Skip to main content
SpringerLink
Log in

Structure, differentiation, and multiplication of Golgi apparatus in fungal hyphae

  • Published:
Protoplasma Aims and scope Submit manuscript

Summary

Golgi apparatus in subapical regions of hyphae consist of paranuclear dictyosomes with 4–5 cisternae each. Transverse and tangential sections provide ultrastructural evidence for a three-dimensional architectural model of the Golgi apparatus and a stepwise mechanism for dictyosome multiplication. The dictyosomes are polarized, with progressive morphological and developmental differentiation of cisternae from the cis to the trans pole. Small membrane blebs and transition vesicles provide developmental continuity between the nuclear envelope and the adjacent dictyosome cisterna at the cis face. Cisternae are formed as fenestrated plates with extended tubular peripheries. The morphology of each cisterna depends on its position in the stack, consistent with a developmental gradient of progressive maturation and turnover of cisternae. Mature cisternae at the trans face are dissociated to produce spheroid and tubular vesicles. Evidence in support of a schematic sequence for increasing the numbers of dictyosomes comes from images of distinctive and unusual forms of Golgi apparatus in hyphal regions where nuclei and dictyosomes multiply, as follows: (a) The area of the nuclear envelope exhibiting “forming-face” activity next to a dictyosome expands, which in turn increases the size of cisternae subsequently assembled at the cis face of the dictyosome. (b) As subsequent large cisternae are formed and mature as they pass through the dictyosome, an entire dictyosome about twice normal size is built up. The number of cisternae per stack remains the same because of continuing turnover and loss of cisternae at the trans face, (c) This enlarged dictyosome becomes separated into two by a small region of the nuclear envelope next to the cis face that acquires polyribosomes and no longer generates transition vesicles, (d) As a consequence, assembly of new dictyosomes is physically separated into two adjacent regions, (e) As.the enlarged cisternae are lost to vesiculation at the trans pole, they are replaced by two separate stacks of cisternae with typical “normal” diameters, (f) The net result is two adjacent dictyosomes where one existed previously. Dictyosome multiplication is thus accomplished as part of the normal developmental turnover of cisternae, without interrupting the functioning of the Golgi apparatus as it continues to produce new secretory vesicles from mature cisternae at the trans face. Coordination of Golgi apparatus multiplication with nuclear division ensures that each daughter nucleus receives a complement of paranuclear dictyosomes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Alcade J, Binoy P, Roa A, Vilaro S, Sandoval IV (1992) Assembly and disassembly of the Golgi complex: two processes arranged in a cis-trans direction. J Cell Biol 116: 69–83

    PubMed  Google Scholar 

  • Beams HW, Kessel RG (1968) The Golgi apparatus: structure and function. Int Rev Cytol 23: 209–276

    PubMed  Google Scholar 

  • Bracker CE, Grove SN (1971) Continuity between cytoplasmic endomembranes and other mitochondrial membranes in fungi. Protoplasma 73: 15–34

    PubMed  Google Scholar 

  • - Heintz CE, Grove SN (1970) Structural and functional continuity among endomembrane organelles in fungi. In: Microscopie Electronique, 7ieme Congress International Microscopie Electronique Societe Francaise de Microscopie Electronique, Paris, pp 103–104

  • —, Grove SN, Heintz CE, Morré DJ (1971) Continuity between endomembrane components in hyphae ofPythium. Cytobiologie 4: 1–8

    Google Scholar 

  • Chida Y, Noguchi T (1989) Multiplication of the dictyosome during formation of autospores in the green algaChlorococcum infusionum. Biol Cell 65: 189–194

    PubMed  Google Scholar 

  • Croze EM, Morré DM, Morré DJ (1983) Three classes of spiny-(clathrin-) coated vesicles in rodent liver based on size distributions. Protoplasma 111: 45–52

    Google Scholar 

  • Cunningham WP, Morré DJ, Mollenhauer HH (1966) Structure of isolated plant Golgi apparatus revealed by negative staining. J Cell Biol 28: 169–179

    PubMed  Google Scholar 

  • Di Orio J, Millington WE (1978) Dictyosome formation during reproduction in colchicine-treatedPediastrum boryanum (Hydrodictyaceae). Protoplasma 97: 329–336

    Google Scholar 

  • Dowben RM (1971) Cell biology. Harper and Row, New York, p 359

    Google Scholar 

  • Dunphy WG, Rothman JE (1985) Compartmental organization of the Golgi stack. Cell 42: 13–21

    PubMed  Google Scholar 

  • Ehemann V, Schroeter D, Paweletz N (1982) Membrane pattern of the Golgi elements of PtK1 cells in mitosis. Eur J Cell Biol 27: 111 (Abstr)

    Google Scholar 

  • Ellinger A, Pavelka M (1982) The Golgi apparatus of rat small intestinal absorptive cells. II. J Submicrosc Cytol 14: 587–596

    PubMed  Google Scholar 

  • Hiller G, Weber K (1982) Golgi detection in mitotic and interphase cells by antibodies to secreted galactosyltransferase. Exp Cell Res 142: 85–94

    PubMed  Google Scholar 

  • Farquhar MG (1985) Progress in unraveling pathways of Golgi traffic. Annu Rev Cell Biol 1: 447–488

    PubMed  Google Scholar 

  • Flickinger CJ (1969) Fenestrated cisternae in the Golgi apparatus of the epididymus. Anat Rec 163: 39–54

    PubMed  Google Scholar 

  • Franke WW, Spring H, Kartenbeck J, Falk H (1977) Cyst formation in some dasycladacean green algae I. Vesicle formations during coenocytotomy inAcetabularia mediterranen. Cytobiologie 14: 229–252

    Google Scholar 

  • Friend DS (1965) The fine structure of Brunner's gland in the mouse. J Cell Biol 25: 563–576

    PubMed  Google Scholar 

  • Girbardt M (1969) Die Ultrastruktur der Apikalregion von Pilzhyphen. Protoplasma 67: 413–441

    Google Scholar 

  • Griffiths G, Simons K (1986) The trans Golgi network: sorting at the exit site of the Golgi complex. Science 234: 438–443

    PubMed  Google Scholar 

  • —, Fuller SD, Back R, Hollinshead M, Pfeiffer S, Simons K (1989) The dynamic nature of the Golgi complex. J Cell Biol 108: 277–297

    PubMed  Google Scholar 

  • Grove SN, Bracker CE (1970) Protoplasmic organization of hyphal tips among fungi: vesicles and Spitzenkörper. J Bacteriol 104: 989–1009

    PubMed  Google Scholar 

  • — — (1978) Protoplasmic changes during zoospore encystment and cyst germination inPythium aphamdermatum. Exp Mycol 2: 51–98

    Google Scholar 

  • — —, Morré DJ (1968) Cytomembrane differentiation in the endoplasmic reticulum-Golgi apparatus-vesicle complex. Science 161: 171–173

    PubMed  Google Scholar 

  • — — — (1970) An ultrastructural basis for hyphal tip growth inPythium ultimum. Am J Bot 57: 245–266

    Google Scholar 

  • Heath IB (1980) Variant mitoses in lower eukaryotes: indicators of the evolution of mitosis. Int Rev Cytol 64: 1–80

    Google Scholar 

  • Howard RJ (1981) Ultrastructural analysis of hyphal tip cell growth in fungi: Spitzenkörper, cytoskeleton and endomembranes after freeze substitution. J Cell Sci 48: 89–103

    PubMed  Google Scholar 

  • Kiermayer O (1970) Elektronenmikroskopische Untersuchungen zum Problem der Cytomorphogenese vonMicrasterias denticulata Breb. I. Allgemeiner Überblick. Protoplasma 69: 97–132

    Google Scholar 

  • Krijnse-Locker J, Ericsson M, Rottier PJM, Griffiths G (1994) Characterization of the budding compartment of mouse hepatitis virus: evidence that transport from the RER to the Golgi complex requires only one vesicular transport step. J Cell Biol 124: 55–70

    PubMed  Google Scholar 

  • Maul GG, Brinkley BR (1970) The Golgi apparatus during mitosis in human melanoma cells in vitro. Cancer Res 30: 2326–2335

    PubMed  Google Scholar 

  • Mellman I, Simons K (1992) The Golgi complex:in vitro veritas? Cell 68: 829–840

    PubMed  Google Scholar 

  • Mollenhauer HH (1965) An intercisternal structure in the Golgi apparatus. J Cell Biol 24: 504–511

    Google Scholar 

  • — (1971) Fragmentation of mature dictyosome cisternae. J Cell Biol 49: 212–214

    PubMed  Google Scholar 

  • —, Morré DJ (1966a) Golgi apparatus and plant secretion. Annu Rev Plant Physiol 17: 27–46

    Google Scholar 

  • — — (1966b) Tubular connections between dictyosomes and forming secretory vesicles in plant Golgi apparatus. J Cell Biol 29: 373–376

    PubMed  Google Scholar 

  • — — (1978a) Structural differences contrast plant and animal Golgi apparatus. J Cell Sci 32: 357–362

    PubMed  Google Scholar 

  • — — (1978b) Structural compartmentation of the cytosol: zones of exclusion, zones of adhesion, cytoskeletal and intercisternal elements. Subcell Biochem 5: 324–357

    Google Scholar 

  • — — (1994) Structure of Golgi apparatus. Protoplasma 180: 14–28

    Google Scholar 

  • — —, Bergmann L (1967) Homology of form in plant and animal Golgi apparatus. Anat Rec 158: 313–318

    PubMed  Google Scholar 

  • Morré DJ (1987) The Golgi apparatus. Int Rev Cytol Suppl 17: 211–253

    Google Scholar 

  • —, Mollenhauer HH (1974) The endomembrane concept: a functional integration of endoplasmic reticulum and Golgi apparatus. In: Robards AW (ed) Dynamic aspects of plant ultrastructure. McGraw-Hill, New York, pp 84–137

    Google Scholar 

  • —, Ovtracht L (1977) Dynamics of Golgi apparatus: membrane differentiation and membrane flow. Int Rev Cytol Suppl 5: 61–188

    PubMed  Google Scholar 

  • Morré DJ, Mollenhauer HH, Bracker CE (1971) The origin and continuity of Golgi apparatus. In: Reinert J, Ursprung H (eds) Results and problems in cell differentiation II: origin and continuity of cell organelles. Springer, Berlin Heidelberg New York, pp 82–126

    Google Scholar 

  • —, Kartenbeck J, Franke WW (1979) Membrane flow and interconversions among endomembranes. Biochim Biophys Acta 559: 71–152

    PubMed  Google Scholar 

  • Noguchi T (1978) Transformation of the Golgi apparatus in the cell cycle, especially at the resting and earliest developmental stages of a green alga,Micrasterias americana. Protoplasma 95: 73–88

    Google Scholar 

  • — (1988) Numerical and structural changes in dictyosomes during zygospore germination ofClosterium ehrenbergii. Protoplasma 147: 135–142

    Google Scholar 

  • Novikoff AB (1973) Lysosomes: a personal account. In: Hers HG, van Hoof F (eds) Lysosomes and storage diseases. Academic Press, New York, pp 1–41

    Google Scholar 

  • —, Essner E, Goldfischer S, Heus M (1962) Nucleosidediphosphatase activities of cytomembranes. In: Harris RJC (ed) The interpretation of ultrastructure. Academic Press, New York, pp 149–192

    Google Scholar 

  • Novikoff PM, Novikoff AB, Quintana N, Hauw J-J (1971) Golgi apparatus, GERL, and lysosomes of neurons in rat dorsal root ganglia studied by thick section and thin section cytochemistry. J Cell Biol 50: 859–886

    PubMed  Google Scholar 

  • Ovtracht L, Morré DJ, Cheetham RD, Mollenhauer HH (1973) Subfractionation of Golgi apparatus from rat liver: method and morphology. J Microsc 18: 87–102

    Google Scholar 

  • Paulik M, Nowack DD, Morré DJ (1988) Isolation of a vesicular intermediate in the cell-free transfer of membrane from transitional elements of the endoplasmic reticulum to Golgi apparatus cisternae of rat liver. J Biol Chem 263: 17738–17748

    PubMed  Google Scholar 

  • Pavelka M, Ellinger A (1983a) Effects of colchicine on the Golgi apparatus and on GERL of rat jejunal absorptive cells. Ultrastructural localization of thiamine pyrophosphatase and acid phosphatase activity. Eur J Cell Biol 29: 253–261

    PubMed  Google Scholar 

  • — — (1983b) The trans Golgi face in rat small intestinal cells. Eur J Cell Biol 29: 253–261

    PubMed  Google Scholar 

  • Pearse BMF (1976) Clathrin: a unique protein associated with intracellular transfer of membrane by coated vesicles. Proc Natl Acad Sci USA 73: 1255–1259

    PubMed  Google Scholar 

  • Pypaert M, Nilsson T, Berger EG, Weaver G (1993) Mitotic Golgi clusters are not tubular endosomes. J Cell Sci 104: 811–813

    PubMed  Google Scholar 

  • Rambourg A, Clermont Y, Marraud A (1974) Three-dimensional structure of the osmium-impregnated Golgi apparatus as seen in the high voltage electron microscope. Am J Anat 140: 27–46

    PubMed  Google Scholar 

  • — —, Hermo L (1979) Three-dimensional architecture of the Golgi apparatus in Sertoli cells of the rat. Am J Anat 154: 455–476

    PubMed  Google Scholar 

  • Roth J, Taatjes DJ, Lucocq JM, Weinstein J, Paulson JC (1985) Demonstration of an extensive trans tubular network continuous with Golgi apparatus stack that may function in glycosylation. Cell 43: 287–295

    PubMed  Google Scholar 

  • Rothman JE (1981) The Golgi apparatus: two organelles in tandem. Science 213: 1212–1219

    PubMed  Google Scholar 

  • — (1994) Mechanisms of intracellular protein transport. Nature 372: 55–63

    PubMed  Google Scholar 

  • —, Orci L (1990) Movement of proteins through the Golgi stack: a molecular dissection of vesicular transport. FASEB J 4: 1460–1468

    PubMed  Google Scholar 

  • Saraste J, Svensson K (1991) Distribution of the intermediate elements operating in ER to Golgi transport. J Cell Sci 100: 415–430

    PubMed  Google Scholar 

  • Schnepf E, Schmitt U (1981) Destruction and reconstitution of the dictyosome in the chrysophycean flagellate,Poterioochromonas malhamensis, after heat-shock, and other heat-shock effects. Protoplasma 106: 261–271

    Google Scholar 

  • Sesso A, de Faria FP, Iwamura ESM, Correa H (1994) A three-dimensional reconstruction study of the rough ER-GoIgi interface in serial thin sections of the pancreatic acinar cell of the rat. J Cell Sci 107: 517–528

    Google Scholar 

  • Tandler B, Morré DJ (1983) The Golgi apparatus of ciliated cells in the cat tracheae negatively-stained in situ and in cell fractions. Protoplasma 115: 193–201

    Google Scholar 

  • Ward RT, Ward E (1968) The multiplication of Golgi bodies in the oocytesoiRanapipiens. J Microsc 7: 1007–1020

    Google Scholar 

  • Werz G (1964) Elektronenmikroskopische Untersuchungen zur Genese des Golgi-Apparates (Dictyosomen) und ihrer Kernab-hängigkeit beiAcetabularia. Planta 63: 366–381

    Google Scholar 

  • Weston JC, Ackerman GA, Greider MH, Nikolewski RF (1972) Nuclear membrane contributions to the Golgi complex. Z Zellforsch Mikrosk Anat 123: 153–160

    PubMed  Google Scholar 

  • Whaley WG (1966) Proposals concerning replication of the Golgi apparatus. In: Sitte P (ed) Probleme der biologischen Reduplikation. Springer, Berlin Heidelberg New York, pp 340–371

    Google Scholar 

  • — (1975) The Golgi apparatus. Springer, Wien New York [Alfert M et al (eds) Cell biology monographs, vol 2]

    Google Scholar 

  • Weidman P, Roth R, Heuser J (1993) Golgi membrane dynamics imaged by freeze-etch electron microscopy: views of different membrane coatings involved in tubulation vs vesiculation. Cell 75: 123–133

    PubMed  Google Scholar 

  • Zhang GF, Driouich A, Staehelin LA (1993) Effect of monensin on plant Golgi: re-examination of the monensin-induced changes in cisternal architecture and functional activities of the Golgi apparatus of sycamore suspension-cultured cells. J Cell Sci 104: 819–831

    PubMed  Google Scholar 

  • Ziegel RF, Dalton AJ (1962) Speculations based on the morphology of the Golgi system in several types of protein secreting cells. J Cell Biol 15: 45–54

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departments of Botany and Plant Pathology, Purdue University, Agricultural Research Building, 47907-1057, West Lafayette, IN, USA

    Charles E. Bracker

  2. Departments of Medicinal Chemistry and Pharmacognosy, Purdue University, West Lafayette, Indiana

    D. James Morré

  3. Biology Department, Goshen College, Goshen, Indiana

    Stanley N. Grove

Authors
  1. Charles E. Bracker
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. James Morré
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stanley N. Grove
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bracker, C.E., James Morré, D. & Grove, S.N. Structure, differentiation, and multiplication of Golgi apparatus in fungal hyphae. Protoplasma 194, 250–274 (1996). https://doi.org/10.1007/BF01882032

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01882032

Keywords

Search

Navigation