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. 1991 Feb 2;112(4):589–602. doi: 10.1083/jcb.112.4.589

Spatial organization of the assembly pathways of glycoproteins and complex polysaccharides in the Golgi apparatus of plants

PMCID: PMC2288847  PMID: 1993733

Abstract

The Golgi apparatus of plant cells is the site of assembly of glycoproteins, proteoglycans, and complex polysaccharides, but little is known about how the different assembly pathways are organized within the Golgi stacks. To study these questions we have employed immunocytochemical techniques and antibodies raised against the hydroxyproline-rich cell wall glycoprotein, extensin, and two types of complex polysaccharides, an acidic pectic polysaccharide known as rhamnogalacturonan I (RG-I), and the neutral hemicellulose, xyloglucan (XG). Our micrographs demonstrate that individual Golgi stacks can process simultaneously glycoproteins and complex polysaccharides. O- linked arabinosylation of the hydroxyproline residues of extensin occurs in cis-cisternae, and glycosylated molecules pass through all cisternae before they are packaged into secretory vesicles in the monensin-sensitive, trans-Golgi network. In contrast, in root tip cortical parenchyma cells, the anti-RG-I and the anti-XG antibodies are shown to bind to complementary subsets of Golgi cisternae, and several lines of indirect evidence suggest that these complex polysaccharides may also exit from different cisternae. Thus, RG-I type polysaccharides appear to be synthesized in cis- and medial cisternae, and have the potential to leave from a monensin-insensitive, medial cisternal compartment. The labeling pattern for XG suggests that it is assembled in trans-Golgi cisternae and departs from the monensin-sensitive trans- Golgi network. This physical separation of the synthesis/secretion pathways of major categories of complex polysaccharides may prevent the synthesis of mixed polysaccharides, and provides a means for producing secretory vesicles that can be targeted to different cell wall domains.

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Selected References

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  1. Anderson R. G., Pathak R. K. Vesicles and cisternae in the trans Golgi apparatus of human fibroblasts are acidic compartments. Cell. 1985 Mar;40(3):635–643. doi: 10.1016/0092-8674(85)90212-0. [DOI] [PubMed] [Google Scholar]
  2. Bowles D. J., Marcus S. E., Pappin D. J., Findlay J. B., Eliopoulos E., Maycox P. R., Burgess J. Posttranslational processing of concanavalin A precursors in jackbean cotyledons. J Cell Biol. 1986 Apr;102(4):1284–1297. doi: 10.1083/jcb.102.4.1284. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Burgess T. L., Kelly R. B. Constitutive and regulated secretion of proteins. Annu Rev Cell Biol. 1987;3:243–293. doi: 10.1146/annurev.cb.03.110187.001331. [DOI] [PubMed] [Google Scholar]
  4. Camirand A., Brummell D., Maclachlan G. Fucosylation of xyloglucan: localization of the transferase in dictyosomes of pea stem cells. Plant Physiol. 1987 Jul;84(3):753–756. doi: 10.1104/pp.84.3.753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Camirand A., Maclachlan G. Biosynthesis of the fucose-containing xyloglucan nonasaccharide by pea microsomal membranes. Plant Physiol. 1986 Oct;82(2):379–383. doi: 10.1104/pp.82.2.379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Denecke J., Botterman J., Deblaere R. Protein secretion in plant cells can occur via a default pathway. Plant Cell. 1990 Jan;2(1):51–59. doi: 10.1105/tpc.2.1.51. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dunphy W. G., Rothman J. E. Compartmental organization of the Golgi stack. Cell. 1985 Aug;42(1):13–21. doi: 10.1016/s0092-8674(85)80097-0. [DOI] [PubMed] [Google Scholar]
  8. Farquhar M. G. Progress in unraveling pathways of Golgi traffic. Annu Rev Cell Biol. 1985;1:447–488. doi: 10.1146/annurev.cb.01.110185.002311. [DOI] [PubMed] [Google Scholar]
  9. Green M. Incorporation of amino acid analogs interferes with the processing of the asparagine-linked oligosaccharide of the MOPC-46B kappa light chain. J Biol Chem. 1982 Aug 10;257(15):9039–9042. [PubMed] [Google Scholar]
  10. Griffiths G., Simons K. The trans Golgi network: sorting at the exit site of the Golgi complex. Science. 1986 Oct 24;234(4775):438–443. doi: 10.1126/science.2945253. [DOI] [PubMed] [Google Scholar]
  11. Harley S. M., Beevers L. Coated Vesicles Are Involved in the Transport of Storage Proteins during Seed Development in Pisum sativum L. Plant Physiol. 1989 Oct;91(2):674–678. doi: 10.1104/pp.91.2.674. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hayashi T., Maclachlan G. Pea xyloglucan and cellulose : I. Macromolecular organization. Plant Physiol. 1984 Jul;75(3):596–604. doi: 10.1104/pp.75.3.596. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hayashi T., Matsuda K. Biosynthesis of xyloglucan in suspension-cultured soybean cells. Occurrence and some properties of xyloglucan 4-beta-D-glucosyltransferase and 6-alpha-D-xylosyltransferase. J Biol Chem. 1981 Nov 10;256(21):11117–11122. [PubMed] [Google Scholar]
  14. Hirschberg C. B., Snider M. D. Topography of glycosylation in the rough endoplasmic reticulum and Golgi apparatus. Annu Rev Biochem. 1987;56:63–87. doi: 10.1146/annurev.bi.56.070187.000431. [DOI] [PubMed] [Google Scholar]
  15. Hunt L. A., Davidson S. K., Golemboski D. B. Unusual heterogeneity in the glycosylation of the G protein of the hazelhurst strain of vesicular stomatitis virus. Arch Biochem Biophys. 1983 Oct 1;226(1):347–356. doi: 10.1016/0003-9861(83)90301-6. [DOI] [PubMed] [Google Scholar]
  16. Huttner W. B., Tooze S. A. Biosynthetic protein transport in the secretory pathway. Curr Opin Cell Biol. 1989 Aug;1(4):648–654. doi: 10.1016/0955-0674(89)90029-x. [DOI] [PubMed] [Google Scholar]
  17. Kornfeld R., Kornfeld S. Assembly of asparagine-linked oligosaccharides. Annu Rev Biochem. 1985;54:631–664. doi: 10.1146/annurev.bi.54.070185.003215. [DOI] [PubMed] [Google Scholar]
  18. McNeil M., Darvill A. G., Fry S. C., Albersheim P. Structure and function of the primary cell walls of plants. Annu Rev Biochem. 1984;53:625–663. doi: 10.1146/annurev.bi.53.070184.003205. [DOI] [PubMed] [Google Scholar]
  19. Moore P. J., Darvill A. G., Albersheim P., Staehelin L. A. Immunogold localization of xyloglucan and rhamnogalacturonan I in the cell walls of suspension-cultured sycamore cells. Plant Physiol. 1986 Nov;82(3):787–794. doi: 10.1104/pp.82.3.787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Morré D. J., Boss W. F., Grimes H., Mollenhauer H. H. Kinetics of Golgi apparatus membrane flux following monensin treatment of embryogenic carrot cells. Eur J Cell Biol. 1983 Mar;30(1):25–32. [PubMed] [Google Scholar]
  21. Orci L., Halban P., Amherdt M., Ravazzola M., Vassalli J. D., Perrelet A. A clathrin-coated, Golgi-related compartment of the insulin secreting cell accumulates proinsulin in the presence of monensin. Cell. 1984 Nov;39(1):39–47. doi: 10.1016/0092-8674(84)90189-2. [DOI] [PubMed] [Google Scholar]
  22. Pfeffer S. R., Rothman J. E. Biosynthetic protein transport and sorting by the endoplasmic reticulum and Golgi. Annu Rev Biochem. 1987;56:829–852. doi: 10.1146/annurev.bi.56.070187.004145. [DOI] [PubMed] [Google Scholar]
  23. Prehm P. Hyaluronate is synthesized at plasma membranes. Biochem J. 1984 Jun 1;220(2):597–600. doi: 10.1042/bj2200597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Pressman B. C., Fahim M. Pharmacology and toxicology of the monovalent carboxylic ionophores. Annu Rev Pharmacol Toxicol. 1982;22:465–490. doi: 10.1146/annurev.pa.22.040182.002341. [DOI] [PubMed] [Google Scholar]
  25. REYNOLDS E. S. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol. 1963 Apr;17:208–212. doi: 10.1083/jcb.17.1.208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Rambourg A., Clermont Y. Three-dimensional electron microscopy: structure of the Golgi apparatus. Eur J Cell Biol. 1990 Apr;51(2):189–200. [PubMed] [Google Scholar]
  27. Roth J. 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. 1984 Feb;98(2):399–406. doi: 10.1083/jcb.98.2.399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rothman J. E., Orci L. Movement of proteins through the Golgi stack: a molecular dissection of vesicular transport. FASEB J. 1990 Mar;4(5):1460–1468. doi: 10.1096/fasebj.4.5.2407590. [DOI] [PubMed] [Google Scholar]
  29. Ryan C. A. Oligosaccharide signalling in plants. Annu Rev Cell Biol. 1987;3:295–317. doi: 10.1146/annurev.cb.03.110187.001455. [DOI] [PubMed] [Google Scholar]
  30. Sadava D., Walker F., Chrispeels M. J. Hydroxyproline-rich wall protein (extensin): biosynthesis and accumulation in growing pea epicotyls. Dev Biol. 1973 Jan;30(1):41–48. [PubMed] [Google Scholar]
  31. Slot J. W., Geuze H. J. A new method of preparing gold probes for multiple-labeling cytochemistry. Eur J Cell Biol. 1985 Jul;38(1):87–93. [PubMed] [Google Scholar]
  32. Staehelin L. A., Giddings T. H., Jr, Kiss J. Z., Sack F. D. Macromolecular differentiation of Golgi stacks in root tips of Arabidopsis and Nicotiana seedlings as visualized in high pressure frozen and freeze-substituted samples. Protoplasma. 1990;157(1-3):75–91. doi: 10.1007/BF01322640. [DOI] [PubMed] [Google Scholar]
  33. Sturm A., Johnson K. D., Szumilo T., Elbein A. D., Chrispeels M. J. Subcellular localization of glycosidases and glycosyltransferases involved in the processing of N-linked oligosaccharides. Plant Physiol. 1987 Nov;85(3):741–745. doi: 10.1104/pp.85.3.741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Tartakoff A. M. Perturbation of vesicular traffic with the carboxylic ionophore monensin. Cell. 1983 Apr;32(4):1026–1028. doi: 10.1016/0092-8674(83)90286-6. [DOI] [PubMed] [Google Scholar]
  35. Tartakoff A. M. The Golgi complex: crossroads for vesicular traffic. Int Rev Exp Pathol. 1980;22:227–251. [PubMed] [Google Scholar]
  36. Titus D. E., Becker W. M. Investigation of the glyoxysome-peroxisome transition in germinating cucumber cotyledons using double-label immunoelectron microscopy. J Cell Biol. 1985 Oct;101(4):1288–1299. doi: 10.1083/jcb.101.4.1288. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Tooze S. A., Tooze J., Warren G. Site of addition of N-acetyl-galactosamine to the E1 glycoprotein of mouse hepatitis virus-A59. J Cell Biol. 1988 May;106(5):1475–1487. doi: 10.1083/jcb.106.5.1475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Williams D. B., Lennarz W. J. Control of asparagine-linked oligosaccharide chain processing: studies on bovine pancreatic ribonuclease B. An in vitro system for the processing of exogenous glycoproteins. J Biol Chem. 1984 Apr 25;259(8):5105–5114. [PubMed] [Google Scholar]

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