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Phosphatases and Differentiation of the Golgi Apparatus

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Phosphatases and Differentiation of the Golgi Apparatus J. Cell Sci. 4, 455-497 (1969) 455 Printed in Great Britain PHOSPHATASES AND DIFFERENTIATION OF THE GOLGI APPARATUS MARIANNE DAUWALDER, W. G. WHALEY AND JOYCE E. KEPHART The Cell Research Institute, Tlie University of Texas at Austin, Texas, U.S.A. SUMMARY Cytochemical techniques for the electron microscopic localization of inosine diphosphatase, thiamine pyrophosphatase, and acid phosphatase have been applied to the developing root tip of Zea mays. Following formaldehyde fixation the Golgi apparatus of most of the cells showed reaction specificity for IDPase and TPPase. Following glutaraldehyde fixation marked localiza- tion of IDPase reactivity in the Golgi apparatus was limited to the root cap, the epidermis, and the phloem. A parallelism was apparent between the sequential morphological development of the apparatus for the secretion of a polysaccharide product, the fairly direct incorporation of tritiated glucose into the apparatus to become a component of this product and the develop- ment of the enzyme reactivity. Acid phosphatase, generally accepted as a lysosomal marker, was found in association with the Golgi apparatus in only a few cell types near the apex of the root. The localization was usually in a single cisterna at the face of the apparatus toward which the production of secretory vesicles builds up and associated regions of what may be smooth endoplasmic reticulum. Since the cell types involved were limited regions of the cap and epidermis and some initial cells, no functional correlates of the reactivity were apparent. Despite the presence of this lysosomal marker, no structures clearly identifiable as ' lysosomes' were found and the lack of reaction specificity in the vacuoles did not allow them to be so defined. INTRODUCTION The discriminative localization of enzyme activities may serve as a key to under- standing many of the integrated biochemical processes within the cell. Such intra- cellular localization is often possible only by cytochemical techniques. Since these techniques are somewhat limited by problems of methodology, the validity of such findings must ultimately be tested by other analytical techniques. The number of instances in which cytochemical results have been supported by biochemical findings is increasing (for example: cytochemically demonstrable mitochondrial ATPase (Lehninger, 1964; Essner, Fogh & Fabrizio, 1965; Roodyn, 1967), certain ATPases of the sarcoplasmic reticulum (Engel & Tice, 1966; Tice & Engel, 1966), microsomal IDPase, GDPase, and UDPase with cytochemical localization in the endoplasmic reticulum (ER) or the Golgi apparatus (Ernster & Jones, 1962; Novikoff, Essner, Goldfischer & Heus, 1962; Novikoff & Heus, 1963; Goldfischer, Essner & Novikoff, 1964), glucose-6-Pase in the ER (Beaufay, Hers, Berthet & de Duve, 1954; Tice & Barrnett, 1962; Terner, Goodman & Spiro, 1965), and lysosomal hydrolases (see dc Reuck & Cameron (eds.), Ciba Symposium on Lysosomes, 1963; de Duve & Wattiaux, 1966; Straus, 1967)). Reid (1967) has reviewed a number of membrane-associated 456 M. Dauwalder, W. G. Whaley and J. E. Kephart enzymic reactivities. The biochemist can characterize the enzyme system or systems of given cell types or of cellular components which can be isolated in reasonably clean preparations. The enzyme cytochemist, often unable to define the enzyme reaction specifically, can study intracellular localization of activity in cells in situ. The cyto- chemical approach finds particular use in the study of differentiation, where the structural integrity of the cell or tissue system is of major importance and functional diversity is developing. The objective of this study was to determine cytochemically the localization of certain phosphatase activities associated with the Golgi apparatus (Novikoff & Goldfischer, 1961; Goldfischer et al. 1964 and others) in the root tip of Zea mays where morphological sequences of differentiation of the Golgi apparatus for participa- tion in secretory activity have been established. The essentially linear arrangement of cells in this system has allowed close correlation of the cytochemical results with development of functional specialization in three different secretory cell lineages. The enzymes studied were inosine diphosphatase (IDPase), thiamine pyrophospha- tase (TPPase), and acid phosphatase (Acid Pase). It will be shown that the Golgi apparatus of most tissue types shows reactivity for IDPase. It will also be shown that the morphological specialization of the Golgi apparatus for participation in the pro- duction of a largely carbohydrate secretory product in the root cap, the epidermis, and the developing sieve tube elements is paralleled by localization of a particular IDPase activity within the apparatus. This IDPase activity appears to relate to the differentiation of the apparatus for polysaccharide synthesis. Additionally it will be shown that in this system TPPase activity is a generally specific though not a universal 'marker' for the Golgi apparatus. Notably in regions of the root cap, even though they are characterized by secretory activity, the Golgi apparatus did not show TPPase localization. In a limited number of cell types, reactivity of Acid Pase was found predominantly at the face of the Golgi apparatus most closely associated with secretory vesicles. This observation relates to possible lysosomal activity in plant cells. A report on this work has been published previously in abstract form (Dauwalder, Kephart & Whaley, 1966). METHODS AND MATERIALS Methods for the cytochemical studies Seeds of a hybrid strain of Zea mays were germinated and grown in moist filter paper at a temperature of approximately 24 °C. After 6 days, the seedlings were removed and central longitudinal slices (usually less than 0-5 mm thick) of the first 3-4 mm (longer than that indicated in Fig. 1 so that all manipulations could be done without damaging the tip) of several root tips were fixed in the following fixatives: 4% formaldehyde in o-i M phosphate buffer, pHy-8; 4% formaldehyde in o-i M cacodylate buffer, pH 7-2; 4% glutaraldehyde in o-i M phosphate buffer, pHy-8; 4% glutaraldehyde in o-i M cacodylate buffer, pH 7-2. The fixatives contained added trace amounts of calcium chloride. Preliminary attempts to use hydroxyadipaldehyde Golgi differentiation and phosp/iatases 457 fixation for these experiments showed modification of the morphology of the Golgi apparatus and other organelles and very limited indications of reaction product. Fixation was at room temperature for at least an hour, and then overnight in a refri- gerator (about 4-5 °C). The samples were then washed in rapidly running water for 3Hh. The reaction mixtures for the IDPase and TPPase were made up according to Novikoff & Goldfischer (1961): IDP (Sigma Chemical Co.: o-oi M-O-02 M) in distilled water, or TPP (Sigma Chemical Co.: o-oi M-O-03 M) in distilled water i-o ml Distilled water 0-4 ml TrK-maleate buffer, 0-2 M (pH, see below) 2-0 ml 1 % Pb(NO3)2 o-6 ml 0-025 M MnCl2 i-o ml In order to maintain a pH of 7-2 for the final reaction mixture, im-maleate buffer of pH 7-35 was used. Reactions run with the buffer at pH 7-2 or the buffer adjusted to give a final reaction mixture of pH 7-2 gave similar results. Controls were run on all samples by substitution of distilled water for the substrate. Both MnCl2 and MgCl2 were tested as activators. Novikoff et al. (1962) suggested some superiority of MnCl2 at least for the ER and it proved to be slightly better in these experiments; hence it was used in the experiments from which data are reported. All reaction mixture solutions were made up fresh the day the experiment was run and centrifuged prior to use. Incubation was carried out in a water bath at 39 °C for 45 min. In the initial experiments, samples of Helix aspersa ovotestis were run in parallel with the plant material and gave results similar to those reported by Meek & Bradbury (1963). The acid phosphatase medium contained 10 ml 0-05 M acetate buffer, pH 5-0; 13-25 mg Pb(NO3)2, and 30-6 mg sodium /?-glycerophosphate (Sigma Chemical Co.). The mixture was incubated overnight at 37 °C, filtered, and readjusted to a pH of 5-0. Samples were reacted in the mixture for 70 or 90 min at 39 °C. The results were not entirely consistent, but except for a slight variation in the final pH, the procedures were performed in the same way each time. Controls were run in the same mixture minus the substrate. Initial experiments were run on formol-calcium-fixed material, and although evidence of the reaction similar to that to be reported here could be seen, the preservation of the tissue was poor. Following the enzymic incubations, the samples were rinsed in buffer and post-fixed for 4 h in 2% OsO4 made up in the same buffer as the initial fixative, either on ice or at room temperature with comparable results. They were then rinsed again in buffer, dehydrated in graded ethanol, changed into 100% acetone, and embedded in Epon- Araldite plastic stock number I (Mollenhauer, 1964). Sectioning was done with diamond knives on Porter-Blum or LKB microtomes. Sections were observed without post-staining or after post-staining with uranyl acetate and lead citrate, and electron- microscopic investigation was done on RCA EMU3D and 3F microscopes. Both longitudinal and transverse sections of the apical 2 mm including the cap of the 458 M. Dauwalder, W. G. Whaley andj. E. Kephart samples were used to define tissue types and determine the extent of penetration of the reaction mixture. In initial experiments run to determine hydrolysis time, samples for study by light microscopy were treated with ammonium sulphide. Phase-contrast microscopic observation of thick, plastic-embedded sections adjacent to the thin sections for electron microscopy was used as means of verifying the electron-micro- scopic data. Two or three root tips per experimental run have been checked, and in electron micrographs over 3000 Golgi stacks have been scored for their reactivity.
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