Fottea 10(2): 251-266, 2010 | DOI: 10.5507/fot.2010.016

Heterothallic and homothallic sexual reproduction in Tabularia fasciculata (Bacillariophyta).

Nickolai A. Davidovich1,*, Irena Kaczmarska2, James M. Ehrman3
1 Karadag Natural Reserve of the National Academy of Sciences, Feodosiya, 98187, Ukraine
2 Department of Biology, Mount Allison University, Sackville, New Brunswick, E4L 1G7, Canada
3 Digital Microscopy Facility, Mount Allison University, Sackville, New Brunswick, E4L 1G7, Canada

Sexual behaviour, pattern of auxosporulation, and breeding system of the araphid diatom Tabularia fasciculata were studied using 64 clones derived from two natural populations from the Canadian Atlantic seashore and the Black Sea. Both inter- and intraclonal reproductions were observed. Heterothallic reproduction was morphologically and behaviourally heterogamous. The heterothallic nature of sexual reproduction in this species allowed the determination of sex ratio in the population, which was 1:1 male:female. A novel type of active movement of gametes designated as male was described and pathways traced and recorded. A few male clones could reproduce intraclonally, but this was not abundant compared to interclonal reproduction. The advantages and inferred significance of each mode of reproduction are discussed. In the semi-natural population of T. fasciculata, two size classes were detected among sexualized individuals, and they gave rise to two size groups of initial cells. Sexual compatibility of all derived clones was independent of cell size class. In cultures, the apical length of initial cells was also strongly correlated to the size of parental gametangia. Cell sizes corresponding to cardinal points in the life cycle were established. Interbreeding of clones derived from the Canadian Atlantic and the Black Sea suggests a pan-Atlantic reproductive compatibility of populations of diatoms conforming to current morphological delineation of T. fasciculata.

Keywords: breeding system, diatoms, gamete mobility, life cycle, sexual reproduction, Tabularia fasciculata

Received: February 10, 2010; Accepted: May 19, 2010; Published: September 1, 2010  Show citation

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Davidovich, N.A., Kaczmarska, I., & Ehrman, J.M. (2010). Heterothallic and homothallic sexual reproduction in Tabularia fasciculata (Bacillariophyta). Fottea10(2), 251-266. doi: 10.5507/fot.2010.016
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References

  1. Amato, A., Kooistra, W.H.C.F., Levialdi Ghiron, J.H., Mann, D.G., Pröschold, T. & Montresor, M. (2007): Reproductive isolation among sympatric cryptic species in marine diatoms. - Protist 158: 193-207. Go to original source...
  2. Andersen, R.A., Berges, J.A., Harrison, P.J. & Watanabe, M.M. (2005): Recipes for freshwater and seawater media. In: Andersen, R.A. (ed.): Algal culturing techniques. - pp. 429-538, Elsevier Academic Press. Go to original source...
  3. Archibald, R.E.M. (1983): The diatoms of the Sundays and Great Fish Rivers in the Eastern Cape Province of South Africa. - Bibliotheca Diatomologica, 1. - 362 pp., J.Cramer, Vaduz.
  4. Behnke, A., Friedl, T., Chepurnov, V.A. & Mann, D.G. (2004): Reproductive compatibility and rDNA sequence analyses in the Sellaphora pupula species complex (Bacillariophyta). - Journal of Phycology 40: 193-208. Go to original source...
  5. Chepurnov, V.A. & Mann, D.G. (1997): Variation in the sexual behaviour of natural clones of Achnanthes longipes (Bacillariophyta). - European Journal of Phycology 32: 147-154. Go to original source...
  6. Chepurnov, V.A. & Mann, D.G. (1999): Variation in the sexual behaviour of Achnanthes longipes (Bacillariophyta). II. Inbred monoecious lineages. - European Journal of Phycology 34: 1-11. Go to original source...
  7. Chepurnov, V.A. & Mann, D.G. (2004):Auxosporulation of Licmophora communis (Bacillariophyta) and a review of mating systems and sexual reproduction in araphid pennate diatoms. - Phycological Research 52: 1-12. Go to original source...
  8. Chepurnov, V.A., Mann, D.G., Sabbe, K. & Vyverman, W. (2004): Experimental studies on sexual reproduction in diatoms. - International Review of Cytology 237: 91-154. Go to original source...
  9. Chepurnov, V.A., Mann, D.G., Sabbe, K., Vannerum, K., Casteleyn, G., Verleyen, E., Peperzak, L. & Vyverman, W. (2005): Sexual reproduction, mating system, chloroplast dynamics and abrupt cell size reduction in Pseudo-nitzschia pungens from the North Sea (Bacillariophyta). - European Journal of Phycology 40: 379-395. Go to original source...
  10. Davidovich, N.A. (2001): Species specific sizes and size range of sexual reproduction in diatoms. - In: Economou-Amilli, A. (ed.): Proceedings of the 16th International Diatom Symposium. - pp.191-196, University of Athens, Athens.
  11. Davidovich, N.A. & Bates, S.S. (1998): Sexual reproduction in the pennate diatoms Pseudo- nitzschia multiseries and P. pseudodelicatissima (Bacillariophyceae). - Journal of Phycology 34: 126-137. Go to original source...
  12. Davidovich, N.A., Kaczmarska, I. & Ehrman, J.M. (2006): The sexual structure of a natural population of the diatom Nitzschia longissima (Bréb.) Ralfs - In: Witkowski, A. (ed.): Proceedings of the 18th International Diatom Symposium. - pp. 27-40, Biopress Limited, Bristol.
  13. Edlund, M.B. & Bixby, R.J. (2001): Intra- and inter- specific differences in gametangial and initial cell size in diatoms. In: Economou-Amilli, A. (ed.): Proceedings of the 16th International Diatom Symposium. - pp. 169-190, University of Athens, Athens.
  14. Edlund, M.B. & Stoermer, E.F. (1997): Ecological, evolutionary, and systematic significanсe of diatom life histories. - Journal of Phycology 33: 897-918. Go to original source...
  15. Evans, K.M., Wortley, A.H. & Mann, D.G. (2007): An assessment of potential diatom ''barcode'' genes (cox1, rbcL, 18S and ITS rDNA) and their effectiveness in determining relationships in Sellaphora (Bacillariophyta). - Protist 158: 349-364. Go to original source...
  16. Geitler, L. (1932): Der Formwechsel der pennaten Diatomeen (Kieselalgen). - Archiv für Protistenkunde 78: 1-226.
  17. Geitler, L. (1935): Reproduction and life history in diatoms. - Botanical Review 1: 149-161. Go to original source...
  18. Geitler, L. (1939): Die Auxosporenbildung von Synedra ulna. - Berichte der Deutschen Botanischen Gesellschaft 57: 432-436. Go to original source...
  19. Geitler, L. (1973): Auxosporenbildung und Systematik bei pennaten Diatomeen und die Cytologie von Cocconeis-Sippen. - Österreichische Botanische Zeitschrift 122: 299-321. Go to original source...
  20. Jewson, D.H. (1992): Size reduction, reproductive strategy and the life cycle of a centric diatom. - Philosophical Transaction of the Royal Society of London B. 335: 191-213. Go to original source...
  21. Kaczmarska, I., Davidovich, N.A. & Ehrman, J.M. (2007a): Sex cells and reproduction in the diatom Nitzschia longissima (Bacillariophyta): discovery of siliceous scales in gamete cell walls and novel elements of the perizonium. - Phycologia 46: 726-737. Go to original source...
  22. Kaczmarska, I., Ehrman, J.M., Moniz, M.B.J. & Davidovich, N.A. (2009): Phenotypic and genetic structure of interbreeding populations of the diatom Tabularia fasciculata (Bacillariophyta). - Phycologia 3: 48 (5): 391-403. Go to original source...
  23. Kaczmarska, I., Martin, J.L., LeGresley, M.M. & Ehrman, J. (2005): Diversity of the diatom genus Pseudo-nitzschia Peragallo in the Quoddy Region of the Bay of Fundy, Canada. - Harmful Algae 4: 1-19. Go to original source...
  24. Kaczmarska, I., Reid, C., Martin, J.L. & Moniz, M.B.J. (2008): Morphological, biological, and molecular characteristics of the diatom Pseudo- nitzschia delicatissima from the Canadian Maritimes. - Botany 86: 763-772. Go to original source...
  25. Kaczmarska, I., Reid, C. & Moniz, M. (2007b): Diatom taxonomy: morphology, molecules and barcodes. In: Kusber, W.H. & Jahn, R. (eds.): Proceedings of the 1st Central-European Diatom Meeting. - pp. 69-72, Berlin-Dahlem. Go to original source...
  26. Karsten, G. (1899): Die Diatomeen der Kieler Bucht. - Wissenschaftliche Meeresuntersuchungen (Kiel), new series 4: 17-207.
  27. Kooistra, W.H.C.F., Forlani, G. & De Stefano, M. (2009) Adaptations of araphid pennate diatoms to a planktonic existence. - Marine Ecology 30: 1-15. Go to original source...
  28. Lundholm, N., Moestrup, Ø., Hasle, G.R. & Hoef- Emden, K. (2003): A study of the Pseudo- nitzschia pseudodelicatissima/cuspidata complex (Bacillariophyceae): what is P. pseudodelicatissima? - Journal of Phycology 39: 797-813. Go to original source...
  29. Lundholm, N., Moestrup, Ø., Kotaki, Y., Hoef-Emden, K., Scholin, C. & Miller, P. (2006): Inter- and intraspecific variation of the Pseudo-nitzschia delicatissima complex (Bacillariophyceae) illustrated by rRNA probes, morphological data and phylogenetic analyses. - Journal of Phycology 42: 464-481. Go to original source...
  30. Mann, D.G. (1982): Auxospore formation in Licmophora (Bacillariophyta). - Plant Systematics and Evolution 139: 289-294. Go to original source...
  31. Mann, D.G., Chepurnov, V.A. & Droop, S.J.M. (1999): Sexuality, incompatibility, size variation, and preferential polyandry in natural populations and clones of Sellaphora pupula (Bacillariophyceae). - Journal of Phycology 35: 152-170. Go to original source...
  32. Mann, D.G., Chepurnov, V.A. & Idei, M. (2003): Mating system, sexual reproduction, and auxosporulation in the anomalous raphid diatom Eunotia (Bacillariophyta). - Journal of Phycology 39: 1067-1084. Go to original source...
  33. Manhart, J.R., Fryxell, G.A., Villas, M.C. & Segura, L.Y. (1995): Pseudo-nitzschia pungens and P. multiseries (Bacillariophyceae): nuclear ribosomal DNAs and species differences. -Journal of Phycology 31: 421-427. Go to original source...
  34. Migita, S. (1967): Morphological and ecological studies on sexual reproduction of marine centric diatoms. - Informational Bulletin on Planktology in Japan 14: 13-22. (In Japanese).
  35. Mizuno, M. (1994): Sexual reproduction and auxospore formation in Achnanthes javanica f. subconstricta. - Diatom Research 9: 133-141. Go to original source...
  36. Moniz, M.B.J. & Kaczmarska, I. (2009): Barcoding diatoms: is there a good marker? - Molecular Ecology Resources 9: 1-10. Go to original source...
  37. Morales, E.A. (2003): Fragilaria pennsylvanica, a new diatom (Bacillariophyceae) species from North America, with comments on the taxonomy of the genus Synedra Ehrenberg. - In: Proceedings of the Academy of Natural Sciences of Philadelphia. - 153: 155-166. Go to original source...
  38. Roshchin, A.M. (1973): O haraktere ukrupneniya kletok Coscinodiscus granii Gough. - Biologicheskie nauki 5: 78-81.
  39. Roshchin, A.M. (1987): Diatomovaya vodorosl' s odnodomnym i dvudomnym vosproizvedeniem. - Zhurnal Obshchej Biologii 48: 771-783. Go to original source...
  40. Roshchin, A.M. (1989): Proyavlenie intsukhta u diatomovoj vodorosli Synedra tabulata. - Zhurnal Obshchej Biologii 50: 412-416.
  41. Roshchin, A.M. (1994): Zhiznennye Tsikly Diatomovykh Vodoroslej. - 170 pp., Naukova Dumka, Kiev.
  42. Roshchin, A.M. & Chepurnov, V.A. (1994): Allogamnyj polovoj protsess i gaploidnyj partenogenez u dvudomnoy vodorosli Licmophora ehrenbergii (Kütz.) Grun. (Bacillariophyta). - Algologia 4: 3-10.
  43. Roshchin, A.M. & Chepurnov, V.A. (1999): Dioecy and monoecy in the pennate diatoms (with reference to the centric taxa). - In: Mayama, M., Idei, M., & Koizumi, I. (eds.): Proceedings of the 14th International Diatom Symposium. - pp. 241- 261, Koeltz Scientific Books, Koenigstein.
  44. Round, F.E., Crawford, R.M. & Mann, D.G. (1990): The Diatoms. Biology and morphology of the genera. - 747 pp., Cambridge University Press, Cambridge.
  45. Sarno, D., Kooistra, W.H.C.F., Medlin, L.K., Percopo, I.& Zingone, A. (2005): Diversity in the genus Skeletonema (Bacillariophyceae).II. An assessment of the taxonomy of S. costatum- like species with the description of four new species. - Journal of Phycology 41: 151-176. Go to original source...
  46. Schmid, A.-M.M. (1995): Sexual reproduction in Coscinodiscus granii Gough in culture: a preliminary report. - In: Marino, D. & Montresor, M. (eds.), Proceedings of the 13th International Diatom Symposium. - pp. 139- 159, Biopress, Bristol.
  47. Snoeijs, P. (1992): Studies in the Tabularia fasciculata complex. - Diatom Research 7: 313-344. Go to original source...
  48. Stickle, A. J. (1986): Mastogloia smithii has a method of sexual reproduction hitherto unknown in raphid diatoms. - Diatom Research 1: 271- 282. Go to original source...
  49. Stoermer, E.F. & Andresen, N.A. (2006): Atypical Tabularia in costal Lake Erie, USA. - In: Ognjanova-Rumenova, N. & Manoylov, K. (eds): Fossil and recent phycological studies. - pp. 351-361, Pensoft Publishers, Sofia- Moscow.
  50. Stosch, H.A. von (1958): Kann die oogame Araphidee Rhabdonema adriaticum als Bindeglied zwischen den beiden grossen Diatomeengruppen angesehen werden? - Berichte der Deutschen Botanischen Gesellschaft 71: 241-249. Go to original source...
  51. Subba Rao, D.V., Partensky, F., Wohlgeschaffen, G. & Li, W.K.W. (1991): Flow cytometry and microscopy of gametogenesis in Nitzschia pungens, a toxic, bloom-forming, marine diatom. - Journal of Phycology 27: 21-26. Go to original source...
  52. Williams D.M. & Round F.E. (1986): Revisions of the genus Synedra Ehrenb. - Diatom Research 1: 313-339. Go to original source...