cell fine Structure Ledbetter, M. C. The Journal of Cell Biology, Vol. 19, Issue 1 https://doi.org/10.1083/jcb.19.1.239	journal	October 1963
Microtubules and Fibrils in the Cytoplasm of Coleus Cells Undergoing Secondary wall Deposition Hepler, P. K. The Journal of Cell Biology, Vol. 20, Issue 3 https://doi.org/10.1083/jcb.20.3.529	journal	March 1964
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
n -Butanol induces depolymerization of microtubules in vivo and in vitro Hirase, Ai; Hamada, Takahiro; Itoh, Tomohiko J. Plant and Cell Physiology, Vol. 47, Issue 7 https://doi.org/10.1093/pcp/pcj055	journal	July 2006
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
Chemical Genetic Screening Identifies a Novel Inhibitor of Parallel Alignment of Cortical Microtubules and Cellulose Microfibrils Yoneda, Arata; Higaki, Takumi; Kutsuna, Natsumaro Plant and Cell Physiology, Vol. 48, Issue 10 https://doi.org/10.1093/pcp/pcm120	journal	October 2007
COBRA encodes a putative GPI-anchored protein, which is polarly localized and necessary for oriented cell expansion in Arabidopsis Schindelman, G. Genes & Development, Vol. 15, Issue 9 https://doi.org/10.1101/gad.879101	journal	May 2001
Binding of Arabinogalactan Proteins by Yariv Phenylglycoside Triggers Wound-Like Responses in Arabidopsis Cell Cultures Guan, Yu; Nothnagel, Eugene A. Plant Physiology, Vol. 135, Issue 3 https://doi.org/10.1104/pp.104.039370	journal	July 2004
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
Analysis of Detergent-Resistant Membranes in Arabidopsis. Evidence for Plasma Membrane Lipid Rafts Borner, Georg H. H.; Sherrier, D. Janine; Weimar, Thilo Plant Physiology, Vol. 137, Issue 1 https://doi.org/10.1104/pp.104.053041	journal	December 2004
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
Characterization of Lipid Rafts from Medicago truncatula Root Plasma Membranes: A Proteomic Study Reveals the Presence of a Raft-Associated Redox System Lefebvre, Benoit; Furt, Fabienne; Hartmann, Marie-Andrée Plant Physiology, Vol. 144, Issue 1 https://doi.org/10.1104/pp.106.094102	journal	March 2007
N-Acetylglucosamine and Glucosamine-Containing Arabinogalactan Proteins Control Somatic Embryogenesis van Hengel, Arjon J.; Tadesse, Zewdie; Immerzeel, Peter Plant Physiology, Vol. 125, Issue 4 https://doi.org/10.1104/pp.125.4.1880	journal	April 2001
A 90-kD Phospholipase D from Tobacco Binds to Microtubules and the Plasma Membrane Gardiner, John C.; Harper, John D. I.; Weerakoon, Nimalika D. The Plant Cell, Vol. 13, Issue 9 https://doi.org/10.1105/TPC.010114	journal	September 2001
The Arabidopsis SOS5 Locus Encodes a Putative Cell Surface Adhesion Protein and Is Required for Normal Cell Expansion Shi, Huazhong; Kim, YongSig; Guo, Yan The Plant Cell, Vol. 15, Issue 1 https://doi.org/10.1105/tpc.007872	journal	December 2002
COBRA, an Arabidopsis Extracellular Glycosyl-Phosphatidyl Inositol-Anchored Protein, Specifically Controls Highly Anisotropic Expansion through Its Involvement in Cellulose Microfibril Orientation Roudier, François; Fernandez, Anita G.; Fujita, Miki The Plant Cell, Vol. 17, Issue 6 https://doi.org/10.1105/tpc.105.031732	journal	April 2005
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
Disruption of arabinogalactan proteins disorganizes cortical microtubules in the root of Arabidopsis thaliana Nguema‐Ona, Eric; Bannigan, Alex; Chevalier, Laurence The Plant Journal, Vol. 52, Issue 2 https://doi.org/10.1111/j.1365-313X.2007.03224.x	journal	August 2007
Sentinels at the wall: cell wall receptors and sensors Humphrey, Tania V.; Bonetta, Dario T.; Goring, Daphne R. New Phytologist, Vol. 176, Issue 1 https://doi.org/10.1111/j.1469-8137.2007.02192.x	journal	October 2007
Phospholipase C signaling involvement in macrotubule assembly and activation of the mechanism regulating protoplast volume in plasmolyzed root cells ofTriticum turgidum Komis, George; Galatis, Basil; Quader, Hartmut New Phytologist, Vol. 178, Issue 2 https://doi.org/10.1111/j.1469-8137.2007.02363.x	journal	January 2008
Rafts: Scale-Dependent, Active Lipid Organization at the Cell Surface: Raft Hypothesis Mayor, Satyajit; Rao, Madan Traffic, Vol. 5, Issue 4 https://doi.org/10.1111/j.1600-0854.2004.00172.x	journal	March 2004
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
Phenovariation induced in Streptocarpus prolixus (Gesneriaceae) by β-glucosyl Yariv reagent Rauh, Richard A.; Basile, Dominick V. Canadian Journal of Botany, Vol. 81, Issue 4 https://doi.org/10.1139/b03-030	journal	April 2003
The effects of taxol and colchicine on microtubule and microfibril arrays in elongating plant cells in culture Weerdenburg, Carol; Seagull, Robert W. Canadian Journal of Botany, Vol. 66, Issue 9 https://doi.org/10.1139/b88-234	journal	September 1988
The Biology of Arabinogalactan Proteins Seifert, Georg J.; Roberts, Keith Annual Review of Plant Biology, Vol. 58, Issue 1 https://doi.org/10.1146/annurev.arplant.58.032806.103801	journal	June 2007
Model Systems, Lipid Rafts, and Cell Membranes Simons, Kai; Vaz, Winchil L. C. Annual Review of Biophysics and Biomolecular Structure, Vol. 33, Issue 1 https://doi.org/10.1146/annurev.biophys.32.110601.141803	journal	June 2004
Membrane Domains Mukherjee, Sushmita; Maxfield, Frederick R. Annual Review of Cell and Developmental Biology, Vol. 20, Issue 1 https://doi.org/10.1146/annurev.cellbio.20.010403.095451	journal	November 2004
Arabinogalactan-Proteins: Structure, Biosynthesis, and Function Fincher, G. B.; Stone, B. A.; Clarke, A. E. Annual Review of Plant Physiology, Vol. 34, Issue 1 https://doi.org/10.1146/annurev.pp.34.060183.000403	journal	June 1983
Thematic review series: Lipid Posttranslational Modifications. GPI anchoring of protein in yeast and mammalian cells, or: how we learned to stop worrying and love glycophospholipids Peter, Orlean; Menon, Anant K. Journal of Lipid Research, Vol. 48, Issue 5 https://doi.org/10.1194/jlr.R700002-JLR200	journal	May 2007
Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis Benfey, P. N.; Linstead, P. J.; Roberts, K. Development, Vol. 119, Issue 1 https://doi.org/10.1242/dev.119.1.57	journal	September 1993

Similar Records

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

Journal Article · Mon Aug 20 20:00:00 EDT 2007 · The Plant Journal · OSTI ID:2483293

The Fragile Fiber1 Kinesin Contributes to Cortical Microtubule-Mediated Trafficking of Cell Wall Components

Journal Article · Sun Feb 01 19:00:00 EST 2015 · Plant Physiology (Bethesda) · OSTI ID:2483313

Making parallel lines meet: Transferring information from microtubules to extracellular matrix

Journal Article · Sun Aug 19 20:00:00 EDT 2012 · Cell adhesion & migration · OSTI ID:2483304

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
arabinogalactan protein
cell wall
cellular communication
cortical microtubules
morphogenesis
roots
signaling cascades

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

Citation Formats

References (53)

Similar Records

Related Subjects