Planta (Berl.) 90, 370--373 (1970)
Short Communication
Central Dilations in Maturing golgi Cisternae-a Common Structural Feature Among Plant Cells ? W~R W. F~A~KE Division of Cell Biology, Institute of Biology II, University of l~reiburg i. Br. l~eeeived November 24~,1969
Sum~ary. Centrally located dilations of the first or second distal-most Golgi eisternae can be observed in diverse plant cells. Their significance and distribution as well as a possible functional correlation to polysaccharide formation is discussed. In a recent publication Brown et al. (1970) have shown that the formation of the cellulosic component of the wall scales of the marine chrysophycean alga Pleurochrysis scher]felii is initiated in distinct cisternae of its Golgi apparatus which are recognized by a central dilation. This dilated cisternal area is distinguished in many instances, by a more or less developed dense layer on its membraneous surface. A tentative functional interpretation of these dilated areas has led to their designation as "centers of polymerization" of the cellulosic microfibrils. Close inspection of onion root tip material has revealed that comparable central dilations occur also in dictyosomes of higher plants. They could be found in rootcap cells as well as in cells of the apical and the postmeristematic zone (Figs. 1--3). I n the dictyosomes of these cells usually comprising 5 to 8 eisternae, either the first or the second distal-most cisternae exhibited such a central dilation. Although they can be observed after all the different fixation procedures employed, including permanganate (compare also Falk, 1962; Mollenhauer, 1965a) and sequential glutaraldehyde-OsO~ fixations they seem to be more prominent after simultaneous use of aldehyde and OsO 4 according to the procedure previously described (Franke et al., 1969). In this connection it is perhaps worth mentioning that after simultaneous fixation the intercisternal fibrils (Turner and Whaley, 1965; Mollenhauer, 1965b; Mollenhauer and Mort6, 1966 ; first description for onion root tip material by Cunningham et al., 1966) could be frequently detected in the material studied (insert,
Fig. 2). The diameter of the above mentioned inflated area of a Golgi cisterna varied in the range from 60 to 300 nm. I n contrast to Pleurochrysis, no
Figs. 1--3. Dilated areas in the central parts of maturing Golgi cisternae in cells of the postmeristematic cylinder (Fig. 1, arrows), of the rootcap (Fig. 2), and the protoderm (Fig. 3) of onion roots. Insert in Fig. 2 shows the intercisternal fibrill~r material of such dictyosomes. Fixation, simultaneous glutaraldehyde-OsQ with postosmication; embedding, Araldite; sectioning, l~eichert ultramicrotome OmU 2; staining, uranyl acetate followed by lead citrate. Magnifications: Figs. 1 and 3, • 50,000; Fig. 2, • 70,000; insert in Fig. 2, • 100,000
372
W.W. Franke:
significant electron dense layer on the intracisternal side of this dilated part could be encountered. Similar central dilations of maturing Golgi cisternae can also be seen in micrographs presented b y other authors from algal (e.g. Stoermer et al., 1965; Falk, 1967; Falk and Kleinig, 1968; Mollenhauer et al., 1968) as well as from higher plant cells (e.g. Perner, 1958; Falk, 1962; Mollenhauer, 1965a). Thus, it seems likely that this structural feature of the plant Golgi apparatus is of wider distribution than hitherto recognized. I n dictyosomes of animal cells, even of those which are known to be highly active in Golgi-mediated polysaccharide formation (e.g. Neutra and Leblond, 1966), such dilations apparently are not a regular structural feature. Considering the relative frequency of the central dilated areas captured in thin sections one has to take into account t h a t they appear only in precise "through-center" sections of the dictyosomes. From the aforementioned finding b y Brown et al. (1970) and in the light of the increasing evidence that synthesis of cellulosic (see also Brown et al., 1969; R a y et al., 1969) and non-cellulosic (for reviews see Northeotc and Pickett-Heaps, 1966; SchnepI, 1969)polysaccharides generally takes place within Golgi cisternae it is tempting to look upon this central dilation as a morphological indicator of certain stages in the formation of polysaccharides. However, since such a localized central swelling of maturing cisternae is found, e.g., also in the silicon matter producing dictyosomes of the diatom Aml)hipleura (Stoermer et al., 1965) it should perhaps be interpreted, in the author's opinion, as a result of the fixation (or dehydration) induced by local differences in the membrane composition or in the cisternal contents rather than as representing an in vivo condition. Polar changes in membrane structure and composition as well as in cisternal contents following the Golgi maturation gradient are well known to be present in plant and animal cells (e.g. Grove et al., 1968). Helpful discussions with Drs. R.M. Brown (University of North Carolina, Chapel Hill) and H. Falk are gratefully acknowledged. Re%rences
Brown, R. M., Jr., Franke, W.W., KMnig, H., Falk, H., Sitte, P.: A cellulosic wall component produced by the Golgi apparatus. Science, 66, 894--896 (1969). Scale formation in chrysophycean algae. I. J. Cell Biol. in press (1970). Cunningham, W. P., Morr6, D. J., Mollenhaucr, H. H. : Structure of isolated plant Golgi apparatus revealed by negative staining. J. Cell Biol. 28, 169--176 (1966). Falk, H. : Zur Physiologic der Golgi-Apparate in der Wurzelhaube der Zwiebel. Z. Naturforsch. 176, 862--863 (1962).
Dilations in Maturing Golgi Cisternae
373
Falk, H. : Zum Feinbau yon Botrydium granulatum Grey. (Xanthophyceae). Arch. Mikrobiol. 58, 212--227 (1967). - - Kleinig, H. : Feinbau und Carotinoide yon Tribonema (Xanthophyceae). Arch. Mikrobiol. 61, 347--362 (1968). Franke, W. W., Krien, S., Brown, R. M., Jr. : Simultaneous glutaraldehyde-osmium tetroxide fixation with postosmication. Histochemie 19, 162--164 (1969). Grove, S.N., Bracker, C. E., MorrO, D. J.: Cytomembrane differentiation in the endoplasmic reticulum-Golgi apparatus-vesicle complex. Science 161, 171--173 (1968). Mollenhauer, I-I. It. : Transition forms of Golgi apparatus secretion vesicles. J. Ultrastrnct. Res. 12, 439--446 (1965a). - - An intercisternal structure in the Golgi apparatus. J. Cell Biol. 24, 504--511 (1965b). - - Evans, W., Kogut, C.: Dictyosome structure in Euglena gracilis. J. Cell Biol. 37, 579--583 (1968). - - Morr6, D. J. : Golgi apparatus and plant secretion. Ann. gev. Plant Physiol. 17, 27--46 (1966). Neutra, M., Leblond, C. P. : Synthesis of the carbohydrate of mucus in the Golgicomplex as shown by electron microscope radioautography of Goblet cells from rats injected with glucose-H3. J. Cell Biol. 30, 119--130 (1966). Northcote, D. H., Pickett-Heaps, J. D. : A function of the Golgi apparatus in polysaccharide synthesis and transport in the root-cap cells of wheat. Biochem. J. 98, 159--167 (1966). Perner, E. S. : Elektronenmikroskopische Untersuehungen zur Cytomorphologie des sogenannten ,,Golgisystems '~ in ~Vurzelzellen verschiedener Angiospermen. Protoplasma 49, 407, 446 (1958). Ray, P. M., Shininger, T. L., Ray, M. M. : Isolation of fl-glucan synthetase particles from plant cells and identification with Golgi membranes. Proc. nat. Acad. Sci. (Wash.), in press (1969). Schnepf, E. : Sekretion und Exkretion bei Pflanzen. Protoplasmatologia, VIII, 8. Wien-New York: Springer 1969. Stoermer, E . F . , Pankratz, It. S., Bowen, C.C.: Fine structure of the diatom Amphipleura pellucida II. Cytoplasmic fine structure and frustule formation. Amer. J. Bot. 52, 1067--1078 (1965). Turner, F . R . , Whaley, W. G.: Intercisternal elements of the Golgi apparatus. Science 147, 1303--1304 (1965). Dr. Werner W. Franke Lehrstuhl fiir Zellbiologie Institut ftir Biologie I I d . Universit~t 7800 Freiburg i. Br. Sch~nzleweg 9--11
Short Communication
Central Dilations in Maturing golgi Cisternae-a Common Structural Feature Among Plant Cells ? W~R W. F~A~KE Division of Cell Biology, Institute of Biology II, University of l~reiburg i. Br. l~eeeived November 24~,1969
Sum~ary. Centrally located dilations of the first or second distal-most Golgi eisternae can be observed in diverse plant cells. Their significance and distribution as well as a possible functional correlation to polysaccharide formation is discussed. In a recent publication Brown et al. (1970) have shown that the formation of the cellulosic component of the wall scales of the marine chrysophycean alga Pleurochrysis scher]felii is initiated in distinct cisternae of its Golgi apparatus which are recognized by a central dilation. This dilated cisternal area is distinguished in many instances, by a more or less developed dense layer on its membraneous surface. A tentative functional interpretation of these dilated areas has led to their designation as "centers of polymerization" of the cellulosic microfibrils. Close inspection of onion root tip material has revealed that comparable central dilations occur also in dictyosomes of higher plants. They could be found in rootcap cells as well as in cells of the apical and the postmeristematic zone (Figs. 1--3). I n the dictyosomes of these cells usually comprising 5 to 8 eisternae, either the first or the second distal-most cisternae exhibited such a central dilation. Although they can be observed after all the different fixation procedures employed, including permanganate (compare also Falk, 1962; Mollenhauer, 1965a) and sequential glutaraldehyde-OsO~ fixations they seem to be more prominent after simultaneous use of aldehyde and OsO 4 according to the procedure previously described (Franke et al., 1969). In this connection it is perhaps worth mentioning that after simultaneous fixation the intercisternal fibrils (Turner and Whaley, 1965; Mollenhauer, 1965b; Mollenhauer and Mort6, 1966 ; first description for onion root tip material by Cunningham et al., 1966) could be frequently detected in the material studied (insert,
Fig. 2). The diameter of the above mentioned inflated area of a Golgi cisterna varied in the range from 60 to 300 nm. I n contrast to Pleurochrysis, no
Figs. 1--3. Dilated areas in the central parts of maturing Golgi cisternae in cells of the postmeristematic cylinder (Fig. 1, arrows), of the rootcap (Fig. 2), and the protoderm (Fig. 3) of onion roots. Insert in Fig. 2 shows the intercisternal fibrill~r material of such dictyosomes. Fixation, simultaneous glutaraldehyde-OsQ with postosmication; embedding, Araldite; sectioning, l~eichert ultramicrotome OmU 2; staining, uranyl acetate followed by lead citrate. Magnifications: Figs. 1 and 3, • 50,000; Fig. 2, • 70,000; insert in Fig. 2, • 100,000
372
W.W. Franke:
significant electron dense layer on the intracisternal side of this dilated part could be encountered. Similar central dilations of maturing Golgi cisternae can also be seen in micrographs presented b y other authors from algal (e.g. Stoermer et al., 1965; Falk, 1967; Falk and Kleinig, 1968; Mollenhauer et al., 1968) as well as from higher plant cells (e.g. Perner, 1958; Falk, 1962; Mollenhauer, 1965a). Thus, it seems likely that this structural feature of the plant Golgi apparatus is of wider distribution than hitherto recognized. I n dictyosomes of animal cells, even of those which are known to be highly active in Golgi-mediated polysaccharide formation (e.g. Neutra and Leblond, 1966), such dilations apparently are not a regular structural feature. Considering the relative frequency of the central dilated areas captured in thin sections one has to take into account t h a t they appear only in precise "through-center" sections of the dictyosomes. From the aforementioned finding b y Brown et al. (1970) and in the light of the increasing evidence that synthesis of cellulosic (see also Brown et al., 1969; R a y et al., 1969) and non-cellulosic (for reviews see Northeotc and Pickett-Heaps, 1966; SchnepI, 1969)polysaccharides generally takes place within Golgi cisternae it is tempting to look upon this central dilation as a morphological indicator of certain stages in the formation of polysaccharides. However, since such a localized central swelling of maturing cisternae is found, e.g., also in the silicon matter producing dictyosomes of the diatom Aml)hipleura (Stoermer et al., 1965) it should perhaps be interpreted, in the author's opinion, as a result of the fixation (or dehydration) induced by local differences in the membrane composition or in the cisternal contents rather than as representing an in vivo condition. Polar changes in membrane structure and composition as well as in cisternal contents following the Golgi maturation gradient are well known to be present in plant and animal cells (e.g. Grove et al., 1968). Helpful discussions with Drs. R.M. Brown (University of North Carolina, Chapel Hill) and H. Falk are gratefully acknowledged. Re%rences
Brown, R. M., Jr., Franke, W.W., KMnig, H., Falk, H., Sitte, P.: A cellulosic wall component produced by the Golgi apparatus. Science, 66, 894--896 (1969). Scale formation in chrysophycean algae. I. J. Cell Biol. in press (1970). Cunningham, W. P., Morr6, D. J., Mollenhaucr, H. H. : Structure of isolated plant Golgi apparatus revealed by negative staining. J. Cell Biol. 28, 169--176 (1966). Falk, H. : Zur Physiologic der Golgi-Apparate in der Wurzelhaube der Zwiebel. Z. Naturforsch. 176, 862--863 (1962).
Dilations in Maturing Golgi Cisternae
373
Falk, H. : Zum Feinbau yon Botrydium granulatum Grey. (Xanthophyceae). Arch. Mikrobiol. 58, 212--227 (1967). - - Kleinig, H. : Feinbau und Carotinoide yon Tribonema (Xanthophyceae). Arch. Mikrobiol. 61, 347--362 (1968). Franke, W. W., Krien, S., Brown, R. M., Jr. : Simultaneous glutaraldehyde-osmium tetroxide fixation with postosmication. Histochemie 19, 162--164 (1969). Grove, S.N., Bracker, C. E., MorrO, D. J.: Cytomembrane differentiation in the endoplasmic reticulum-Golgi apparatus-vesicle complex. Science 161, 171--173 (1968). Mollenhauer, I-I. It. : Transition forms of Golgi apparatus secretion vesicles. J. Ultrastrnct. Res. 12, 439--446 (1965a). - - An intercisternal structure in the Golgi apparatus. J. Cell Biol. 24, 504--511 (1965b). - - Evans, W., Kogut, C.: Dictyosome structure in Euglena gracilis. J. Cell Biol. 37, 579--583 (1968). - - Morr6, D. J. : Golgi apparatus and plant secretion. Ann. gev. Plant Physiol. 17, 27--46 (1966). Neutra, M., Leblond, C. P. : Synthesis of the carbohydrate of mucus in the Golgicomplex as shown by electron microscope radioautography of Goblet cells from rats injected with glucose-H3. J. Cell Biol. 30, 119--130 (1966). Northcote, D. H., Pickett-Heaps, J. D. : A function of the Golgi apparatus in polysaccharide synthesis and transport in the root-cap cells of wheat. Biochem. J. 98, 159--167 (1966). Perner, E. S. : Elektronenmikroskopische Untersuehungen zur Cytomorphologie des sogenannten ,,Golgisystems '~ in ~Vurzelzellen verschiedener Angiospermen. Protoplasma 49, 407, 446 (1958). Ray, P. M., Shininger, T. L., Ray, M. M. : Isolation of fl-glucan synthetase particles from plant cells and identification with Golgi membranes. Proc. nat. Acad. Sci. (Wash.), in press (1969). Schnepf, E. : Sekretion und Exkretion bei Pflanzen. Protoplasmatologia, VIII, 8. Wien-New York: Springer 1969. Stoermer, E . F . , Pankratz, It. S., Bowen, C.C.: Fine structure of the diatom Amphipleura pellucida II. Cytoplasmic fine structure and frustule formation. Amer. J. Bot. 52, 1067--1078 (1965). Turner, F . R . , Whaley, W. G.: Intercisternal elements of the Golgi apparatus. Science 147, 1303--1304 (1965). Dr. Werner W. Franke Lehrstuhl fiir Zellbiologie Institut ftir Biologie I I d . Universit~t 7800 Freiburg i. Br. Sch~nzleweg 9--11
