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Observations on the Developmental Morphology and Fine Structure of Pit Connections in Red Algae Introduction Pits

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Observations on the Developmental Morphology and Fine Structure of Pit Connections in Red Algae Introduction Pits Cytologia 37: 759-768, 1972 Observations on the Developmental Morphology and Fine Structure of Pit Connections in Red Algae Eva Konrad Hawkins1 Fairleigh Dickinson University, Rutherford, New Jersey, U. S. A. Received July 22, 1971 Introduction Pits (thin spots) with conspicuous pit connections have been observed since the last century (Klein 1877, early descriptions are reviewed by Falkenberg 1901) in cell walls of red algae. Pit connections are formed between daughter cells of a division (primary pit connections) and between cells that have remained in contact or achieved new contact during development (secondary pit connections). The structure and possible function of pit connections of red algae have been subjects of considerable speculation and controversy. One group of phycologists (Schmitz 1883, Falkenberg 1901, Kohl 1902, Miranda 1930) has held that openings between cells of red algae are plugged by a perforated membrane which, in turn, is bordered by dense plates on both sides. Slender protoplasmic filaments, con necting adjacent protoplasts, would traverse this membrane. Another group (Ambronn 1880, Archer 1876, Kienitz-Gerloff 1902) opposed this conclusion and described the "membrane" as homogeneous. Mangenot (1924) found special cytoplasmic differentiations, "plasmodesms," without any pit closing membrane between adjacent cells of red algae. He viewed these as "synapses" and suggested that they function as sites of an intercellular exchange of nutrients and transmission of stimuli in red algae. Jungers (1933) classified "synapses" into the following types: 1) a densely staining lens-shaped body, set in the central orifice of the crosswall, found in Cera mium and Griffithsia: 2) two densely staining discs separated by a fine membrane, found in Polysiphonia and Delesseria. He did not think "synapses" have a "proto plasmic content" and did not accept their role in "protoplasmic communications." Though this classification was questioned (Muldorf 1937), the structure of pit connections was not clarified (Kylin 1940). Early phycologists postulated the significance of pit connections in the phy logeny and taxonomy of red algae. However, the resolution of the light microscope severely limited their studies. Light microscopy could not assess the evolutionary (Denison and Caroll 1966) or taxonomic (Dixon 1963) significance of this structure. Knowledge of the fine structure of pit connections may assist not only in classification or in advancing theories of phylogenetic importance. Several para sitic algae establish cytoplasmic contact with cells of their photosynthetic host re 1 Present address: Department of Biology, University of Pennsylvania, Philadelphia, Pa. 19104, U. S. A. 760 E. K. Hawkins Cytologia 37 lative by the formation of pit connections (Martin and Pocock 1953). Phototropic orientations of branches of various red algae to unilateral illuminations are known (Berthold 1882). What regulates these orientations at the cellular level is not under stood. Secondary pit connections are significant in anastomoses of neighboring branches. The highly regular net-like form of some members of the Delesseriaceae is maintained by primary and secondary pit connections (Papenfuss 1937). Through these secondary contacts and reinforcements additional meshes are formed and the gross morphology of entire organisms is altered. Fusion between lateral branches to form a reticulate system of interconnecting cells may be observed in a number of red algal genera (Halodictyon, Haloplegma, Rhododictyon, etc.). In view of the multiple significance of pit connections in the biology of red algae and the insufficient knowledge available to us on their developmental mor phology and fine structure (Myers et al. 1959, Bouck 1962, Peyriere 1963, Bishoff 1965, Bisalputra et al. 1967, Ramus 1969) this study was undertaken to clarify further their structure. Materials and methods Ceramium diaphanum and Polysiphonia sp. were collected below low tide level from rocks at Sayville, L. I. and Sea Gate, Coney Island. Callithamnion roseum was obtained from unialgal cultures (Konrad Hawkins 1968). Apical parts (approx. 1cm long) were fixed in Karnovsky's fixative (1965) for 3 hours. Cal lithamnion and Ceramium were postfixed in 1% sodium cacodylate buffered osmium tetroxide at pH 7.5 for 1hr. Polysiphonia was postfixed in 2% sodium cacodylate buffered osmium tetroxide at pH 8 for 3 hrs. They were embedded in agar prior to dehydration. Dehydration was carried out at 0-4•Ž in a graded series of acetone/water mixtures. Final embedding was in Epon 812; sections were cut with a diamond knife and stained with uranyl acetate and lead citrate (Venable and Coggeshall 1965). Micrographs were made with and RCA EMU-3H electron microscope. Observations Primary pit connections of varying morphology were found between cortical , segment and axial cells of Ceramium diaphanum. Some suggest biconvex discs , constricted along their equator (Figs. 1-10). Their diameter is 0.3-0.7ƒÊ at the plane of constriction. A triple-layered membrane (Figs. 1, 2), 80-100A thick, surrounds equatorial furrows facing cell walls. Its relationship to the plasma membrane (Figs. 7, 8) could not be ascertained, since the latter has not been clearly preserved. The lateral limiting membrane is in contact with microfibrils of the cell wall (Fig. 2). Convex surfaces stain intensely to a depth of 30-50mƒÊ. Staining intensity gradually decreases at both surfaces to a depth of 100mƒÊ. Beyond these electron dense regions numerous fibrous thread-like formations traverse the youngest connections (Fig. 7). 1972 Observations on the Developmental Morphology and Fine Structure of Pit 761 Figs. 1-6. Pit connections between cortical cells of Ceramium diaphanum. 1-2, serial longi tudinal sections. Height-to-width ratios of the pit connections indicate a cut near the median in Fig. 1, submedian in Fig. 2. Note attachment of branched microfibrils (mf) of the cell wall (cw) to limiting membrane (lm). 3, longitudinal lateral section through the equatorial furrow. The pit connection appears as two separated discs. 4, oblique lateral section. 5, oblique tangential section. -Microfibrils (mf) of the cell wall show a circular orientation around the equator. 6, near cross section, through equatorial furrow. Scales, 500mƒÊ. 762 E. K. Hawkins Cytologia 37 An attempt was made to correlate occurrence of the biconvex constricted form (Figs. 1-6) with developmental conditions of the linked cells. Dense and vacuolated cells of varying sizes compose the cortex of Ceramium. They are formed by intercalary cell divisions. Biconvex, constricted pit connections were found between cortical cells where one or both of the linked members was intensely Figs. 7-10. Longitudinal sections of pit connections between segment cells of an apex of Ceramium diaphanum. 7, near median section between second and third segment cell. Fibrous thread-like structures (f) are parallel to the longitudinal axis of the expanding thallus. Plasma membranes (pm) are not clearly enough defined to allow conclusions about their relation to lateral membranes. 8, longitudinal section between fifth and sixth segment cell. 9, longitudinal lateral section between sixth and seventh segment cell. Note five-layered appearance of adjacent lateral membranes (arrows) near the innermost edge of the equatorial furrow. 10, oblique lateral section between third and fourth segment cell. Scales, 500mƒÊ. stained and nonvacuolated. This indicated a recent cell division and a newly formed pit connection between daughter cells. Segment cells of Ceramium originate by continuous divisions of dome-shaped apical cells. As their distance from the tip increases, they enlarge into axial cells 1972 Observations on the Developmental Morphology and Fine Structure of Pit 763 surrounded by nodal cortication. Successive segment cells of an apex represent successive developmental stages of one segment cell. Similarly, one may visualize successive pit connections of a single apex as representative stages in the develop ment of one pit connection, with youngest forms occurring nearest to the tip. Pit connections (Figs. 7-10) between segment cells of an apex show similar morphology to those (Figs. 1-6) which contact at least one small nonvacuolated cortical cell of basal regions. This suggests that biconvex, constricted forms re present early developmental stages of pit connections. Morphological similarities to young pit connections of Ceramium diaphanum (Figs. 1-10) were observed also in apices of Callithamnion roseum and Polysiphonia sp. (Fig. 15). Figs. 11-14. Longitudinal section of pit connections of Ceramium diaphanum. 11, flattened, lens-shaped form between vacuolated cortical cells. Scale 500mƒÊ. 12, pit connection between axial cells was pulled apart during its preparation for electron microscopy. Note empty, electron transparent space between densely stained opposite halves of the dics. Scale, 1ƒÊ. 13, pit connections between vacuolated axial cells. Scale 10ƒÊ. 14, pit connection of Fig. 13 magnified. Scale, 1ƒÊ. The proportions of biconvex forms change during growth. Alterations in proportions are brought about by a disproportionate increase in width of the connections with respect to: 1) depth of the equatorial furrows, 2) height of the connections. Equatorial furrows may not change in depth or may even disappear during growth of the pit connections; yet the connections may increase 5-10 fold in width during development. Decreased height-to-width ratios of pit connections (diam>1ƒÊ)
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