دورية أكاديمية

Ultrastructure of the extraordinary pedal gland in Asplanchna aff. herricki (Rotifera: Monogononta).

التفاصيل البيبلوغرافية
العنوان: Ultrastructure of the extraordinary pedal gland in Asplanchna aff. herricki (Rotifera: Monogononta).
المؤلفون: Hochberg R; Department of Biology, University of Massachusetts Lowell, Lowell, Massachusetts, USA., Wallace RL; Department of Biology, Ripon College, Ripon, Wisconsin, USA., Walsh EJ; Department of Biological Sciences, University of Texas at El Paso, El Paso, Texas, USA., Araújo TQ; Department of Biology, University of Massachusetts Lowell, Lowell, Massachusetts, USA.
المصدر: Journal of morphology [J Morphol] 2024 Sep; Vol. 285 (9), pp. e21765.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Wiley Country of Publication: United States NLM ID: 0406125 Publication Model: Print Cited Medium: Internet ISSN: 1097-4687 (Electronic) Linking ISSN: 00222887 NLM ISO Abbreviation: J Morphol Subsets: MEDLINE
أسماء مطبوعة: Publication: <2005- > : Hoboken, N.J. : Wiley
Original Publication: 1931- : Philadelphia, Pa. : Wistar Institute of Anatomy and Biology
مواضيع طبية MeSH: Rotifera*/ultrastructure , Rotifera*/anatomy & histology, Animals ; Exocrine Glands/ultrastructure ; Exocrine Glands/anatomy & histology ; Secretory Vesicles/ultrastructure ; Golgi Apparatus/ultrastructure ; Microscopy, Electron, Transmission
مستخلص: Rotifers possess complex morphologies despite their microscopic size and simple appearance. Part of this complexity is hidden in the structure of their organs, which may be cellular or syncytial. Surprisingly, organs that are cellular in one taxon can be syncytial in another. Pedal glands are widespread across Rotifera and function in substrate attachment and/or egg brooding. These glands are normally absent in Asplanchna, which lack feet and toes that function as outlets for pedal glandular secretions in other rotifers. Here, we describe the ultrastructure of a pedal gland that is singular and syncytial in Asplanchna aff. herricki, but is normally paired and cellular in all other rotifers. Asplanchna aff. herricki has a single large pedal gland that is active and secretory; it has a bipartite, binucleate, syncytial body and a cytosol filled with rough endoplasmic reticulum, Golgi, and several types of secretory vesicles. The most abundant vesicle type is large and contains a spherical electron-dense secretion that appears to be produced through homotypic fusion of condensing vesicles produced by the Golgi. The vesicles appear to undergo a phase transition from condensed to decondensed along their pathway toward the gland lumen. Decondensation changes the contents to a mucin-like matrix that is eventually exocytosed in a "kiss-and-run" fashion with the plasma membrane of the gland lumen. Exocytosed mucus enters the gland lumen and exits through an epithelial duct that is an extension of the syncytial integument. This results in mucus that extends from the rotifer as a long string as the animal swims through the water. The function of this mucus is unknown, but we speculate it may function in temporary attachment, prey capture, or floatation.
(© 2024 The Author(s). Journal of Morphology published by Wiley Periodicals LLC.)
References: Balazs, E., Galik‐Olah, Z., Galik, B., Somogyvari, F., Kalman, J., & Datki, Z. (2021). External modulation of Rotimer exudate secretion in monogonant rotifers. Ecotoxicology and Environmental Safety, 220, 112399. https://doi.org/10.1016/j.ecoenv.2021.112399.
Bentfeld, M. E. (1971). Studies of oogenesis in the rotifer, Asplanchna. II. Oocyte growth and development. Zeitschrift fur Zellforschung und mikroskopische Anatomie, 115, 184–195.
Brown, D. (1989). Membrane recycling and epithelial cell function. American Journal of Physiology‐Renal Physiology, 256(1), F1–F12.
Burgess, T. L., & Kelly, R. B. (1987). Constitutive and regulated secretion of proteins. Annual Review of Cell Biology, 3(1), 243–293.
Chin, W. C., Orellana, M. V., Quesada, I., & Verdugo, P. (2004). Secretion in unicellular marine phytoplankton: Demonstration of regulated exocytosis in Phaeocystis globosa. Plant and Cell Physiology, 45(5), 535–542.
van Cleave, H. J. (1932). Eutely or cell constancy in its relation to body size. The Quarterly Review of Biology, 7(1), 59–67.
Clément, P., & Wurdak, E. (1991). Rotifera. In F. W. Harrison & E. E. Ruppert (Eds.), Microscopic anatomy of invertebrates, Volume 4: Aschelminthes (pp. 219–297). Wiley‐Liss Inc.
Datki, Z., Acs, E., Balazs, E., Sovany, T., Csoka, I., Zsuga, K., Kalman, J., & Galik‐Olah, Z. (2021). Exogenic production of bioactive filamentous biopolymer by monogonant rotifers. Ecotoxicology and Environmental Safety, 208, 111666.
Datki, Z., Balazs, E., Galik, B., Sinka, R., Zeitler, L., Bozso, Z., Kalman, J., Hortobagyi, T., & Galik‐Olah, Z. (2022a). The interacting rotifer‐biopolymers are anti‐and disaggregating agents for human‐type beta‐amyloid in vitro. International Journal of Biological Macromolecules, 201, 262–269.
Datki, Z., Darula, Z., Vedelek, V., Hunyadi‐Gulyas, E., Dingmann, B. J., Vedelek, B., Kalman, J., Urban, P., Gyenesei, A., Galik‐Olah, Z., Galik, B., & Sinka, R. (2023). Biofilm formation initiating rotifer‐specific biopolymer and its predicted components. International Journal of Biological Macromolecules, 253, 127157. https://doi.org/10.1016/j.ijbiomac.2023.127157.
Datki, Z., Sinka, R., Galik, B., & Galik‐Olah, Z. (2022b). Particle‐dependent reproduction and exogenic biopolymer secretion of protozoa co‐cultured rotifers. International Journal of Biological Macromolecules, 211, 669–677.
Davies, N., Lafleur, A., Hochberg, R., Walsh, E. J., & Wallace, R. L. (2024). Key to sessile gnesiotrochan rotifers: Families, monospecific species in Flosculariidae, species of Atrochidae, Conochilidae, and Limnias. Zootaxa, 5397, 497–520. https://doi.org/10.11646/zootaxa.5397.4.3.
Dickson, M. R., & Mercer, E. H. (1966). Fine structure of the pedal gland of Philodina roseola (Rotifera). Journal of Microscopy (Paris), 5, 81–90.
Ejsmont‐Karabin, J. (2023). Rotifers of Lake Psammon: A knowledge synthesis. Hydrobiologia, 851, 2949–2964.
Fontaneto, D., & De Smet, W. E. (2014). Rotifera. In W. Kükenthal (Ed.), Gastrotricha and Gnathifera (pp. 217–300). Walter de Gruyter GmbH & Co KG.
Gilbert, J. J. (1983). Rotifera. In K. G. Adiyodi & R. G. Adiyodi (Eds.), Reproductive biology of invertebrates. Volume I. Oogenesis, oviposition, and oosorption (pp. 181–209). John Wiley and Sons.
Gilbert, J. J. (1988). Rotifera. In K. G. Adiyodi & R. G. Adiyodi (Eds.), Reproductive biology of invertebrates. Volume III. Accessory sex glands (pp. 73–80). Oxford and IBH Publishing Co.
Gilbert, J. J. (1989). Rotifera. In K. G. Adiyodi & R. G. Adiyodi (Eds.), Reproductive biology of invertebrates. Volume IV, Part A. Fertilization, development, and parental care (pp. 179–199). Oxford and IBH Publishing Co.
Goldberg, W. M. (2018). Coral food, feeding, nutrition, and secretion: A review. In M. Kloc & J. Z. Zubiak (Eds.), Marine organisms as model systems in biology and medicine (pp. 377–421).
de Guerne, M. J. (1888). IV.—Monographic note on the Rotifera of the family Asplanchnidæ. Annals and Magazine of Natural History, 2(7), 28–40.
Hampton, S. E., & Gilbert, J. J. (2001). Observations of insect predation on rotifers. Hydrobiologia, 446/447, 115–121.
Hampton, S. E., Gilbert, J. J., & Burns, C. W. (2000). Direct and indirect effects of juvenile Buenoa macrotibialis (Hemiptera: Notonectidae) on the zooplankton of a shallow pond. Limnology and Oceanography, 45, 1006–1012.
Hardy, C. R., & Linder, H. P. (2005). Intraspecific variability and timing in ancestral ecology reconstruction: A test case from the Cape flora. Systematic Biology, 54(2), 299–316.
Hickernell, L. M. (1917). A study of desiccation in the rotifer, Philodina roseola, with special reference to cytological changes accompanying desiccation. The Biological Bulletin, 32(6), 343–406.
Hochberg, R., Araújo, T. Q., Walsh, E. J., Mohl, J. E., & Wallace, R. L. (2023). Fine structure of the retrocerebral organ in the rotifer Trichocerca similis (Monogononta). Invertebrate Biology, 142(1), e12396.
Houy, S., Croisé, P., Gubar, O., Chasserot‐Golaz, S., Tryoen‐Tóth, P., Ory, S., & Gasman, S. (2013). Exocytosis and endocytosis in neuroendocrine cells: Inseparable membranes!. Frontiers in Endocrinology, 4, 62255.
Hyman, L. H. (1951). The invertebrates: Acanthocephala, Aschelminthes, and Entoprocta. In E. J. Boell (Ed.), The pseudocoelomate Bilateria (pp. vii+–573). McGraw-Hill.
Jørgensen, C., Kørboe, T., Møhlenberg, F., & Riisgård, H. (1984). Ciliary and mucus‐net filter feeding, with special reference to fluid mechanical characteristics. Marine Ecology Progress Series, 15(3), 283–292.
Kappner, I., Al‐Moghrabi, S., & Richter, C. (2000). Mucus‐net feeding by the vermetid gastropod Dendropoma maxima in coral reefs. Marine Ecology Progress Series, 204, 309–313.
Kiφrboe, T., & Titelman, J. (1998). Feeding, prey selection and prey encounter mechanisms in the heterotrophic dinoflagellate Noctiluca scintillans. Journal of Plankton Research, 20(8), 1615–1636.
Koste, W. (1978). Rotatoria. Die Radertiere Mittel‐Europas, 2nd ed. Gebruder Borntraeger, Berlin and Stuttgart. V. 1, text, 673 p.; V. 2, plates, 476.
Meldolesi, J., & Ceccarelli, B. (1981). Exocytosis and membrane recycling. Philosophical Transactions of the Royal Society of London. B, Biological Sciences, 296(1080), 55–65.
Mellman, I., Fuchs, R., & Helenius, A. (1986). Acidification of the endocytic and exocytic pathways. Annual Review of Biochemistry, 55(1), 663–700.
Montgomery, Jr., T. H. (1903). On the morphology of the rotatorian family Flosculariidae. Proceedings of the Academy of Natural Sciences of Philadelphia, 55, 363–395.
Nance, J. M., & Braithwaite, L. F. (1979). The function of mucous secretions in the cushion star Pteraster tesselatus Ives. Journal of Experimental Marine Biology and Ecology, 40(3), 259–266.
Nozais, C., Duchêne, J. C., & Bhaud, M. (1997). Control of position in the water column by the larvae of Poecilochaetus serpens (Polychaeta): The importance of mucus secretion. Journal of Experimental Marine Biology and Ecology, 210(1), 91–106.
Obertegger, U., & Wallace, R. L. (2023). Trait‐based research on Rotifera: The holy grail or just messy. Water, 15(8), 1459.
de Paggi, S. B. J. (2002). Family Asplanchnidae Eckstein, 1883. Rotifera. Vol. 6: Asplanchnidae, Gastropodidae, Lindiidae, Microcodidae, Synchaetidae, Trochosphaeridae and Filinia. In H. J. Dumont (Ed.), Guides to the Identification of the Microinvertebrates of the Continental Waters of the World (Vol. 18, pp. 1–27). Backhuys.
de Paggi, S. B. J., Wallace, R., Fontaneto, D., & Marinone, M. C. (2020). Phylum Rotifera. In C. Damborenea, D. C. Rogers, & J. H. Thorp (Eds.), Thorp and Covich's freshwater invertebrates (pp. 145–200). Academic Press.
Pavelka, M., & Roth, J. (2015). Functional ultrastructure: Atlas of tissue biology and pathology. Springer. https://doi.org/10.1007/978-3-7091-1830-6.
Petersen, J. K. (2007). Ascidian suspension feeding. Journal of Experimental Marine Biology and Ecology, 342(1), 127–137.
Remane, A. (1933). Rotatoria (4. Lieferung). In H.G. Bronn (Ed.), H.G. Bronn's Klassen und Ordnungen des Tier‐Reichs. Vierter Band: Vermes. II. Abteilung: Aschelminthen. I. Buch: Rotatorien, Gastrotrichen und Kinorhynchen (pp. 452–576). Akademische Verlagsgesellschaft.
Rutter, G. A., & Tsuboi, T. (2004). Kiss and run exocytosis of dense core secretory vesicles. Neuroreport, 15(1), 79–81.
Shiel, R. J., & Koste, W. (1993). Rotifera from Australia inland waters. IX. Gastropodidae, Synchaetidae, Asplanchnidae (Rotifera: Monogononta). Transactions of the Royal Society of Australia, 117(3), 111–139.
Snell, T. W. (1998). Chemical ecology of rotifers. Hydrobiologia, 387, 267–276.
Sørensen, M. V., & Giribet, G. (2006). A modern approach to rotiferan phylogeny: combining morphological and molecular data. Molecular Phylogenetics and Evolution, 40(2), 585–608.
Sudzuki, M. (1955). Life history of some Japanese Rotifers I. Science Reports of the Tokyo Daigaku Dai, 118, 41–63.
Sudzuki, M. (1957a). Studies on the egg‐carrying types in Rotifera. II. Genera Brachionus and Keratella. Zoological Magazine, Tokyo, 66, 11–20.
Sudzuki, M. (1957b). Studies on the egg‐carrying types in Rotifera III. Genus Anuraeopsis Japan., engl. summ. Zoological Magazine, Tokyo, 66, 407–415.
Vasilikopoulos, A., Herlyn, H., Fontaneto, D., Wilson, C. G., Nowell, R. W., Flot, J. F., Barraclough, T. G., & Van Doninck, K. (2024). Whole‐genome analyses converge to support the Hemirotifera hypothesis within Syndermata (Gnathifera). Hydrobiologia, 851(12), 2795–2826.
Verdugo, P. (2005). Polymer gel phase transition in condensation‐decondensation of secretory products. Advances in Polymer Science, 110, 145–156.
Walsh, E. J. (1989). Oviposition behavior of the littoral rotifer Euchlanis dilatata. Hydrobiologia, 186–187, 157–161.
Walsh, E. J., Wallace, R. L., & Shiel, R. J. (2005). Toward a better understanding of the phylogeny of the Asplanchnidae (Rotifera). Hydrobiologia, 546, 71–80.
Wierzejski, A. (1893). Rotatoria (wrotki) Galicyi. Nakładem Akademii Umiejetności. Sklad Glôwny W Ksiegarnu Spólki Wydawniczej Polskiej.
Wurdak, E. S. (1987). Ultrastructure and histochemistry, of the stomach of Asplanchna sieboldi. Hydrobiologia, 147, 361–371.
Wurdak, E. (2017). External morphology of the eggs of Asplanchnopus multiceps (Schrank, 1793) (Rotifera): Solving the 150‐year‐old case of mistaken identity. Hydrobiologia, 796, 161–168.
Yang, H., & Hochberg, R. (2018a). Ultrastructural and elemental characterization of the extracorporeal tube of the sessile rotifer Floscularia conifera (Rotifera: Gnesiotrocha). Invertebrate Biology, 137(4), 319–328.
Yang, H., & Hochberg, R. (2018b). Ultrastructure of the extracorporeal tube and “cement glands” in the sessile rotifer Limnias melicerta (Rotifera: Gnesiotrocha). Zoomorphology, 137(1), 1–12.
Yang, H., Hochberg, R., Walsh, E. J., & Wallace, R. L. (2021). Ultrastructure of extracorporeal secretions of four sessile species of Rotifera (Gnesiotrocha), with observations on the chemistry of the gelatinous tube. Invertebrate Biology, 140(2), e12318.
Štrojsová, M., & Vrba, J. (2007). Rotifer digestive enzymes: Direct detection using the ELF technique. Hydrobiologia, 593, 159–165.
معلومات مُعتمدة: DEB 2051684 National Science Foundation; DEB 2051704 National Science Foundation; DEB 2051710 National Science Foundation
فهرسة مساهمة: Keywords: exocrine; mucus; secretion; zooplankton
تواريخ الأحداث: Date Created: 20240817 Date Completed: 20240817 Latest Revision: 20240817
رمز التحديث: 20240818
DOI: 10.1002/jmor.21765
PMID: 39152664
قاعدة البيانات: MEDLINE
الوصف
تدمد:1097-4687
DOI:10.1002/jmor.21765