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Proteins reacting with cadherin and catenin antibodies are present in maize showing tissue-, domain-, and development-specific associations with endoplasmic-reticulum membranes and actin microfilaments in root cells

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Summary

With heterologous antibodies raised against animal N-cadherin, α-catenin, and β-catenin, we have visualized their reactive proteins within cells of maize root apices. Embedding using Steedman's wax allowed us to accomplish tissue-specific analysis which revealed that cells of epidermis, endodermis/pericycle, and outer stele tissues, all of which are tightly associated to each other, are especially enriched with presumed plant homologues of N-cadherin and both catenins. In the root epidermis, trichoblasts initiating root hairs showed prominent accumulations of cadherin-like antigens at outgrowing domains where they co-localize with actin. Close associations of cadherin-like proteins with F-actin were detected in parenchymatic cells of the stele, also at the immunogold electron microscopy level. A possible role of these interesting proteins in membrane-membrane interactions is indicated by their prominent accumulations at endoplasmic-reticulum-enriched pit-field-based plant cell adhesion domains in plasmolyzing cells of maize root apices exposed to mannitol. Intriguingly, these unique adhesion domains of plasmolyzing cells are enriched with endoplasmic-reticulum-resident calreticulin. Cadherin-like, but not catenin-like, proteins were abundant also within the nucleoplasm.

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Abbreviations

AGPs:

arabinogalactan proteins

EM:

electron microscopy

ER:

endoplasmic reticulum

MFs:

microfilaments

SB:

stabilizing buffer

References

  • Abe S, Ito Y, Davies E (1992) Co-sedimentation of actin, tubulin and membranes in the cytoskeleton fractions from peas and mouse 3T3 cells. J Exp Bot 43: 941–949

    Google Scholar 

  • Adams CL, Nelson WJ, Smith SJ (1996) Quantitative analysis of cadherin-catenin-actin reorganization during development of cell-cell adhesion. J Cell Biol 135: 1899–1911

    Google Scholar 

  • Baluška F, Volkmann D, Barlow PW (1996) Specialized zones of development in roots: view from the cellular level. Plant Physiol 112: 3–4

    Google Scholar 

  • —, Vitha S, Barlow PW, Volkmann D (1997) Rearrangements of F- actin arrays in growing cells of intact maize root apex tissues: a major developmental switch occurs in the postmitotic transition region. Eur J Cell Biol 72: 113–121

    Google Scholar 

  • Barth AIM, Nähtke IS, Nelson WJ (1997) Cadherins, catenins and APC protein: interplay between cytoskeletal complexes and signalling pathways. Curr Opin Cell Biol 9: 683–690

    Google Scholar 

  • Bissell MJ, Barcellos-Hoff MH (1987) The influence of extracellular matrix on gene expression: is structure the message? J Cell Sci Suppl 8: 327–343

    Google Scholar 

  • Burridge K, Fath K, Kelly T, Nuckolls G, Turner C (1988) Focal adhesions: transmembrane junctions between the extracellular matrix and the cytoskeleton. Annu Rev Cell Biol 4: 487–525

    Google Scholar 

  • Craig S, Staehelin LA (1988) High pressure freezing of intact plant tissues: evaluation and characterization of novel features of the endoplasmic reticulum and associated membrane systems. Eur J Cell Biol 46: 80–93

    Google Scholar 

  • De Ruijter N, Emons AM (1993) Immunodetection of spectrin antigens in plant cells. Cell Biol Int 17: 169–182

    Google Scholar 

  • Du H, Clarke AE, Bacic A (1996) Arabinogalactan-proteins: a class of extracellular matrix proteoglycans involved in plant growth and development. Trends Cell Biol 6: 411–414

    Google Scholar 

  • Ettinger L, Doljanski F (1992) On the generation of form by continuous interactions between cells and their extracellular matrix. Biol Rev 67: 459–489

    Google Scholar 

  • Faraday CD, Spanswick RM (1993) Evidence for a membrane skeleton in higher plants: a spectrin-like polypeptide co-isolates with rice root plasma membranes. FEBS Lett 318: 313–316

    Google Scholar 

  • Fowler JE, Quatrano RS (1997) Plant cell morphogenesis: plasma membrane interactions with the cytoskeleton and cell wall. Annu Rev Cell Dev Biol 13: 697–743

    Google Scholar 

  • Gens JS, Reuzeau C, Doolittle KW, McNally JG, Pickard BG (1996) Covisualization by computational optical-sectioning microscopy of integrin and associated proteins at the cell membrane of living onion protoplasts. Protoplasma 194: 215–230

    Google Scholar 

  • Goodbody KC, Venverloo CJ, Lloyd CW (1991) Laser microsurgery demonstrates that cytoplasmic strands anchoring the nucleus across the vacuole of premitotic plant cells are under tension: implications for division plane alignment. Development 113: 931–939

    Google Scholar 

  • Goosen-de Roo L, Burggraaf PD, Libbenga KR (1983) Microfilament bundles associated with tubular endoplasmic reticulum in fusiform cells in the active cambial zone oFFraxinus excelsior L. Protoplasma 116: 204–208

    Google Scholar 

  • Grabski S, Xie XG, Holland JF, Schindler M (1994) Lipids trigger changes in the elasticity of the cytoskeleton in plant cells: a cell optical displacement assay for live cell measurements. J Cell Biol 126: 713–726

    Google Scholar 

  • Gumbiner BM (1996) Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 84: 345–357

    Google Scholar 

  • Hahne G, Hoffman F (1984) The effect of laser microsurgery on cytoplasmic strands and cytoplasmic streaming in isolated plant protoplasts. Eur J Cell Biol 33: 175–179

    Google Scholar 

  • Hepler PK, Palevitz BA, Lancelle SA, McCauley MM, Lichtscheidl IK (1990) Cortical endoplasmic reticulum in plants. J Cell Sci 96: 355–373

    Google Scholar 

  • Huber O, Bierkamp C, Kemler R (1996) Cadherins and catenins in development. Curr Opin Cell Biol 8: 685–691

    Google Scholar 

  • Hynes RO (1987) Integrins: a family a cell surface receptors. Cell 48: 549–554

    Google Scholar 

  • Ingber DE (1993) Extracellular matrix as a regulator of epithelial polarity, cell growth, and tissue pattern. In: Vay Liang W Go (ed) The pancreas: biology, pathobiology, and disease. Raven, New York, pp 369–380

    Google Scholar 

  • Kachar B, Reese TS (1988) The mechanism of cytoplasmic streaming in characean algal cells: sliding of endoplasmic reticulum along actin filaments. J Cell Biol 106: 1545–1552

    Google Scholar 

  • Kaminskyj SGW, Heath IB (1995) Integrin and spectrin homologues, and cytoplasm-wall adhesion in tip growth, J Cell Sci 108: 849–856

    Google Scholar 

  • Katembe WJ, Swatzell LJ, Makaroff CA, Kiss JZ (1997) Immunolocalization of integrin-like proteins inArabidopsis andChara. Physiol Plant 99: 7–14

    Google Scholar 

  • Knebel W, Quader H, Schnepf E (1990) Mobile and immobile endoplasmic reticulum in onion bulb epidermis cells: short- and longterm observations with a confocal laser scanning microscope. Eur J Cell Biol 52: 328–340

    Google Scholar 

  • Knight A, Kendrick-Jones J (1993) A myosin-like protein from a higher plant. J Mol Biol 231: 148–154

    Google Scholar 

  • Knoblauch M, van Bel AJE (1998) Sieve tubes in action. Plant Cell 10: 35–50

    Google Scholar 

  • Knudsen KA, Soler AP, Johnson KR, Wheelock MJ (1995) Interaction of α-actinin with the cadherin/catenin cell-cell adhesion complex via α-catenin. J Cell Biol 130: 67–77

    Google Scholar 

  • Lee C, Ferguson M, Chen LB (1989) Construction of the endoplasmic reticulum. J Cell Biol 109: 2045–2055

    Google Scholar 

  • Li Y-Q, Moscatelli A, Cai G, Cresti M (1997) Functional interactions among cytoskeleton, membranes, and cell wall in the pollen tube of flowering plants. Int Rev Cytol 176: 133–199

    Google Scholar 

  • Lichtscheidl IK, Url WG (1990) Organization and dynamics of cortical endoplasmic reticulum in inner epidermal cells of onion bulb scales. Protoplasma 157: 203–215

    Google Scholar 

  • —, Lancelle SA, Hepler PK (1990) Actin-endoplasmic reticulum complexes inDrosera: their structural relationship with the plasmalemma, nucleus, and organelles in cells prepared by high pressure freezing. Protoplasma 155: 116–126

    Google Scholar 

  • Liebe S, Menzel D (1995) Actomyosin-based motility of endoplasmic reticulum and chloroplasts inVallisneria mesophyll cells. Biol Cell 85: 207–222

    Google Scholar 

  • Luna EJ, Hitt AL (1992) Cytoskeleton-plasma membrane interactions. Science 258: 955–964

    Google Scholar 

  • Lynch TM, Lintilhac PM, Domozych D (1998) Mechanotransduction molecules in the plant gravisensory response: amyloplast/statolith membranes contain a β1 integrin-like protein. Protoplasma 201: 92–100

    Google Scholar 

  • Marrs JA, Andersson-Fisone C, Jeong MC, Cohen-Gould L, Zurzolo C, Nabi IR, Rodriguez-Boulan E, Nelson WJ (1995) Plasticity in epithelial cell phenotype: modulation by expression of different cadherin cell adhesion molecules. J Cell Biol 129: 507–519

    Google Scholar 

  • Masuda Y, Takagi S, Nagai R (1991) Protease-sensitive anchoring of microfilament bundles provides tracks for cytoplasmic streaming inVallisneria. Protoplasma 162: 151–159

    Google Scholar 

  • Menzel D (1994) Dynamics and pharmacological perturbations of the endoplasmic reticulum in the unicellular green algaAcetabularia. Eur J Cell Biol 64: 113–119

    Google Scholar 

  • Miller DD, de Ruijter NCA, Emons AMC (1997) From signal to form: aspects of the cytoskeleton-plasma membrane-cell wall continuum in root hair tips. J Exp Bot 48: 1881–1896

    Google Scholar 

  • Napier RM, Trueman S, Henderson J, Boyce JM, Hawes C, Fricker MD, Venis MA (1995) Purification, sequencing and functions of calreticulin from maize. J Exp Bot 46: 1603–1613

    Google Scholar 

  • Oparka KJ, Prior DAM, Crawford JW (1994) Behaviour of plasma membrane, cortical ER and plasmodesmata during plasmolysis of onion epidermal cells. Plant Cell Environ 17: 163–171

    Google Scholar 

  • Parthasarathy MV, Purdue TD, Witzum A, Alvernaz JA (1988) Actin network as a normal component of the cytoskeleton in many vascular plant cells. Am J Bot 72: 1318–1323

    Google Scholar 

  • Pesacreta TC, Parthasarathy MV (1984) Microfilament bundles in the roots of a conifer,Chamaecyparis obtusa. Protoplasma 121: 54–64

    Google Scholar 

  • Quader H (1990) Formation and disintegration of cisternae of the endoplasmic reticulum visualized in live cells by conventional fluorescence and confocal laser scanning microscopy: evidence for the involvement of calcium and cytoskeleton. Protoplasma 155: 166–175

    Google Scholar 

  • —, Hofmann A, Schnepf E (1987) Shape and movement of the endoplasmic reticulum in onion bulb epidermis cells: possible involvement of actin. Protoplasma 144: 17–26

    Google Scholar 

  • Reichelt S (1996) Characterization and localization of the unconventional myosin VIII in plant cells. PhD thesis, University of Bonn, Bonn, Federal Republic of Germany

    Google Scholar 

  • Reuzeau C, Pont-Lezica RF (1995) Comparing plant and animal extracellular matrix-cytoskeleton connections — are they alike? Protoplasma 186: 113–121

    Google Scholar 

  • —, Doolittle KW, McNally JG, Pickard BG (1997) Covisualization in living onion cells of putative integrin, putative spectrin, actin, putative intermediate filaments, and other proteins at the cell membrane and in endomembrane sheath. Protoplasma 199: 173–197

    Google Scholar 

  • Ryu J-H, Takagi S, Nagai R (1995) Stationary organization of the actin cytoskeleton inVallisneria: the role of stable microfilaments at the end walls. J Cell Sci 108: 1531–1539

    Google Scholar 

  • —, Mizuno K, Takagi S, Nagai R (1997) Extracellular components implicated in the stationary organization of the actin cytoskeleton in mesophyll cells ofVallisneria. Plant Cell Physiol 38: 420–432

    Google Scholar 

  • Šamaj J, Baluška F, Volkmann D (1998) Cell-specific expression of two arabinogalactan-protein epitopes recognized by monoclonal antibodies JIM8 and JIM13 in maize roots. Protoplasma 204: 1–12

    Google Scholar 

  • Sanders LC, Wang C-S, Walling LL, Lord EM (1991) A homolog of the substrate adhesion molecule vitronectin occurs in four species of flowering plants. Plant Cell 3: 629–635

    Google Scholar 

  • Staehelin LA (1997) The plant ER: a dynamic organelle composed of a large number of discrete functional domains. Plant J 11: 1151–1165

    Google Scholar 

  • Takeichi M (1991) Cadherin cell adhesion receptors as a morphogenetic regulator. Science 251: 1451–1455

    Google Scholar 

  • — (1995) Morphogenetic roles of classic cadherins. Curr Opin Cell Biol 7: 619–627

    Google Scholar 

  • Thimann KV, Reese K, Nachmias VT (1992) Actin and the elongation of plant cells. Protoplasma 171: 153–166

    Google Scholar 

  • Thorsch J, Esau K (1981) Changes in the endoplasmic reticulum during differentiation of a sieve element inGossypium hirsutum. J Ultrastruct Res 74: 183–194

    Google Scholar 

  • Venverloo CJ, Libbenga KR (1987) Regulation of the plane of cell division in vacuolated cells: the function of nuclear positioning and phragmoplast formation. J Plant Physiol 131: 267–284

    Google Scholar 

  • Wagner VT, Brian L, Quatrano RS (1992) Role of vitronectin-like molecule in embryo adhesion of the brown algaFucus. Proc Natl Acad Sci USA 89: 3644–3648

    Google Scholar 

  • Wang C-S, Walling LL, Gu YQ, Ware CF, Lord EM (1994) Two classes of proteins and mRNAs inLilium longiflorum L. identified by human vitronectin probes. Plant Physiol 104: 711–717

    Google Scholar 

  • Weaver VM, Roskelley CD (1997) Extracellular matrix: the central regulator of cell and tissue homeostasis. Trends Cell Biol 7: 40–42

    Google Scholar 

  • Wyatt SE, Carpita NC (1993) The plant cytoskeleton-cell wall continuum. Trends Cell Biol 3: 413–417

    Google Scholar 

  • Yamaguchi Y, Nagai R (1981) Motile apparatus in hallisneria leaf cells: organization of microfilaments. J Cell Sci 48: 193–205

    Google Scholar 

  • Zhu J-K, Shi J, Singh U, Wyatt SE, Bressan RA, Hasezawa PM, Carpita NC (1993) Enrichment of vitronectin- and fibronectinlike proteins in NaCl-adapted plant cells and evidence for their involvement in plasma membrane-cell wall adhesion. Plant J 3: 637–646

    Google Scholar 

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Baluška, F., Šamaj, J. & Volkmann, D. Proteins reacting with cadherin and catenin antibodies are present in maize showing tissue-, domain-, and development-specific associations with endoplasmic-reticulum membranes and actin microfilaments in root cells. Protoplasma 206, 174–187 (1999). https://doi.org/10.1007/BF01279265

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  • DOI: https://doi.org/10.1007/BF01279265

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