|
Basic Research THE LABORATORY OF R. MALCOLM BROWN, JR. Online Article |
|
Algae as tools in studying the biosynthesis of cellulose, nature's most abundant macromolecule R. Malcolm Brown, Jr. Department of Botany The University of Texas at Austin Austin, Texas 78712 U.S.A. Taken from: Experimental Phycology. Cell Walls and Surfaces, Reproduction, Photosynthesis. 1990 (pp 20-39) Ed. W. Wiessner, D.G. Robinson, and R. C. Starr Springer-Verlag Berlin Heidelberg New York London Paris Tokyo Hong Kong Barcelona ISBN 3-540-52496-7 Contents
INTRODUCTION
The most dominant polysaccharide of the cell wall is cellulose. The universal distribution of this natural polymer among prokaryotic and eukaryotic organisms attests to its ancient evolutionary history. Not only is cellulose found among photosynthetic and protistan cells, it is present in animals such as the Ascidians (Wardrop, 1970). Furthermore, levels of elevated cellulose synthesis have been suggested in humans with the disease scleroderma (Hall, et al, 1960). The algae have been prominent organisms of study among eukaryotic organisms because of their great diversity of structure and cellular organization. Chloroplast morphology (Gibbs, 1981), organization of the mitotic apparatus (Pickett-Heaps, 1972), cell wall structure and composition (Preston, 1974), flagellar apparatus (Stewart and Mattox, 1978), and reproduction have provided a wealth of information on algal phylogeny (Stewart and Mattox, 1982); however, very few studies have concentrated on evolutionary and phylogenetic aspects of cell walls, let alone cellulose, mainly because the cellulose synthases had never been observed or isolated. In 1976, the first successful application of freeze fracture demonstrated the structure of a cellulose synthase complex in Oocystis apiculata (Brown and Montezinos, 1976). These membrane associated structures, called terminal synthesizing complexes (=TCs), were found at the growing tip of microfibril impressions on the E-fracture face of the plasma membrane. Earlier, Roelofsen (1958) had predicted that an organized terminal enzyme complex would be found; however, the shape and geometry could not be predicted at that time. In 1964, Preston proposed the ordered granule hypothesis for the cellulose synthase complex. This study was based on observations of remnants of organized particle subunits associated with the innermost wall of Chaetomorpha. During this time, the freeze fracture technique was becoming widely used, and organized particle complexes were found in the plasma membranes, particularly abundant in yeasts (Moor and Muhlethaler, 1963). Thus, a logical extension of the possibility of such an organization could be made for the cellulose synthesizing complex. Interestingly, TCs were not observed in cells which had been chemically fixed or treated with glycerol or cryoprotectants. The breakthrough in finding TCs came when Brown and Montezinos demonstrated that rapid direct freezing of living cells yielded organized particle structures associated with the tips of microfibrils. Since 1976, TCs have been found in more than 14 algal genera, and presently, a distinct pattern of TC structure is beginning to emerge which provides some insight into the substantial diversity of cellulose microfibril synthesis among the algae. In this presentation, the fundamental TC diversity among the algae will be described. Because TC variation is the greatest among the algae, it also provides hints at the relationship between TC organization and microfibril shape, molecular weight of the cellulose, and crystallization. Phylogenetic relationships based on TC structure can be correlated with other structural and biochemical evidence. This presentation will conclude with a proposed evolutionary history of cellulose biogenesis. So far, only two basic forms of TCs have been found among eukaryotic cells. The linear TC was first discovered in Oocystis and is present among most members of the Ulvophyceae (Hotchkiss and Brown, 1989) (Fig 1). The rosette TC was reported simultaneously by Mueller and Brown (1980) and Giddings, et a], (1980). Earlier, Mueller, et al (1976) had observed a globular component of the TC on the E-fracture face of the plasma membrane in corn roots. Subsequent examination of the P-fracture face revealed a rosette of 6 symmetrically organized particle subunits (Fig 2). Unlike that in the corn root, the rosette TC found in Micrasterias frequently is organized in ordered arrays, especially during secondary wall formation (Giddings, et al, 1980). Furthermore, the rosette subunits have been shown to span both layers of the bimolecular leaflet. Since these first reports, rosette TC's have been found in a variety of organisms, ranging from the land plants to Chara (McLean and Juniper, 1986) and Nitella (Hotchkiss and Brown, 1987).
Interestingly, only the rosette TC has been found among the vascular plants. Thus, algal ancestors with rosette TCs have assumed added importance with respect to understanding the evolution of land plants. For a more detailed elaboration of the distribution of TC's among eukaryotic cells, consult the report of Brown (1985). Since this publication, TCs have been found in other organisms and will briefly described. In 1987, Hotchkiss and Brown described a solitary rosette TC in Nitella translucens (Hotchkiss and Brown, 1987). This TC is virtually indistinguishable from that of land plants, in addition, a solitary- rosette TC has been observed in Chara (McLean and Juniper, 1986). Only in the Zygnematales has an ordered consolidation of TC's been found, and among one member, Mougeotia, the TCs are exclusively solitary (Hotchkiss et al 1989 ). Thus, the consolidation of rosette TCs appears to have been a more recent event (Hotchkiss and Brown, 1989a). When wall composition is taken into consideration, the evidence strongly supports that the Charophyceae is the phylogenetic line which may have given rise to the vascular plants. Another interesting and different TC structure recently was found in the xanthophycean genus, Vaucheria (Mizuta et al, 1989). Overall, the TC is linear, but the subunit arrangement within the TC is in the form of unique diagonal rows (Fig 3).
The relationship between TC geometry and microfibril shape is better understood in Vaucheria (Mizuta et al, 1989). Each subunit of the diagonal row assembles a single glucan chain. Glucan chain products of the diagonal row aggregate to form an ordered aggregate. Aggregates unite laterally to form a thin ribbon-shaped microfibril. Whether or not the peculiar subunit geometry within the linear TC of Vaucheria is indicative of other xanthophycean algae is unknown at present. Vaucheria is yet but another example demonstrating the great diversity of cellulose biogenesis among the algae. With the rudimentary evidence at hand, one can now consider the evolution of cellulose biogenesis. THE EVOLUTION OF THE TC AND CELLULOSE BIOGENESIS Based on TC ultrastructure and cellulose organization, it is possible to construct a phylogenetic pathway for cellulose biogenesis (Fig 4). Although somewhat premature, this treatment gives several important and interesting clues to the subject of eukaryotic cellular evolution. Clearly, the algae as a group have been pivotal in the diversification of cellulose microfibril assembly as exemplified by the diversity of TC and microfibril morphology. The evolution of cellulose among prokaryotic cells will first be considered. The fact that cellulose assembly occurs among two widely divergent prokaryotic groups suggests that this process must have been an ancient one. The investigations of Woese have shed much light on bacterial evolution. Using homologous sequences in rRNA, it has been possible to unambiguously examine and measure phylogenetic relationships among the bacteria (Woese, 1987). The genus, Sarcina is a gram + bacterium and is considered primitive among the eubacteria. Sarcina also is an obligate anaerobe. Cellulose synthesis in Sarcina was first described by Canale-Parola et al (1961). We have also studied cellulose synthesis in Sarcina (Roberts and Brown, unpublished data) and have come to the conclusion supporting Canale-Parola et al that only the cellulose II polymorph is synthesized. The exact site of cellulose synthesis is unknown; however, membrane fractions of Sarcina can synthesize cellulose II in vitro (Lin, Roberts, and Brown, unpublished data).
Among the prokaryotes, the purple bacteria as a group are thought to be more advanced (Woese, 1987). They have been considered as progenitors of mitochondria in the eukaryotic cell (Yang et al, 1985). Interestingly, many genera in this group synthesize cellulose. These include, Acetobacter, Rhizobium, and Agrobacterium (Deinema and Zevenhuizen, 1971). As Woese points out, the purple bacteria are closely related and seem to have evolved special relationships with vascular plants as exemplified by nodules for nitrogen fixation in Rhizobium to tumors in Agrobacterium. The cellulose of Agrobacterium has been proposed to aid in establishing the virulence although it is not critical (Matthysee, 1983). The cellulose synthesized by Rhizobium may aid in attaching the bacterium to the root hair tip where it will initiate infection thread formation (Roife and Gresshoff, 1988). In addition, cellulose is synthesized in Alcaligenes; however no cellulose synthesis has been observed in E. coli. Among the purple bacteria, only the cellulose I polymorph is synthesized (one exception is a mutation in Acetobacter giving rise to cellulose II synthesis, see Roberts et al, 1989). The site of cellulose microfibril synthesis is a linear row of particles parallel to the longitudinal axis of the cell (Brown et al, 1976). On the surface of the LPS layer of the cell envelope is a pore complex through which fibrils are extruded. The enzyme complex is located in the cytoplasmic membrane (Bureau and Brown, 1987).- Groups of three or more particles are required to assemble subfibrils which consolidate to form a microfibril tangential to the cell surface (Haigler et al, 1980). Microfibrils unite to form bundles which, in turn, group to assemble ribbons. The ribbons are visible with darkfield microscopy, and the progress of cellulose synthesis can be directly monitored using time lapse video microscopy (Brown and Santos, unpublished observations; Brown and Colpitts, 1978; Lin and Brown, 1989). In Rhizobium and Agrobacterium, the sites of cellulose assembly are similar; however, fewer microfibrils consolidate. Only a floe of cellulose is produced, while in Acetobacter, a thick leathery membrane or pellicle is synthesized. The function of cellulose biosynthesis in -Acetobacter is_ unknown. Acetobacter xylinum is an obligate aerobe. Therefore the buoyancy of its cellulose could provide an aerobic environment for cells active in cellulose synthesis (Schramm and Hestrin, 1954). Why Acetobacter would divert large pools of metabolic substrate into cellulose is unknown; however, cellulose could serve as a reserve pool for metabolism. Unfortunately, extensive cellulase activity has not been found; yet, degradation of non-crystalline carboxymethylcellulose can occur (Brown and White, unpublished observations). Fundamental research investigations of cellulose biogenesis in Acetobacter have yielded perhaps the most extensive evidence for the molecular mechanisms of cellulose assembly. Cellulose has now been synthesized in vitro (Glaser, 1958); a specific activator for cellulose synthesis has been found (Ross et al, 1985), the in vitro product characterized morphologically (Lin et al, 1985), the in vitro crystalline polymorph deduced (Bureau and Brown, 1987), the cellular site of the synthase localized (Bureau and Brown, 1987), the cellulose synthase purified (Lin and Brown, 1989,), and gene cloning for the purified enzyme initiated (Saxena and Brown, 1989). Cellulose synthesis among the blue green algae has been mentioned only once in the literature, and conclusive evidence for this is lacking (Frey-Wyssling, 1976). According to Woese (1987), the cyanobacteria emerged from the distance matrix phylogenetic tree of the eubacteria almost from the same region as the gram + bacteria and also close to the purple bacteria. Thus, it is clear that cellulose biogenesis must have been an ancient process during the evolution of life on earth. With the accumulating evidence of cellulose biogenesis among prokaryotes, the evolution of cellulose among this group can now be addressed. The cellulose II polymorph appears to be primitive. This polymorph is the more thermodynamically stable form with an additional inter-chain H-bond formed per glucose residue. Cellulose II can form spontaneously from solution when cellulose is solubilized by such agents as DMSO/paraformaldehyde or cupraammonium reagents (Blackwell et al, 1986). On the other hand, cellulose I is a metastable polymorph, presumably assembled only by living organisms. Therefore, cellulose I is more advanced, requiring additional mechanisms for chain orientation and positioning to achieve the metastable state. The first cellulose producer probably had its glucan synthase randomly organized in association with the membrane (Fig 5). Under these primitive conditions, only cellulose II could bioynthesized in vivo. Thus, in Sarcina, glucan chains appear to be randomly positioned over the cell surface in an amorphous array. Sarcina is an excellent example of an extant organism which lacks mechanisms to consolidate and organize the glucan synthase complex to induce ordered microfibril assembly and aggregation into bundles and ribbons of cellulose 1. On the other hand, the purple bacteria evolved the mechanisms to order glucan chains into various conformations leading to a diversity of cellulose I microfibril assembly. Because of abundant evidence suggesting that the purple bacteria are more advanced (Woese, 1987), it follows that cellulose I assembly is more advanced. A logical extension of this evolutionary advancement is to consider the evolution of cellulose among the eukaryotes. Did these cells obtain genes for cellulose synthesis from the eubacteria? If so, what are the likely candidates? It is obvious that if the mitochondria of eukaryotes came from the purple bacteria, did they also transfer the genes for organized cellulose I synthesis? This is an intriguing question, one which must await cloning and sequencing of the genes for the cellulose synthases. We shall now consider one of the greatest mysteries in biology- the origin of cellulose synthesis among eukaryotic cells. The possibility that the genes for cellulose synthesis may have come from the purple bacteria has been alluded to. What was the first eukaryotic organism to have received the cellulose synthase gene? An examination of phylogenetic trees indicates that among the extant primitive eukaryotes, cellulose is found among one group, namely, the cellular slime molds. Cellulose I of low crystallinity has been found in Dictyostelium (Roberts and Brown, unpublished data). Because Dictyostelium is non-photosynthetic, it seems highly unlikely that it could have received the genes for cellulose synthesis from a photosynthetic prokaryotic progenitor. It seems attractive, therefore, that the purple bacteria may have donated these complexes. Dictyostelium TCs are unlike any so far found among eukaryotic cells. They appear to consist of linear arrays of single particles (Fig. 4' (Mizuta and Brown, unpublished results). These arrays are somewhat similar to those found in Acetobacter. Thus, among eukaryotic organisms, the linear arrangement of single rows of particle subunits (arrows) in Dictyostelium appears to be primitive. This is also supported by the low crystallinity of cellulose I from this organism.
Certain fungi, among them, the Oomycetes, synthesize cellulose. Yet, nothing is known of TC structure among the fungi. This is a major research area which needs immediate attention. One could predict, however, that if Vaucheria is closely related to Saprolegnia, the unique linear TC with diagonal rows (Mizuta and Brown, 1989) might be found in the latter. Why many of the fungi opted for chitin as the major wall polymer is an interesting sidelight to the question of the evolution of cellulose synthesis. Some of the fungi are almost as primitive as Dictyostelium, yet there is scant knowledge of chitin synthesis among primitive eukaryotes, let alone the eubacteria and archaebacteria. Perhaps nutrition may have played a role in the more efficient utilization of strong polymers. Since chitin walled organisms may have required more nitrogen, the energy budget would be greater. Thus, to synthesize a polymer of cellulose would represent a selective advantage from a nutritional point of view (Duchesne and Larson, 1989). THE EVOLUTION OF CELLULOSE SYNTHESIS AMONG PHOTOSYNTHETIC EUKARYOTES At this junction, the algae certainly have played a diversified role, for it is here that the greatest variety of TCs and cellulose structure is found among the algae (Fig 6). Gunderson et al, 1987) have suggested on the basis of 18S rRNA sequences that a cellulose producing oomycete, Achlya bisexual is, is closely related to Ochromonas danica, a chitin producer. Perhaps the fungi and chromophytes appeared at roughly the same time. The recent studies of Pearasso et al, 1989) have shed some light on the origin of the algae. On the basis of 28S cytoplasmic rRNA homology, they found that three distinct groups emerged late among eukaryotes: rhodophytes, chromophytes, and chlorophytes. A late occurrence of eukaryotic photosynthetic symbiosis was implied. The conserved rosette/linear TCs among the algae suggests that the synthase may have come from the more primitive fungi or Dictyostelium, rather than through the chloroplast. Again, this implies that even earlier, the ancient eukaryotic mitochondrion may have contained the genes for cellulose synthase. Could the cellulose synthase of the Rhodophyta have come from the cyanobacteria? This question cannot be answered until we have more data on the presence and physical characteristics of cellulose among the cyanobacteria. If only cellulose II is present among the cyanobacteria, it would be difficult to imagine an independent evolutionary event to organize the TC to allow it to produce cellulose I which is found among the Rhodophyta. If, however, Nostoc is found to produce cellulose I in vivo, the hypothesis that the cyanobacteria could have been the progenitors of the Rhodophyta, would be strengthened. It should be apparent that these questions cannot really be answered, let alone seriously considered, until we have sequence information on the cellulose synthase; yet these questions do need to be placed before the scientific community now so that the blueprint for solving this great mystery can be expedited. The origin of cellulose synthesis among the major algal groups is still a major mystery. Consider that cellulose is known among the Pyrrophyta, the Chrysophycease, the Xanthophyceae, the Phaeophyta, and the Chlorophyta (Fig 6). Did each of these major groups receive a cellulose synthase independently, possibly from pro-chloroplast capture? The diversity of TC structure among these groups might suggest multiple independent captures, yet only the purple bacteria are known to synthesize cellulose I, the same polymorph found among the great diversity of algae (with the exception of Halicystis, Sisson, 1938; Roberts and Brown, 1989, unpublished data). This argues in favor of a single capture of the cellulose synthase very early in eukaryotic evolution, possibly through the purple bacteria donation of the pro- mitochondrial apparatus. This implies that the organizational machinery for glucan chain assembly into the cellulose I polymorph may have also been introduced early through transfer to an ancient eukaryotic progenitor. Then, Dictyostelium may be an example of one of the most ancient surviving groups which received the cellulose synthase from a prokaryotic progenitor. These are provocative questions, but ones which cannot be answered with certainty at present.
Cellulose synthase is an ancient molecule as evidenced by its ubiquity among prokaryotic and eukaryotic organisms. It therefore must have served an important early function in the origin of life on earth. The most advanced eukaryotic land plants have the rosette cellulose synthase TC. Advanced members of the Charophyta have the rosette TC, an so do members of the Zygnemetales. At present, all pieces to the puzzle are not in place. Critically important algae need to be investigated for their TC structure to provide more direct confirming data for the rosette TC in land plant evolution. These include Coleochaetae, members of the Trentepholiales (Cephaleuros), the Klebsormidiales (Klebshormidium), the Chlorokybales (Chlorokybus), and other members of the Zygnematales ( Zygnema, Netrium) . The concept of symbiotic capture of the cellulose synthase in eukaryotic cells needs more study (Fig 7). Did the cellulose synthase come from a mitochondrial progenitor (through the purple bacteria)? Did it originate through a chloroplast progenitor (from the cyanobacteria, pro- chlorophyta, or pro-chromophyta)? Did the cellulose synthase transfer directly from the prokaryote chromosome or plasmid? Perhaps one or more symbiotic captures occurred, giving rise the the diversity of TC morphology and microfibril diversity. The known diversity of cellulose microfibril structure, degree of polymerization, and crystallinity, suggests that secondary modifications to the primary glucan synthase must have occurred. Perhaps even the regulation of cellulose synthase activity has been modified, although cellulose synthase activity appears largely constitutive. The diversity of fibrillar polymers other than cellulose among the algae supports an extremely diverse evolution in cell wall structure, possibly reflecting the wide range of environments for survival. Algae have served as excellent model systems in the quest for understanding cellulose biogenesis. Not only do the algae synthesize diverse forms off cellulose, they offer an uncompromising approach for cytological observation, coupled with a potential for isolation, cloning, and sequencing of the genes involved in cellulose biogenesis. The coming decade will see great advances in cellulose biogenesis research. Appreciation is expressed to Richard Santos for his unfailing loyalty and support throughout the past 19 years. Also, my former and present graduate students, post-doctoral fellows, and visitors to the lab deserve recognition for their contributions to this research. I thank Inger Johansen for preparing this manuscript. This research was supported by the National Science Foundation, The Johnson & Johnson Centennial Chair Endowment, and funds from the University of Texas at Austin. Blackwell J, Lee DM, Kurz D, Su MY (1986) Structure of cellulose-solvent complexes. In: Young R, Rowell RM (eds) Cellulose-Structure, Modification, and Hydrolysis. John Wiley and Sons, New York, p 51-66. Brown Jr RM, Montezinos DL (1976) Cellulose microfibrils: visualization of biosynthetic and orienting complexes in association with the plasma membrane. Proc Natl Acad Sci USA 73: 143-147. Brown Jr RM, Willison JHM, Richardson CL (1976) Cellulose biosynthesis in Acetobacter xylinum; visualization of the site of synthesis and direct measurement of the in vivo process. Proc Natl Acad Sci USA 73:4565-4569. Brown Jr RM, Colpitts TJ (1978) Direct visualization of cellulose synthesis by high resolution darkfield microscopy and time-lapse cinematography. J Cell Biol 79(2):157a. Brown Jr RM (1985) John Innes Symposium - Cellulose microfibril assembly and orientation: recent developments. J Cell Sci Suppl 2:13-32. Brown Jr RM, Lin FC (1989) Time lapse video microscopy of cellulose assembly by Acetobacter xylinum. J Cell Biol 109 (No 4, Pt 2) 90a. Bureau TE, Brown Jr RM (1987) In vitro synthesis of cellulose II from a cytoplasmic membrane fraction of Acetobacter xylinum. Proc Natl Acad Sci USA 84:6985-6989. Canale-Parola E, Borasky R, Wolfe RS (1961) Studies on Sarcina ventriculi. III. Localization of cellulose. J Bacteriol 81:311-318. Deinema MH, Zevenhuizen LPTM (1971) Formation of cellulose fibrils by gram-negative bacteria and their role in bacterial flocculation. Archiv Mikrobiol 78:42-57. Duchesne LC, Larson DW (1989) Cellulose and the evolution of plant life. Bioscience 39(4) :238-241. Frey-Wyssling A (1976). In: Zimmerman W, Cariquist S, Ozenda P, Wuiff HD (eds) The Plant Cell Wall. Gebruder Borntraeger, Berlin Stuttgart, p 277. Gibbs SP (1981) The chloroplasts of some algal groups may have evolved from endosymbiotic eukaryotic algae. Ann New York Acad Sci 361:193-208. Giddings TH, Brower DL, Staehelin LA (1980) Visualization of particle complexes in the plasma membrane of Micrasterias denticulata associated with the formation of cellulose fibrils. J Cell Biol 84:327-339. Glaser L (1958) The synthesis of cellulose in cell-free extracts of Acetobacter xylinum. J Biol Chem 232:627-636. Gunderson JH, Elwood H, Ingold A, Kindle K, Sogin ML (1987) Phylogenetic relationships between chlorophytes, chryso- phytes, and oomycetes. Proc Natl Acad Sci USA 84:5823-5827. Haigler CH, Brown Jr RM, Benziman M (1980) Calcofluor white ST alters cellulose synthesis in Acetobacter xylinum. Science 210:903-906. Hall DA, Happey F, Lloyd PJ, Saxl H (1959) Oriented cellulose as a component of mammalian tissue. 151:497-516. Hotchkiss Jr AT, Brown Jr RM (1987) The association of rosette and globule terminal complexes with cellulose microfibril assembly in Nitella translucens (Charophyceae). J Phycol 23:229-237. Hotchkiss A, and Brown Jr RM (1989) Evolution of the cellulosic cell wall in the charophyceae. In: Schuerch C (ed) Cellulose and Wood- Chemistry and Technology. John Wiley & Sons, New York, p 591-609. Hotchkiss A, Gretz MR, Hicks KB, Brown Jr RM (1989) The composition and phylogenetic significance of the Mougeotia (Charophyceae) cell wall. J Phycol in press. Lin FC, Brown Jr RM, Cooper JB, Delmer DP (1985) Synthesis of fibrils in vitro by a solubilized cellulose synthase from Acetobacter xylinum. Science 230:822-825. Matthysee AG (1983) Role of bacterial cellulose fibrils in Agrobacterium tumefaciens infection. J Bacteriol 154(2) -906-915. McLean B, Juniper BE (1986) The plasma membrane of young Chara internodal cells revealed by rapid freezing. Planta 169:153-161. Mizuta S, Roberts EM, Brown Jr RM, (1989) A new cellulose synthesizing complex in Vaucheria hamata and its relation to microfibril assembly. In: Schuerch, C (ed) Cellulose and Wood - Chemistry and Technology. John Wiley & Sons, New York, p 659-676. Moor H, Muhlethaler K (1963) Fine structure in frozen-etched yeast cells. J Cell Biol 17:609-628. ======== Mueller SC, Brown Jr RM, Scott TK (1976) Cellulosic microfibrils: nascent stages of synthesis in a higher plant cell. Science 194:949-951. Mueller SC, Brown Jr RM (1980) Evidence for an Intramembranous component associated with a cellulose microfibril synthesizing complex in higher plants. J Cell Biol 84:315-326. Pearasso R, Baroin A., Qu LH, Bachellerie JP, Adoutte A (1989) Origin of the algae. Nature 339:142-144. Pickett-Heaps JD, Marchant H (1972) The phylogeny of the green algae: a new proposal. Cytobios 6:255-264. Preston RD (1964) Structural and mechanical aspects of plant cell walls with particular reference to synthesis and growth. In: Zimmermann, MH (ed) Formation of Wood in Forest Trees. Academic Press, New York, p 169-201. Preston RD (1974) The physical biology of plant cell walls. Chapman and Hall, London. Roberts EM, Saxena IM, Brown Jr RM (1989) Biosynthesis of Cellulose II in Acetobacter xylinum. In: Schuerch C (ed) Cell Wall and Wood - Chemistry and Technology. John Wiley and Sons, New York, p 689-704. Roelofsen A (1958) Cell-wall structure as related to surface growth. Acta Bot Neeri 7:77-89. Roife BG, Gresshoff PM (1988) Genetic analysis of legume nodule initiation. Ann Rev Plant Physiol and Plant Mol Biol 39:297-319. Ross P, AloniY, Weinhouse C, Michaeli D, Weinberger-Ohana P, Meyer R, Benziman M (1985) An unusual oligonucleotide regulates cellulose synthesis in Acetobacter xylinum. FEBS Lett 186(2) :191-196. Saxena IM, Brown Jr RM (1989) Cellulose biosynthesis in Acetobacter xylinum; a genetic approach. In: Schuerch C (ed) Cellulose and Wood - Chemistry and Technology. John Wiley and Sons, New York, p 537-557. Schramm M, Hestrin S (1954) Factors affecting production of cellulose at the air/liquid interface of a culture of Acetobacter xylinum. J Gen Microbiol 11:123-129. Sisson W (1938) The existence of mercerized cellulose and its orientation in Halicystis as indicated by x-ray diffraction analysis. Science 87:350-351. Stewart KD, Mattox KR (1978) Structural evolution in the flagellated cells of green algae and land plants. Biosystems 10:145-152. Stewart KD, Mattox KR (1982) Phylogeny of phytoflagellates. in Rosowski JR, and Parker BC (ed) Selected Papers in Phycology It. Phycological Soc Amer, Lawrence, Kan p 626-640. Wardrop AB (1970) The structure and formation of the test of Pyura stolonifera (Tunicata). Protoplasma 70:73-86. Woese CR (1987) Bacterial evolution. Microbiol Reviews 51(2) :221-271. Yang D, Oyaizu Y, Oyaizu H, Olsen GJ, Woese CR (1985) Mitochondrial origins. Proc Natl Acad Sci USA 82:4443-4447. The above material taken from: Experimental Phycology Cell Walls and Surfaces Reproduction, Photosynthesis Edited by W. Wiessner, D. G. Robinson and R. C. Starr With 91 Figures 1990 Springer-Verlag Berlin Heidelberg NewYorl London Paris Tokyo Hong Kong Barcelona Professor Dr. WOLFGANG WIESSNER Professor DAVID G. ROBINSON Pflanzenphysiologisches Institut der Universitat Untere Karspiile 2 3400 Gottingen, FRG Professor RICHARD C. STARR, Ph. D. The University of Texas at Austin Austin, TX 78712, USA ISBN 3-540-52496-7 Springer-Verlag Berlin Heidelberg New York ISBN 0-387-52496-7 Springer-Verlag New York Berlin Heidelberg
|
