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Regulation of Ciliary Pattern in Dileptus (Ciliata). I. Sensory Cilia and Their Conversion Into Locomotor Cilia

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Regulation of Ciliary Pattern in Dileptus (Ciliata). I. Sensory Cilia and Their Conversion Into Locomotor Cilia /. Embryol exp. Morph. Vol. 68, pp. 99-114, 1982 99 Printed in Great Britain © Company of Biologists Limited 1982 Regulation of ciliary pattern in Dileptus (Ciliata). I. Sensory cilia and their conversion into locomotor cilia By KRYSTYNA GOLINSKA1 From the Nencki Institute of Experimental Biology, Department of Cell Biology, Warsaw SUMMARY The surface of Dileptus contains three different regions: locomotor, oral and sensory. Each region has cilia with a specific structure and arranged in a characteristic pattern. In the morphogenetic situation when a sensory region transforms into a locomotor one, sensory cilia undergo structural changes converting them into locomotor cilia. The evidence for this is that cilia are found in the transforming region with an inner microtubular pattern inter- mediate between that of sensory and locomotor cilia. There are also changes in distribution of sensory units leading to a pattern characteristic of locomotor cilia. The conversion of sensory cilia into locomotor ones is also confirmed by a complete lack of evidence for resorption of sensory units within the transforming region, although the resorption is usually very easily observed with the transmission electron microscope. Transformation lasts about 5 h after the operation; afterwards locomotor cilia of normal appearance occupy the trans- formed region. This way of regulation of ciliary pattern has not been previously described. Its most surprising feature is the regulation of inner structure in an already differentiated ciliary unit. Some aspects of mechanisms which could control this kind of pattern regulation,! are discussed. INTRODUCTION The surface of a ciliate cell is usually subdivided into several cortical territories where ciliary structures have an organization characteristic of the region. During post-traumatic regeneration the lost regions form anew, while the intact regions (in morphallactically regenerating ciliates) diminish in size, and the resulting organism is a perfectly proportioned miniature (Jerka-Dziadosz, 1976; Golinska & Kink, 1977; Golinska, 1979; Bakowska & Jerka-Dziadosz, 1980). Ciliary pattern on regenerating fragments is adjusted through precisely localized proliferation and resorption of ciliary units (Jerka-Dziadosz & Golinska 1977). The ciliature of Dileptus, according to morphological criteria, falls into three categories: oral, locomotor, and sensory cilia. Cilia of each kind occupy a separate region on the cell, and are organized in a specific pattern. During 1 Author's address: Nencki Institute of Experimental Biology, Department of Cell Biology, Warsaw 02-093, Poland. 100 K. GOLINSKA post-traumatic regeneration ciliature of each kind seems to regulate in its specific way. The oral ciliature in Dileptus is regulated through proliferations and resorptions of ciliary units that occur only within special areas of prolifera- tion and resorption localized at the both ends of an elongated oral structure (Golinska & Kink, 1976, 1977; Kink, 1976). Locomotor ciliature is regulated through proliferations and resorptions which are not restricted to any localized areas, but rather reflect the changes of the shape of cell. Resorptions are found mostly on the narrowing regions of the cell, whilst proliferations are numerous on the widening or elongating parts (Golinska & Kink, 1977). In most cases, oral or locomotor cilia undergo resorption when present on those parts of cortex that are transformed into another cortical region. The pattern of sensory cilia can probably also be regulated through resorption and/or proliferation of its ciliary units. According to the present observations, however, sensory cilia when present on a territory changing into a region of locomotor cilia undergo internal restructuring leading to transformation of sensory cilia into locomotor ones. This represents the case of transdetermination occurring within organelles. Usually, in ciliates as well as in metazoans, the switch in differentiation is possible only before the structure is fully developed. A well-known example is the formation of a complete mouth out of a fragment of early oral primordia in Stentor (Tartar 1957). In the case described here a differentiated organellum (sensory cilium) undergoes an additional formation of some structural elements and dedifferentiation of the others, becoming the unit of another ciliary pattern. Some implications of this mode of pattern regulation upon the nature of control mechanisms are discussed. MATERIALS AND METHODS Cultures of Dileptus anser were maintained as described elsewhere (Golinska & Jerka-Dziadosz, 1973). All observations were performed on anterior cellular processes, the so-called probosces. The probosces were isolated from the trunks of cells by transections made by hand, using a microknife. Level of transection was slightly above the base of proboscis, because in such fragments rows of sensory cilia reach the posterior pole of the cell, and this was essential for interpretation of some of the results. To obtain a quantity of viable fragments, some portion of endoplasm from trunk was pushed into probosces before transection. This method was successfully utilized in previous study (Golinska, 1979). For observations, samples of 20-50 fragments were prepared, and then fixed at definite times after the end of the operations. Light-microscopic observations were done on the material stained with protargol, using slightly modified method of Dragesco (1962). Cells were fixed with freshly prepared mixture of 1 part OsO4 (4 %), 1 part of glutaraldehyde (6 %), 1 part of cacodylate buffer 0-1 M, pH 6-5 (HC1), during 15 min. Fixed cells Sensory cilia and their conversion into locomotor cilia 101 were then transferred onto microscope slides and covered with albumin. The preparations were hardened in 1:1 mixture of HC1 20 % and ethanol 95 °C, for about 1 h, then washed in 95 °C ethanol and allowed to dry. Further procedures, from potassium permanganate treatment onwards, followed the procedure of Dragesco (1962). Electron-microscope observations were performed using standard preparative methods, except for fixation. The fixative used was a mixture similar to that described for light-microscope preparations, but cacodylate buffer (0-1 M) was pH 7-2, and time of fixation 30 min. Thin sections were then stained with uranyl acetate followed by lead citrate. The sections were examined in a JEM 100B transmission electron microscope. RESULTS Ciliary pattern of Dileptus The cell of Dileptus is elongated, at the anterior end of its trunk there are cytostomal structures and a slender process the so-called proboscis (Fig. 1). The body is covered with cilia of three kinds: oral, locomotor and sensory ones. The oral ciliature of Dileptus is situated around the cytostome and on the ventral side of proboscis. Locomotor cilia occupy the whole surface of the trunk and the left and right sides of the basal portion of probsocis. Sensory cilia are localized along the whole length of the dorsal side of proboscis (Fig, 1). Studies on the fine structure of oral ciliature revealed its complexity (Grain & Golinska, 1969). The most characteristic element of oral ciliature of Dileptus is a non-ciliated kinetosome with nematodesma (Fig. 2) - a kind of ciliary rootlet which accompany only the oral ciliature. Locomotor cilia have ciliary shafts of typical structure. Accessory fibres at the proximal level of kinetosome, namely transverse, postciliary, and kineto- desmal fibre, are also similar to those found in other ciliates (Golinska & Kink, 1976). The root fibre is of a kind found in dileptuses only: it is built up of several, usually five, microtubules directed toward the anterior pole of the cell (Fig. 3). The microtubules form a loose bundle, and near to kinetosomes; the short and striated microfilamentous component of this fibre can also be seen. Locomotor cilia are arranged in a similar pattern on the trunk and on the basal portion of proboscis. There are longitudinal rows of single ciliary Units (Fig. 5) uniformly scattered within a row. The number of rows and the number of ciliary units within a row vary considerably. Sensory cilia of Dileptus are situated in prolongation to three, four or five rows of dorsal locomotor cilia. The sensory cilia are grouped in pairs and arranged in longitudinal rows (Fig. 4). The distance in between the sensory pairs lengthens toward the top of proboscis. The sensory cilium differs from locomotor cilium in the fine structure of ciliary shaft, and of the root fibre. Kinetosomes of both organelles are Very 102 K. GOLINSKA • Oral cilia Proboscis \ - Sensory cilia Level of Cytostome transection " -Locomotor cilia Trunk < Fig. 1. Side view of ciliary regions in Dileptus. Fig. 2. Non-ciliated oral kinetosomes bearing nematodesmata («). x 33000. Bar = 0-5 /im. Fig. 3. Kinetosome and rootlet of locomotor cilium. (m.t.), microtubular, and (m./.) microfilamentous component of the root fibre (often of a striated appearance), x 50500. Bar = 0-5 fim. Fig. 4. Pattern of sensory cilia. There are three rows of double-kinetosomal sensory units on the dorsal side of proboscis (left side of the photograph). On the right side of the photograph infraciliary oral structures are visible. Protargol preparation, x 4500. Bar = 5 /an. Fig. 5. Pattern of locomotor cilia. Kinetosomes indicated by arrows, black spheres are nuclei. Protargol preparation, x 5500. Bar = 5 /im. Fig. 6. Sensory (s.c.) and oral (o.c.) cilia on the distal part of proboscis. Differences in length between the cilia of two kinds are clearly
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