Summary
Arabinogalactan proteins (AGPs) are proteoglycans detected in high amounts at plant cell surfaces; however, details of their subcellular localization are largely unknown. Immunolocalization studies with the anti-AGP monoclonal antibody LM2 have indicated that this AGP epitope is associated with secretory compartments such as endoplasmic reticulum and Golgi apparatus within plant cells actively producing and secreting AGPs. The LM2 epitope contains a β-linked glucuronic acid residue and occurs in the polysaccharide moiety of AGPs. We have localized this AGP epitope also to the tonoplast and to cytoplasmic strands. Endomembrane association of AGPs was confirmed with two other monoclonal antibodies, JIM13 and MAC207, both reacting with carbohydrate AGP epitopes containing GlcpA-β(1→3)-D-GalpA-α(1→2)-L-Rha residues. Immunocytochemistry is supported by biochemical analysis which shows that LM2 reacts with the microsomal fraction and also with low-molecular-weight material of the detergent phase after Triton X-114 phase separation prepared from maize roots. Our results indicate that some AGP epitopes are closely associated with endomembranes.
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Abbreviations
- AGP:
-
arabinogalactan protein
- ER:
-
endoplasmic reticulum
- GlcA:
-
glucuronic acid
References
Andreae M, Lang WC, Barg C, Robinson DG (1988) Hydroxypro-line-arabinosylation in the endoplasmic reticulum of maize roots. Plant Sci 56: 205–212
Balestrini R, Hahn MG, Mendgen K, Faccio A, Bonfante P (1996) Differential localization of carbohydrate epitopes in plant cell walls in the presence and absence of arbuscular mycorrhizal fungi. Plant Physiol 111: 203–213
Baluška F, Parker JS, Barlow PW (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
—, Vitha S, Barlow PW, Volkmann D (1997a) 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
—, Šamaj J, Volkmann D, Barlow PW (1997b) Impact of taxol-mediated stabilization of microtubules on nuclear morphology, ploidy levels and cell growth in maize roots. Biol Cell 89: 221–231
Bordier AL (1981) Phase separation of integral membrane proteins in Triton-X-114 solution. J Biol Chem 256: 1604–1607
Brewin NJ (1996) Plant membrane structure and function in theRhizobium-legume symbiosis. In: Smallwood M, Knox JP, Bowles DJ (eds) Membranes: specialized functions in plants. Bios Scientific Publishers, Oxford, pp 507–524
Brown DA, Rose JK (1992) Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68: 533–544
Butowt R, Niklas A, Rodrigues-Garcia MI, Majewska-Sawka A (1999) Involvement of JIM13 and JIM8 responsive carbohydrate epitopes in early stages of cell wall formation. J Plant Res 112: 107–116
Carter HE, Strobach DR, Hawthorne JN (1969) Biochemistry of the sphingolipids XVIII: complete structure of tetrasaccharide phytoglycolipid. Biochemistry 8: 383–388
Chen CG, Pu ZY, Moritz RL, Simpson RJ, Bacic A, Clarke AE, Mau SL (1994) Molecular cloning of a gene encoding an arabino-galactan-protein from pear (Pyrus communis) cell suspension culture. Proc Natl Acad Sci USA 91: 10305–10309
Day DA, Copeland L (1991) Carbon metabolism and compartmentation in nitrogen-fixing legume nodules. Plant Physiol Biochem 29: 185–201
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
Ferguson C, Bacic A, Anderson MA, Read SM (1999) Subcellular distribution of arabinogalactan proteins in pollen grains and tubes as revealed with a monoclonal antibody raised against stylar arabinogalactan proteins. Protoplasma 206: 105–117
Gibeaut DM, Carpita NC (1991) Tracing cell wall biogenesis in intact cells and plants. Selective turnover and alteration of soluble and cell wall polysaccharides in grasses. Plant Physiol 97: 551–561
Herman EM, Lamb CJ (1992) Arabinogalactan-rich glycoproteins are localized on the cell surface and in intravacuolar multivesicular bodies. Plant Physiol 98: 264–272
Hsieh TCY, Kaul K, Laine RA, Lester RL (1978) Structure of a major glycophosphoceramide from tobacco leaves. PSL-I: 2-deoxy-2-acetamido-D-glucopyranosyl(α1→4)-D-glucuronopyra-nosyl(α1→2)myoinositol-1-O-phosphoceramide. Biochemistry 17: 3575–3581
Jauh GY, Lord EM (1996) Localization of pectins and arabinogalactan-proteins in lily (Lilium longiflorum L.) pollen tube and style, and their possible roles in pollination. Planta 199: 251–261
Kaul K, Lester RL (1978) Isolation of six novel phosphoinositolcontaining sphingolipids from tobacco leaves. Biochemistry 17: 3569–3575
Kawasaki S (1981) Synthesis of arabinose-containing cell wall precursors in suspension-cultured tobacco cells I: intracellular site of synthesis and transport. Plant Cell Physiol 22: 431–442
— (1987) Synthesis of arabinose-containing cell wall precursors in suspension-cultured tobacco cells IV: differential subfractionation and comparison of the acidic precursors. Plant Cell Physiol 28: 925–935
Kikuchi S, Ohinata A, Tsumuraya Y, Hashimoto Y, Kaneko Y, Matsushima H (1993) Production and characterization of antibodies to the β-(l→6)-galactotetraosyl group and their interaction with arabinogalactan-proteins. Planta 190: 525–535
Kjellbom P, Snogerup L, Stöhr C, Reuzeau C, McCabe PF, Pennell RI (1997) Oxidative cross-linking of plasma membrane arabinogalactan proteins. Plant J 12: 1189–1196
Knox JP (1993) The role of cell surface glycoproteins in differentiation and morphogenesis. In: Battey NH, Dickinson HG, Hetherington AM (eds) Post-translational modifications in plants. Cambridge University Press, Cambridge, pp 267–283
— (1995) Developmental regulated proteoglycans and glycoproteins of the plant cell surface. FASEB J 9: 1004–1012
— (1996) Arabinogalactan-proteins: developmentally regulated proteoglycans of the plant cell surface. In: Smallwood M, Knox JP, Bowles DJ (eds) Membranes: specialized functions in plants. Bios Scientific Publisher, Oxford, pp 93–102
— (1997) The use of antibodies to study the architecture and developmental regulation of plant cell walls. Int Rev Cytol 171: 79–120
—, Linstead PJ, Peart J, Cooper C, Roberts K (1991) Developmentaly regulated epitopes of cell surface arabinogalactan proteins and their relation to root tissue pattern formation. Plant J 1: 317–326
Kreuger M, van Holst G-J (1996) Arabinogalactan proteins and plant differentiation. Plant Mol Biol 30: 1077–1086
Li YQ, Faleri C, Geitmann A, Zhang H-Q, Cresti M (1995) Immunogold localization of arabinogalactan proteins, unesterified and esterified pectins in pollen grains and pollen tubes ofNicotiana tabacum L. Protoplasma 189: 26–36
Lichtscheidl IK, 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
Mau SL, Chen CG, Pu ZY, Moritz RL, Simpson RJ, Bacic A, Clarke AE (1995) Molecular cloning of cDNAs encoding the protein backbones of arabinogalactan-proteins from the filtrate of suspension-cultured cells ofPyrus communis andNicotiana alata. Plant J 8: 269–281
McCabe PF, Valentine TA, Forsberg S, Pennell RI (1997) Soluble signals from cells identified at the cell wall establish a developmental pathway in carrot. Plant Cell 9: 2225–2241
Misawa H, Tsumuraya Y, Kaneko Y, Hashimoto Y (1996) alpha-L-Fucosyltransferases from radish primary roots. Plant Physiol 110: 665–673
Moore PJ, Swords KMM, Lynch MA, Staehelin A (1991) Spatial organization of the assembly pathways of glycoproteins and complex polysaccharides in the Golgi apparatus of plants. J Cell Biol 112: 589–602
Norman PM, Wingate VPM, Fitter MS, Lamb CJ (1986) Monoclonal antibodies to plant plasma-membrane antigens. Planta 167: 452–459
Nothnagel EA (1997) Proteoglycans and related components in plant cells. Int Rev Cytol 174: 195–291
Pennell RI, Knox JP, Scofield GN, Selvendran RR, Roberts K (1989) A family of abundant plasma membrane-associated glycoproteins related to the arabinogalactan proteins is unique to flowering plants. J Cell Biol 108: 1967–1977
—, Janniche L, Kjellbom P, Scofield GN, Peart JM, Roberts K (1991) Developmental regulation of a plasma membrane arabinogalactan protein epitope in oilseed rape flowers. Plant Cell 3: 1317–1326
— —, Scofield GN, Booij H, de Vries SC, Roberts K (1992) Identification of a transitional cell state in the developmental pathway to carrot somatic embryogenesis. J Cell Biol 119: 1371–1380
Rodgers MW, Bolwell GP (1992) Partial purification of Golgibound arabinosyltransferase and two isoforms of xylosyltransferase from French beanPhaseolus ulgaris L. Biochem J 288: 817–822
Roth J (1984) Cytochemical localization of terminal N-acetyl-D-galactosamine residues in cellular compartments of intestinal goblet cells: implications for the topology of O-glycosylation. J Cell Biol 98: 399–406
Šamaj J, Baluška F, Volkmann D (1998) Cell-specific expression of two arabinogalactan-protein epitopes by monoclonal antibodies JIM8 and JIM13 in maize roots. Protoplasma 204: 1–12
— —, Bobák M, Volkmann D (1999a) Extracellular matrix surface network of embryogenie units of friable maize callus contains arabinogalactan-proteins recognized by monoclonal antibody JIM4. Plant Cell Rep 18: 369–374
—, Ensikat HJ, Baluska F, Knox JP, Barthlott W, Volkmann D (1999b) Immunogold localization of plant surface arabinogalactan-proteins using glycerol liquid substitution and scanning electron microscopy. J Microsc 193: 150–157
—, Braun M, Baluška F, Ensikat HJ, Tsumuraya Y, Volkmann D (1999c) Specific localization of arabinogalactan-protein epitopes at surface of maize root hairs. Plant Cell Physiol 40: 874–883
Schibeci A, Pnjak A, Fincher GB (1984) Biosynthesis of arabinogalactan-protein inLolium multiflorum (Italian ryegrass) endosperm cells, subcellular distribution of galactosyltransferases. Biochem J 218: 633–636
Schindler T, Bergfeld R, Schopfer P (1995) Arabinogalactan proteins in maize coleoptiles: developmental relationship to cell death during xylem differentiation but not to extension growth. Plant J 7: 25–36
Schopfer P (1990) Cytochemical identification of arabinogalactan protein in the outer epidermal wall of maize coleoptiles. Planta 183: 139–142
Schultz C, Gilson P, Oxley D, Youl J, Bacic A (1998) GPI-anchors on arabinogalactan proteins: implications for signalling in plants. Trends Plant Sci 3: 426–431
Sedgley M, Clarke AE (1986) Immuno-gold localisation of arabinogalactan protein in the developing style ofNicotiana alata. Nord J Bot 6: 591–598
Smallwood M, Yates EA, Willats WGT, Martin H, Knox JP (1996) Immunochemical comparison of membrane-associated and secreted arabinogalactan-proteins in rice and carrot. Planta 198: 452–459
Tooze SA, Tooze J, Warren G (1988) Site of addition of N-acetyl-galactosamine to the E1 glycoprotein of mouse hepatitis virus A59. J Cell Biol 106: 1475–1487
Verma DPS, Cheon CI, Hong Z (1994) Small GTP-binding proteins and membrane biogenesis in plants. Plant Physiol 106: 1–6
Vicré M, Jauneau A, Knox JP, Driouch A (1998) Immunolocaliza-tion of β-(1→4) and β-(1→6)-D-galactan epitopes in the cell wall and Golgi stacks of developing flax root tissues. Protoplasma 203: 26–34
Winicur ZM, Zhang GF, Staehelin A (1998) Auxin deprivation induces synchronous Golgi differentiation in suspension-cultured tobacco BY-2 cells. Plant Physiol 117: 501–513
Yariv J, Lis H, Katchalski E (1967) Precipitation of arabic acid and some seed polysaccharides by glycosylphenylazo dyes. Biochem J 105: 1C-2C
Yates EA, Valdor JF, Haslam SM, Morris HR, Dell A, Mackie W, Knox JP (1996) Characterization of carbohydrate structural features recognized by anti-arabinogalactan-protein monoclonal antibodies. Glycobiology 6: 131–139
Youl JJ, Bacic A, Oxley D (1998) Arabinogalactan-proteins fromNicotiana alata andPyrus communis contain glycosylphos-phatidylinositol membrane anchors. Proc Natl Acad Sci USA 95: 7921–7926
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Dedicated to Professor Walter Gustav Url on the occasion of his 70th birthday
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Šamaj, J., Šamajová, O., Peters, M. et al. Immunolocalization of LM2 arabinogalactan protein epitope associated with endomembranes of plant cells. Protoplasma 212, 186–196 (2000). https://doi.org/10.1007/BF01282919
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DOI: https://doi.org/10.1007/BF01282919