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Basket Scales of the Green Alga, Mesostigma Viride: Chemistry and Ultrastructure

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Basket Scales of the Green Alga, Mesostigma Viride: Chemistry and Ultrastructure Basket scales of the green alga, Mesostigma viride: chemistry and ultrastructure DAVID S. DOMOZYCH* Department of Biology, Skidmore College, Saratoga Springs, NY 12866, USA BRIAN WELLS and PETER J. SHAW Department of Cell Biology, John Innes Institute for Plant Science Research, Colney Lane, Norwich NR4 7UH, UK * Author for correspondence Summary The unicellular green algal flagellate, Mesostigma tially digested scales revealed the presence of two viride, possesses an extracellular matrix consisting protein components, a high Mr, non-migrating form of three layers of highly distinct scales. This study and a form with a Mr of approximately 48000. focused upon the elaborate basket scales. The basket Further biochemical analyses of scales showed the scale is approximately 450-500 nm in height and presence of two major sugars: glucose and the consists of a solid base, two distinct lattices, two unusual keto sugar acid, 3-deoxy-lyxo-2-heptulosaric upper rims and various struts and roots. Pure acid, or DHA. Antibodies to scales were raised in rats preparations of isolated basket scales were obtained and used in immunolabeling studies. It is estimated and used for subsequent chemical and immunologi- from immunofluorescence studies that a cell of 8 /on cal analyses. X-ray microanalyses revealed the scale contains about 800 basket scales. The scales are in a as being mineralized with both calcium and phos- close-packed arrangement resulting in quasi-crystal- phorus. Fourier Transform Infrared Spectroscopic line arrays upon the cell surface. analyses revealed the presence of phosphate, sugges- ting in turn that the basket scale is complexed with Key words: basket scales, extracellular matrix, Mesostigma, calcium phosphate. SDS-gel electrophoresis of par- DHA, calcium phosphate. Introduction 1989). In some genera, hundreds of thousands of scales may coat the surface of a single cell (e.g. see Moestrup and The extracellular matrices of green plants constitute a Walne, 1979). Electron-microscopic studies have revealed heterogeneous assortment of biochemicals and complexed that the scales are processed within the Golgi apparatus minerals. Modern research efforts have shown that these (GA) (Manton, 1966; Manton and Ettl, 1965; for review, coverings range from the polysaccharide/glycoprotein- see Domozych, 1984). Because of their distinctive shape based cell wall meshwork of higher plants, to crystalline and intricate substructure, specific information concern- glycoprotein walls of chlamydomonad flagellates, to ing the precise morphological aspects of GA-mediated mineralized coverings of green algae (Roberts, 1989; processing of individual scale types has been gathered for Roberts et al. 1985; Adair and Snell, 1990; Varner and Lin, some forms (Moestrup and Walne, 1979). However, little if 1989; Simkiss and Wilbur, 1989; Porcella and Walne, anything is known about the chemistry of the various 1980). In addition to understanding the chemical nature scale types or the biochemistry of the unique secretory and polymeric microarchitecture of plant cell coverings, system involved in scale ontogenesis. recent research has just begun to focus upon elucidating Recently, attempts have been made to elucidate the the secretory pathways involved in the intracellular chemical nature of flagellar membrane scales and thecal processing of plant extracellular matrices (Ali et al. 1986; scale components in thecate, green algal flagellates, close Brummel et al. 1990; Moore et al. 1991; Moore and relatives of prasinophycean forms (Becker et al. 1989, Staehelin, 1988; Staehelin and Chapman, 1987; Staehelin 1990). These studies have reported distinct 2-keto-sugar et al. 1990). In the most primitive, extant group of green acid-containing polysaccharides and distinct protein com- plants, the Prasinophyceae or Micromonadophyceae (Mat- ponents. As part of an ongoing study of the secretory tox and Stewart, 1984; Norris, 1980), many organisms are network in scale-bearing green algae, an analysis of the characterized by a distinct extracellular covering of scales. large, outer body scales of the freshwater prasinophyte, The various scale types often possess elaborate mor- Mesostigma viride, was undertaken. This report describes phology and are often arranged in multiple layers upon structural and chemical analyses of the distinct basket the cell and flagellar surfaces (Pennick, 1984; Domozych, scales. Journal of Cell Science 100, 397-407 (1991) Printed in Great Britain © The Company of Biologists Limited 1991 397 Materials and methods and stored at -80°C or freeze dried. For electron microscope analysis of purity, scales were pelleted down into Beem capsules, General and electron-microscopic analyses fixed with 1 % OsO4/0.05 M cacodylate buffer (pH 7.8), dehydrated Cultures of Mesostigma viride (CCAP 50/1) were routinely in acetone and infiltrated and embedded with Spurr's resin. maintained in sterile Woods Hole medium (Nichols, 1973) Sectioning and TEM observation were performed as above. In enriched with soil extract (9 parts Woods Hole medium to 1 part some instances, scales were dried on a Formvar-coated/carbon- soil extract) in 250 ml sterile Erlenmyer flasks in a Sherer Growth stabilized copper grid and rotary shadowed. chamber (14/10 light-dark cycle, 2000 lux cool white fluorescent light, 17(±1)°C). Transfers were made every 2 weeks. For mass Biochemical and dissolution analyses cultures, Mesostigma cultures were maintained in sterile, 151 Scales were processed for electrophoresis by previously described glass containers under the above conditions. Sterile air was methods (Hames, 1981). Scales were partially dissolved by boiling pumped into the culture solution to maintain suspension for 3 min in 0.0625 M Tris-HCl (pH6.8), 2% SDS, 5% agitation. 2-mercaptoethanol, 10 % glycerol and 0.002 % Bromophenol Blue. Digested scale components were separated on a 5% to 15% Cells were processed for routine transmission electron mi- polyacrylamide gel with a discontinuous buffer system. Total croscopy (TEM) using previously described techniques (Domo- carbohydrate determination was by the method of Kochert zych, 1987). For immunocytochemistry, cells were fixed at 4°C for (1978a) and total protein determination was by the method of 30min in 0.5% glutaraldehyde in 0.05 M cacodylate buffer Kochert (19786). For scale dissolution analyses, a solution of (pH 7.8). Cells were then washed with cold (4°C) cacodylate buffer 1 mgml"1 of scales in distilled water was prepared, separated into three times by gentle resuspension and centrifugation. Cells were 0.2 ml aliquots in 1.5 ml centrifuge tubes and centrifuged in a then pelleted into the tip of a cold beem capsule. Immediately microcentrifuge. The resultant scale pellets were resuspended in: thereafter, cells were sequentially dehydrated to 70 % ethanol in 0.1 M EDTA, 0.1 M EGTA, 200 mM CDTA, 2M KOH, 1M HC1, 1% 10% increments (lOmin/increment) at 4°C. After lOmin in 70% SDS, 67% H2SO4, 0.5 M boric acid, 4 M urea, 2 M sodium ethanol, the beems capsules were brought to -20°C in a cold box perchlorate or distilled water. For room temperature studies, as described by Wells (1985). Dehydration then continued in 10 % tubes were kept at 25 °C for 1-2 h or placed in a boiling water bath increments (20 min/increment) to 100% ethanol. Beem capsules for 5 min or for EGTA and CDTA, placed in a 60 °C oven for 2h. with cells were then sequentially infiltrated with 10 %, 20 %, 30 %, After treatments, the individual tubes, were centrifuged and 50%, 60%, 75%, 90% and 100% London resin (LR White, pellets (if present) were washed with 50 mM Tris-HCl buffer and Medium Grade; Agar Aids, UK) in an ethanol series (2h per recentrifuged. Suspensions of resultant pellets were processed infiltration stage). The London resin was prepared with an and used for TEM and immunoblot analyses as described ultraviolet (UV) accelerator (0.5% benzoin methyl ether). Beem elsewhere in this study. When no pellet was visible, it was capsules were then left overnight at — 20 °C in 100 % London resin. assumed that the scales were digested. After a fresh change of London resin the next morning, the beem capsule-cell preparations were hardened by 24 h of indirect UV A carbohydrate analysis of the scales was performed at the light treatment at -20°C followed by an additional indirect UV Complex Carbohydrate Research Center (Athens, Georgia, USA). polymerization at room temperature for an additional 24 h. For glycosyl composition and linkage analysis, two methods were Antimonate labeling preparations and subsequent control used: trimethylsilyl (TMS) methylglycoside analysis (for identifi- EGTA digestion analyses were performed by the method of Wick cation of acidic sugars, amino sugars and neutral sugars) and alditol acetate analysis (for neutral sugars) (York etal. 1985). The and Hepler (1980). In addition, dissolution of antimonate preparation of TMS methylglycosides was accomplished by precipitates in sections with 200 mM CDTA (trans-l,2-diamino- dissolving the sample in 1M HC1 in methanol at 100 °C for 18 h. cyclohexane-./V,iV,iv'',iV'-tetraacetic acid) was also undertaken. The solvents were evaporated, the sample was then iV-acetylated For all TEM preparations, sections were cut using a Reichert using pyridine/acetic anhydride in methanol. The solvents were Ultratome ultramicrotome and viewed on a JEOL 1200 EX TEM then again evaporated. The sample was then reacted with Tri-Sil at 80 kV. For routine analyses, sections were stained with reagent (Pierce Chem.) at 80°C for 20 min. The solvents were then standard uranyl acetate/lead citrate prior to TEM viewing. evaporated and the samples were dissolved in hexane and analyzed by gas chromatography (GC) and GC/mass spectral Basket scale isolation analysis (MS). Alditol acetates were prepared by hydrolyzing the sample in 2 M trifluoroacetic acid (TFA) at 120 °C for 2h. Solvents Basket scale isolation was performed as follows: cells from mass were evaporated. The sample was reduced with sodium boro- cultures were harvested using a Sorvall continuous-flow centrifu- deuteride in acetic acid. Borate was removed by repeated gation device (type KSB Szent-Gyorgiyi and Blum) attached to an evaporations with methanol/acetic acid.
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