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Ascophyllum and Its Symbionts. VII. Three-way Interactions Among Ascophyllum nodosum (Phaeophyceae), Mycophycias ascophylli (Ascomycetes) and Vertebrata lanosa (Rhodophyta)

  • Garbary, David J. (Department of Biology, St. Francis Xavier University) ;
  • Deckert, Ron J. (Department of Botany, Weber State University) ;
  • Hubbard, Charlene B. (Department of Biology, St. Francis Xavier University)
  • Published : 2005.12.01

Abstract

Ascophyllum nodosum (L.) Le Jolis has a systemic infection with the ascomycete Mycophycias ascophylli (Cotton) Kohlmeyer and Volkmann-Kohlmeyer with which it establishese a mutualistic symbiosis. In addition, A. nodosum is the host for the obligate red algal epiphyte, Vertebrata lanosa (L.) Christensen. Using light and electron microscopy we describe morphological and cytochemical changes occurring as a consequence of rhizoid penetration of V. lanosa into cortical host tissue. Rhizoids induce localized cell necrosis based on physical damage during rhizoid penetration. Host cells adjacent to the rhizoid selectively undergo a hypersensitive reaction in which they become darkly pigmented and become foci for hyphal development. Light and electron microscopy show that M. ascophylli forms dense hyphal aggregations on the surface of the V. lanosa rhizoid and extensive endophytic hyphal growths in the rhizoid wall. This is the first morphological evidence of an interaction between M. ascophylli and V. lanosa. We speculate that M. ascophylli may be interacting with V. lanosa to limit tissue damage to their shared host. In addition, the fungus provides a potential pathway for the transfer of materials (e.g., nutrients and photosynthate) between the two phototrophs.

Keywords

References

  1. Aberg P. 1989. Distinguishing between genetic individuals in Ascophyllum nodosum populations on the Swedish west coast. Br. Phycol. J. 24: 183-190 https://doi.org/10.1080/00071618900650171
  2. Adaskaveg J.E. 1992. Defense mechanisms in leaves and fruits of trees to fungal infection. In: Blanchette R.A. and Biggs A.R. (eds), Defense Mechanisms of Woody Plants Against Fungi. Springer-Verlag, Berlin. pp. 207-245
  3. Baardseth E. 1970. Synopsis of biological data on knobbed wrack Ascophyllum nodosum (Linnaeus) Le Jolis. FAG Fisheries Bulletin 38: 1-40
  4. 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
  5. Choi H.-G., Kim M.-S., Guiry M.D. and Saunders G.W. 2001. Phylogenetic relationships of Polysiphonia (Rhodomelaceae, Rhodophyta) and its relatives based on anatomical and nuclear small-subunit rDNA sequence data. Can. J. Bot. 79: 1465-1476 https://doi.org/10.1139/cjb-79-12-1465
  6. Ciciotte S.L. and Thomas R.J. 1997. Carbon fixation between Polysiphonia lanosa (Rhodophyceae) and its brown algal host. Am. J. Bot. 84: 1614-1616 https://doi.org/10.2307/2446623
  7. Citharel J. 1972. Contribution a 1'etude du metabolisme azote des algues marines. Utilisation metabolique d' acide glutamique-14C par Ascophyllum nodosum (Linne) Le Jolis et Polysiphonia Lanosa (Linne) Tandy. Bot. Mar. 15: 157-161 https://doi.org/10.1515/botm.1972.15.3.157
  8. Cousins R. 1982. The effect of exposure to wave action on the morphology and pigmentation of Ascophyllum nodosum (L.) Le Jolis in southeastern Canada. Bot. Mar. 25: 191-195 https://doi.org/10.1515/botm.1982.25.4.191
  9. Cousins R. 1984. Estimation of annual production by the intertidal brown alga Ascophyllum nodosum (L.) Le Jolis. Bot. Mar. 27: 217-227 https://doi.org/10.1515/botm.1984.27.5.217
  10. Deckert R.J. and Garbary D.J. 2005. Ascophyllum and its symbionts. VI. Microscopic characterization of the Ascophyllum nodosum (Phaeophyceae), Mycophycias ascophylli (Ascomycetes) symbiotum. Algae 20: 225-232 https://doi.org/10.4490/ALGAE.2005.20.3.225
  11. Deckert R.J., Melville L.H. and Peterson R.L. 2001. Structural features of a Lophodermium endophyte during the cryptic life-cycle phase in the foliage of Pinus strobus. Mycol. Res. 105: 991-997 https://doi.org/10.1016/S0953-7562(08)61957-7
  12. Filion-Myklebust C. and Norton T.A. 1981. Epidermis shedding in the brown seaweed Ascophyllum nodosum (L.) Jolis, and its ecological significance. Mar. Biol. Let. 2: 34-51
  13. Garbary 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
  14. Garbary D.J. and London J, 1995. The Ascophyllum / Polysiphonia / 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. Garbary D.J. and MacDonald K.A. 1995. The Ascophyllum / Polysiphonia / 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. Garbary 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
  17. Harlin M.M. and Craigie J.S. 1975. The distribution of photosynthate in Ascophyllum nodosum as it relates to epiphytic Polysiphonia Lanosa. J. Phycol. 11: 109-113
  18. 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
  19. Kohlmeyer J. and Kohlmeyer E. 1972. Is Ascophullum nodosum lichenized? Bot. Mar. 15: 109-112 https://doi.org/10.1515/botm.1972.15.2.109
  20. Kohlmeyer J. and Kohlmeyer E. 1979. Marine Mycology, The Higher Fungi. Academic Press, New York. 690 pp
  21. Kohlmeyer J. and Volkmann-Kohlmeyer B. 1998. Mycophycias, a new genus for the mycobionts of Apophlaea, Ascophyllum and Pelvetia. Systema Ascomycetum 16: 1-7
  22. Kuc J. 1983. Induced systemic resistance in plants to diseases caused by fungi and bacteria. In: Bailey J.A. and Deverall B.J. (eds), The Dynamics of Plant Defense. Academic Press, New York. pp. 255-271
  23. Lobban C.S. and Baxter D.M. 1983. Distribution of the red algal epiphyte Polysiphonia lanosa on its brown algal host Ascophyllum nodosum in the Bay of Fundy, Canada. Bot. Mar. 26: 533-538 https://doi.org/10.1515/botm.1983.26.11.533
  24. Moe R. 1997. Verrucaria tavaresiae sp. nov., a marine lichen with a brown algal photobiont. Bull. Cal. Lichen Soc. 4: 7-11
  25. Pavia H., Cervin G., Lindgren A. and Aberg P. 1997. Effects of UV-B radiation and simulated herbivory on phlorotannins in the brown alga Ascophyllum nodosum. Mar. Ecol. Prog. Ser. 157: 139-146 https://doi.org/10.3354/meps157139
  26. Pearson G.A. and Evans L.V. 1990. Settlement and survival of Polysiphonia lanosa (Ceramiales) spores on Ascophyllum nodosum and Fucus vesiculosus (Fucales). J. Phycol. 26: 597-603 https://doi.org/10.1111/j.0022-3646.1990.00597.x
  27. Pearson G.A. and Evans L.V. 1991. Stimulation of secondary rhizoid production in Polysiphonia lanosa by brown algal tissues and exudates. Br. Phycol. J. 26: 93-94
  28. Penot M. 1974. Ionic exchange between the tissues of Ascophyllum nodosum (L.) Le Jolis and Polysiphonia lanosa (L.) Tandy. Zeit. Pflanzenphysiol. 73: 125-131 https://doi.org/10.1016/S0044-328X(74)80083-8
  29. Penot M., Hourmant A. and Penot M. 1993. Comparative study of metabolism and forms of transport between Ascophyllum nodosum and Polysiphonia lanosa. Physiol. Plant. 87: 291-296 https://doi.org/10.1111/j.1399-3054.1993.tb01733.x
  30. Penot M. and Penot M. 1974. Ion transport and exchange between Ascophyllum nodosum (L.) Le Jolis and some epiphytes. Proc. Intn. Seaw. Symp. 8: 217-223
  31. Rawlence D.J. 1972. An ultrastructural study of the relationship between rhizoids of Polysiphonia lanosa (L.) Tandy (Rhodophyceae) and tissue of Ascophyllum nodosum (L.) Le Jolis (Phaeophyceae). Phycologia 11: 279-290 https://doi.org/10.2216/i0031-8884-11-3-279.1
  32. Rawlence D.J. and Taylor A.R.A. 1970. The rhizoids of Polysiphonia lanosa. Can. J. Bot. 48: 607-611 https://doi.org/10.1139/b70-083
  33. Rawlence D. J. and Taylor A.R.A. 1972. A light and electron microscopic study of rhizoid development in Polysiphonia lanosa (L.) Tandy. J. Phycol. 8: 15-24
  34. Rindi F. and Guiry M.D. 2004. Composition and spatio temporal variability of the epiphytic macroalgal assemblage of Fucus vesiculosus Linnaeus at Clare Island, Mayo, western Ireland. J. Exp. Mar. Biol. Ecol. 311: 233-252 https://doi.org/10.1016/j.jembe.2004.05.009
  35. Round F.E. 1981. The Ecology of Algae. Cambridge University Press Cambridge, UK. 653 pp
  36. Russell G. and Veltkamp C.J. 1984. Epiphyte survival on skinshedding macrophytes. Mar. Ecol. Prog. Ser. 18: 149-153 https://doi.org/10.3354/meps018149
  37. 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 Petro derma maculiforme (Phaeophyceae): thallus organization and symbiont interaction. Am. J. Bot. 91: 511-522 https://doi.org/10.3732/ajb.91.4.511
  38. Schardl C.L., Liu J. S., White J.F., Finkel R.A. and Burke J. 1991. Molecular phylogenetic relationships of non-pathogenic grass mycosymbionts and clavicipitaceous plant pathogens. PI. Syst. Evol. 178: 27-41 https://doi.org/10.1007/BF00937980
  39. Schoenwaelder M.A.E. 2002. The occurrence and cellular significance of physodes in brown algae. Phycologia 41: 125-139 https://doi.org/10.2216/i0031-8884-41-2-125.1
  40. South G.R. and Tittley I. 1986. A Checklist and Distributional Index of the Benthic Marine Algae of the North Atlantic Ocean. Huntsman Marine Laboratory and British Museum (Natural History), St. Andrews, New Brunswick and London. 76 pp
  41. Stone J.K., Viret O., Petrini O. and Chapela I.H. 1994. Histological studies of host penetration by endophytic fungi. In: Petrini, O. and Ouellette G.B. (eds), Host Wall Alterations by Parasitic Fungi APS Press. pp. 115-157
  42. Tian Lining and Garbary D.J. 1992. The Ascophyllum / olysiphonia/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
  43. Wahl M. 1989. Marine epibiosis. I. Fouling and antifouling: some basic effects. Mar. Ecol. Prog. Ser. 58: 175-189 https://doi.org/10.3354/meps058175
  44. Wahl M. and Mark O. 1999. The predominantly facultative nature of epibiosis: experimental and observational evidence. Mar. Ecol. Prog. Ser. 187: 59-66 https://doi.org/10.3354/meps187059

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