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The Korean Society of Phycology (한국조류학회(藻類))
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Ascophyllum and its symbionts. VI. Microscopic Characterization of the Ascophyllum nodosum (Phaeophyceae), Mycophycias ascophylli (Ascomycetes) Symbiotum

  • Deckert, R. J. (Department of Botany, Weber State University) ;
  • Garbary, D. J. (Department of Biology, St. Francis Xavier University)
  • Published : 2005.09.01
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Abstract

Optical microscopy of recently living and cleared material of the fucoid, Ascophyllum nodosum (L.) Le Jolis, revealed novel aspects of its interaction with the ascomycete Mycophycias ascophylli (Cotton) Kohlmeyer and Kohlmeyer (previously Mycosphaerella ascophylli Cotton). Most host cells are associated with hyphae by lateral attachment of cell walls. Hyphae form extensive networks throughout the host thallus and show considerable differentiation in the various host tissues. In the base of epidermal cells, hyphae form multicellular rings around each host cell to produce a continuous network. In medullary regions, long, relatively unbranched and longitudinally aligned hyphae occur, with radial branches extending into cortical regions. Scattered in the inner cortex of host tissue are numerous multicellular nodes of smaller, polygonal to irregular shaped cells with five or more radiating arms of hyphae. Individual hyphal cells show a variety of specializations including swellings and appressoria-like attachments to some host cells. These observations provide the morphological basis for the mutualistic symbiosis supported by recent experimental work. We conclude that this association is best described by the term “symbiotum.”

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References

  1. Baardseth E. 1970. Synopsis of biological data on knobbed wrack Ascophyllum nodosum (Linnaeus) Le Jolis. FAD Fish. Bull. 38: 1-40
  2. Bacon C.W. and Hill N.S. 1996. Symptomless grass endophytes: products of coevolutionary symbioses and their role in the ecological adaptations of grasses. In: Redlin S.C. and Carris L.M. (eds), Endophytic Fungi in Grasses and Woody Plants: Systematics, Ecology and Evolution. APS Press, St. Paul, Minnesota. pp. 155-178
  3. Budel B. and Scheidegger C. 1996. Thallus morphology and anatomy. In: Nash T.H. (ed.), Lichen Biology. Cambridge University Press, Cambridge, U.K. pp. 37-64
  4. Chapman A.R.O. 1995. Functional ecology of fucoid algae:twenty-three years of progress. Phycologia 34: 1-32 https://doi.org/10.2216/i0031-8884-34-1-1.1
  5. Clay K. 1988. Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecology 69: 10-16 https://doi.org/10.2307/1943155
  6. Clay K. 1990. Fungal endophytes of grasses. Ann. Rev. Ecol. Syst. 21: 275-297 https://doi.org/10.1146/annurev.es.21.110190.001423
  7. Clay K. and Holah J. 1999. Fungal endophyte symbiosis and plant diversity in successional fields. Science 285: 1742-1743 https://doi.org/10.1126/science.285.5434.1742
  8. Cotton A.D. 1909. Notes on marine pyrenomycetes. Trans. Br. Mycol. Soc. 3: 92-99
  9. Fell J.W. and Newell S.Y. 1998. Biochemical and molecular methods for the study of marine fungi. In: Cooksey K.E. (ed.), Molecular Approaches to the Study of the Ocean. Chapman & Hall, London. pp. 259-283
  10. Fries L. 1988. Ascophyllum nodosum (Phaeophyta) in axenic culture and its response to the endophytic fungus Mycosphaerella ascophylli and epiphytic bacteria. J. Phycol. 24: 333-337
  11. Fries N. and Thoren-Tolling K. 1978. Identity of the fungal endophyte of Ascophyllum with Mycosphaerella ascophylli established by means of fluorescent antibody techniques. Bot. Mar. 21: 409-411 https://doi.org/10.1515/botm.1978.21.7.409
  12. Carbary D.J. and Deckert R.J. 2001. Three part harmony Ascophyllum and its symbionts. In: Seckbach J. (ed.), Symbiosis: Mechanisms and Model Systems. Kluwer, Dortrecht, The Netherlands. pp. 309-321
  13. Carbary D.J. and Cautam A. 1989. The Ascophyllum / Polysiphonia / Mycosphaerella symbiosis. I. Population ecology of Mycosphaerella from Nova Scotia. Bot. Mar. 32: 181-186 https://doi.org/10.1515/botm.1989.32.2.181
  14. Carbary D.J. and London J. 1995. The Ascophylluml Polysiphonial Mycosphaerella symbiosis. V. Mycosphaerella protects A. nodosum from desiccation. Bot. Mar. 38: 529-33 https://doi.org/10.1515/botm.1995.38.1-6.529
  15. Carbary D.J. and MacDonald K.A. 1995. The Ascophyllum / Polysiphonial / Mycosphaerella symbiosis. IV. Mutualism in the Ascophyllum / Mycosphaerella symbiosis. Bot. Mar. 38: 221-225 https://doi.org/10.1515/botm.1995.38.1-6.221
  16. Carbary D.J. and McDonald A.R. 1998. Molecules, organelles and cells: fluorescence microscopy and red algal development. In: Cooksey K.E. (ed.), Molecular Approaches to the Study of the Ocean. Chapman & Hall, London. pp. 409-422
  17. Carbary D.J., Tian Lining and Burke J. 1991. The Ascophyllum / Polysiphonia / Mycosphaerella symbiosis. II. Aspects of the ecology and distribution of Polysiphonia in Nova Scotia. Bot. Mar. 34: 391-401 https://doi.org/10.1515/botm.1991.34.5.391
  18. Goff L.J. and Coleman A.W. 1990. DNA: microfluorometric studies. In: Cole K.M. and Sheath R.G. (eds), Biology of the Red Algae. Cambridge University Press, Cambridge, U.K. pp.43-71
  19. Hawksworth D.L. 1988. The variety of fungal-algal symbioses, their evolutionary significance, and the nature of lichens. Bot. J. Lin. Soc. 96: 3-20 https://doi.org/10.1111/j.1095-8339.1988.tb00623.x
  20. Issac S. 1992. Fungal - Plant Interactions. Chapman & Hall, London
  21. Kingham D.L. and Evans L.V. 1986. The Pelvetia-Mycosphaerella interrelationship. In: Moss S.T. (ed.), The Biology of Marine Fungi. Cambridge University Press, Cambridge, U.K. pp. 177-187
  22. Kohlmeyer J. and Hawkes M.W. 1983. A suspected case of mycophycobiosis between Mycosphaerella apophlaeae(Ascomycetes) and Apophlaea spp. (Rhodophyta). J. Phycol. 19: 257-260 https://doi.org/10.1111/j.0022-3646.1983.00257.x
  23. Kohlmeyer J. and Kohlmeyer E. 1972. Is Ascophyllum nodosum lichenized? Bot. Mar. 15: 109-112 https://doi.org/10.1515/botm.1972.15.2.109
  24. Kohlmeyer J. and Kohlmeyer E. 1979. Marine Mycology, the Higher Fungi. Academic Press, New York
  25. Kohlmeyer J. and Volkmann-Kohlmeyer B. 1998. Mycophycias, a new genus for the mycobionts of Apophlaea, Ascophyllum and Pelvetia. Systema Ascomycetum 16: 1-7
  26. Lud D., Huiskes A.H.L. and Ott S. 2001. Morphological evidence for the symbiotic character of Turgidosculum complicatum Kohlm & Kohlm. ( = Mastodia tesselata Hook. f. & Harvey). Symbiosis 31: 141-151
  27. Moe R. 1997. Verrucaria tavaresiae sp. nov., a marine lichen with a brown algal photobiont. Bull. Cal. Lichen Soc. 4: 7-11
  28. Nash T.H. 1996. Lichen Biology. Cambridge University Press, Cambridge, U.K
  29. Omacini M., Chaneton E.J., Chersa C.M., and Mulller C.B. 2001. Symbiotic fungal endophytes control insect host-parasite interaction webs. Nature 409: 78-81 https://doi.org/10.1038/35051070
  30. Power M. E., Tilman D., Estes J.A., Menge B.A., Bond W.J. Mills L.S., Daily G., J. Castilla C., Lubchenco J. and Paine R.T. 1996. Challenges in the quest for keystones. Bioscience 46: 609-620 https://doi.org/10.2307/1312990
  31. Rudgers J.A., Koslow J.M. and Clay K. 2004. Endophytic fungi alter relationships between diversity and ecosystem properties. Ecol. Let. 7: 42-51 https://doi.org/10.1046/j.1461-0248.2003.00543.x
  32. Sanders W.B., Moe R.L. and Ascaso C. 2004. The intertidal marine lichen formed by the pyrenomycete fungus Verrucaria tavaresiae (Ascomycotina) and the brown alga Petroderma maculiforme (Phaeophyceae): thallus organization and symbiont interaction. Am. J. Bot. 91: 511-522 https://doi.org/10.3732/ajb.91.4.511
  33. Schardl C.L., Liu J.S., White J.F. Jr., Finkel R.A. and Burke J. 1991. Molecular phylogenetic relationships of nonpathogenic grass mycosymbionts and clavicipitaceous plant pathogens. Pl. Syst. Evol. 178: 27-41 https://doi.org/10.1007/BF00937980
  34. Schulz B. and Boyle C. 2005. The endophytic continuum. Mycol. Res.109: 661-686 https://doi.org/10.1017/S095375620500273X
  35. Smith A.L. and Ramsbottom J. 1915. Is Pelvetia canaliculata a lichen? New Phytol. 14: 295-298 https://doi.org/10.1111/j.1469-8137.1915.tb07167.x
  36. Stocker-Worgotter E. 1995. Experimental cultivation of lichens and lichen symbionts. Can. J. Bot. 73 (Suppl, 1): 5579-5589
  37. Stone J.K. 1987. Initiation and development of latent infections by Rhabdocline parkeri on Douglas-fir. Can. J. Bot. 65: 2614-2621 https://doi.org/10.1139/b87-352
  38. Tian Lining and Carbary D.J. 1992. The Ascophyllum / Polysiphonia/Mycosphaerella symbiosis. III. Culture studies on the interaction between Polysiphonia lanosa and Ascophyllum nodosum. Bot. Mar. 35: 341-349 https://doi.org/10.1515/botm.1992.35.4.341
  39. West C.P.. Oosterhuis D.M. and Wullschleger S.D. 1990. Osmotic adjustment in tissues of tall fescue in response to water deficit. Environ. Exp. Bot. 30: 1-8 https://doi.org/10.1016/0098-8472(90)90002-L

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