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New morphological aspects of cephalodium formation in the lichen Lobaria pulmonaria (Lecanorales, Ascomycota)

Published online by Cambridge University Press:  08 January 2013

Carolina CORNEJO
Affiliation:
Swiss Federal Institute for Forest, Snow and Landscape Research WSL, 8903 Birmensdorf, Switzerland. Email: carolina.cornejo@wsl.ch
Christoph SCHEIDEGGER
Affiliation:
Swiss Federal Institute for Forest, Snow and Landscape Research WSL, 8903 Birmensdorf, Switzerland. Email: carolina.cornejo@wsl.ch

Abstract

Cephalodia were investigated on young and mature thalli of Lobaria pulmonaria. Cephalodia originate from contact between hyphae and cyanobacteria on the upper or lower cortex or, less frequently, in the apical zone. Young thalli were found to associate with cyanobacteria even in the anchoring zone. Cephalodia formed on the young thalli or the anchoring hyphae share the same phenotypic characteristics. In spite of being composed of paraplectenchymatous hyphae, the cortex of mature thalli preserves a considerable plasticity, enabling the formation of cephalodia. The cyanobacterial incorporation process begins with cortical hyphae growing out towards adjacent cyanobacterial colonies, enveloping them and incorporating them into the thallus. The incorporation process is the same on the upper and the lower cortex. Early stages of cephalodia are usually found in young lobes, whereas in the older parts of the thallus only mature cephalodia are found.

Type
Articles
Copyright
Copyright © British Lichen Society 2013

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References

Antoine, M. E. (2004) An ecophysiological approach to quantifying nitrogen fixation by Lobaria oregana . Bryologist 107: 8287.Google Scholar
Benner, J. W., Conroy, S., Lunch, C. K., Toyoda, N. & Vitousek, P. M. (2007) Phosphorus fertilization increases the abundance and nitrogenase activity of the cyanolichen Pseudocyphellaria crocata in Hawaiian montane forests. Biotropica 39: 400405.CrossRefGoogle Scholar
Büdel, B. & Scheidegger, C. (1996) Thallus morphology and anatomy. In Lichen Biology (Nash, T. H. III, ed): 2436. Cambridge: Cambridge University Press.Google Scholar
Costa, J.-L., Paulsrud, P., Rikkinen, J. & Lindblad, P. (2001) Genetic diversity of Nostoc endophytically associated with two bryophyte species. Applied and Environmental Microbiology 67: 43934396.Google Scholar
Costa, J.-L., Martinez Romero, E. & Lindblad, P. (2004) Sequence based data supports a single Nostoc strain in individual coralloid roots of cycads. FEMS Microbiology Ecology 49: 481487.Google Scholar
De los Ríos, A., Raggio, J., Pérez-Ortega, S., Vivas, M., Pintado, A., Green, T. G. A., Ascaso, C. & Sancho, L. G. (2011) Anatomical, morphological and ecophysiological strategies in Placopsis pycnotheca (lichenized fungi, Ascomycota) allowing rapid colonization of recently deglaciated soils. Flora 206: 857864.Google Scholar
Díaz, E.-M., Sacristán, M., Legaz, M.-E. & Vicente, C. (2009) Isolation and characterization of a cyanobacterium-binding protein and its cell wall receptor in the lichen Peltigera canina . Plant Signaling and Behavior 4: 598603.CrossRefGoogle ScholarPubMed
Díaz, E.-M., Vicente-Manzanares, M., Sacristán, M., Vicente, C. & Legaz, M.-E. (2011) Fungal lectin of Peltigera canina induces chemotropism of compatible Nostoc cells by constriction-relaxation pulses of cyanobiont cytoskeleton. Plant Biology 12: 615621.Google Scholar
Elifio, S. L., De Lourdes, M., Da Silva, C. C., Iacomini, M. & Gorini, P. A. J. (2000) A lectin from the lichenized Basidiomycete Dictyonema glabratum . New Phytologist 148: 327334.Google Scholar
Feoktistov, A. S., Kitashov, A. V. & Lobakova, E. S. (2009) The characterization of lectins from the tripartite lichen Peltigera aphthosa (L.) Willd. Moscow University Biological Sciences Bulletin 64: 2327.Google Scholar
Forsell, K. B. J. (1884) Lichenologische Untersuchungen: Ueber die Cephalodien. Flora 67: 18, 33–46, 58–63, 177–187.Google Scholar
Green, T. G. A., Horstmann, J., Bonnett, H., Wilkins, A. & Silvester, W. B. (1980) Nitrogen fixation by members of the Stictaceae (lichenes) of New Zealand. New Phytologist 84: 339348.CrossRefGoogle Scholar
Green, T. G. A., Schlensog, M., Sancho, L. G., Winkler, J. B., Broom, F. D., Schroeter, B. (2002) The photobiont determines the pattern of photosynthetic activity within a single lichen thallus containing cyanobacterial and green algal sectors (photosymbiodeme). Oecologia 130: 191198.CrossRefGoogle ScholarPubMed
Guzman, G., Quilhota, W. & Galloway, D. J. (1990) Decomposition of species of Pseudocyphellaria and Sticta in a southern Chilean forest. Lichenologist 22: 325331.Google Scholar
Hawksworth, D. L. & Hill, D. J. (1984) The Lichen-forming Fungi. Glasgow and London: Blackie & Son Ltd. Google Scholar
Henssen, A. & Jahns, H. M. (1974) Lichenes. Stuttgart: Thieme Verlag.Google Scholar
Honegger, R. (1987) Questions about pattern formation in the algal layer of lichens with stratified (heteromerous) thalli. Bibliotheca Lichenologica 25: 5971.Google Scholar
Honegger, R. (2001) The symbiotic phenotype of lichen-forming Ascomycetes. In The Mycota IX. (Hock, B., ed): 165188. Berlin, Heidelberg: Springer-Verlag.Google Scholar
Hue, M. L'abbé (1904) Description de deux espèces de lichens et de céphalodies nouvelles: Céphalodies. Extrait des annals de l'association des naturalistes de Levallois-Perret 10: 3741.Google Scholar
Jahns, H. M. (1988) The lichen thallus. In CRC Handbook of Lichenology (Galun, M., ed.): 95143. Boca Raton, Florida: CRC Press.Google Scholar
Jensen, M. & Siebke, K. (1997) Fluorescence imaging of lichens in the macro scale. Symbiosis 23: 183196.Google Scholar
Jordan, W. P. (1970) The internal cephalodia of the genus Lobaria . Bryologist 73: 669681.Google Scholar
Kardish, N., Silberstein, L., Flemminger, N. & Galun, M. (1991) Lectin from the lichen Nephroma laevigatum Ach. Localization and function. Symbiosis 11: 4762.Google Scholar
Kaule, A. (1932) Die Cephalodien der Flechten. Flora 126: 144.Google Scholar
Knops, J. M., Nash, T. H. III, Boucher, V. L. & Schlesinger, W. H. (1991) Mineral cycling and epiphytic lichens: implications at the ecosystem level. Lichenologist 23: 309321.CrossRefGoogle Scholar
Knowles, R. D., Pastor, J. & Biesboer, D. D. (2006) Increased soil nitrogen associated with dinitrogen-fixing, terricolous lichens of the genus Peltigera in northern Minnesota. Oikos 114: 3748.Google Scholar
Lallemant, R. & Bernard, T. (1977) Obtention de cultures pures des mycosymbiotes du Lobaria laetevirens (Lightf.) Zahlbr. et du Lobaria pulmonaria (L.) Hoffm.: le role des gonidies. Revue Bryologique et Lichenologique 43: 303308.Google Scholar
Lawrey, J. D. (1986) Biological role of lichen substances. Bryologist 89: 111122.CrossRefGoogle Scholar
Legaz, M.-E., Fontaniella, B., Millanes, A.-M. & Vicente, C. (2004) Secreted arginases from phylogenetically far-related lichen species act as cross-recognition factors for two different algal cells. European Journal of cell biology 83: 435446.Google Scholar
Lehr, H., Galun, M., Ott, S., Jahns, H.-M. & Fleminger, G. (2000) Cephalodia of the lichen Peltigera aphthosa (L.) Willd. Specific recognition of the compatible photobiont. Symbiosis 29: 357365.Google Scholar
Lohtander, K., Oksanen, I. & Rikkinen, J. (2003) Genetic diversity of green algal and cyanobacterial photobionts in Nephroma (Peltigerales). Lichenologist 35: 325329.Google Scholar
Lücking, R., Lawry, J. D., Sikaroodi, M., Gillevet, P. M., Chaves, J. L., Sipman, H. J. M. & Bungartz, F. (2009) Do lichens domesticate photobionts like farmers domesticate crops? Evidence from a previously unrecognized lineage of filamentous cyanobacteria. American Journal of Botany 96: 14091418.Google Scholar
Miądlikowska, J. & Lutzoni, F. (2000) Phylogenetic revision of the genus Peltigera (lichen-forming Ascomycota) based on morphological, chemical, and large subunit nuclear ribosomal DNA data. International Journal of Plant Science 161: 925958.Google Scholar
Miądlikowska, J. & Lutzoni, F. (2004) Phylogenetic classification of peltigeralean fungi (Peltigerales, Ascomycota) based on ribosomal RNA small and large subunits. American Journal of Botany 91: 449464.CrossRefGoogle ScholarPubMed
Moreau, M. F. (1921) Recherches sur les lichens de la famille des Stictacées . Annales des Sciences Naturelles. Botanique, Dixiéme Série, 3: 297374.Google Scholar
Myllys, L., Stenroos, S., Thell, A. & Kuusinen, M. (2007) High cyanobiont selectivity of epiphytic lichens in old growth boreal forest of Finland. New Phytologist 173: 621629.Google Scholar
Nylander, W. (1868) Circa cephalodia simul epigena et hypogena. Flora 51: 372373.Google Scholar
Ott, S., Treiber, K. & Jahns, H.-M. (1993) The development of regenerative thallus structures in lichens. Botanical Journal of the Linnean Society 113: 6176.Google Scholar
Paulsrud, P. & Lindblad, P. (2002) Fasciclin domain proteins are present in Nostoc symbionts of lichens. Applied and Environmental Microbiology 68: 20362039.Google Scholar
Paulsrud, P., Rikkinen, J. & Lindblad, P. (1998) Cyanobiont specificity in some Nostoc-containing lichens and a Peltigera aphthosa photosymbiodeme. New Phytologist 139: 517524.CrossRefGoogle Scholar
Paulsrud, P., Rikkinen, J. & Lindblad, P. (2000) Spatial patterns of photobiont diversity in some Nostoc-containing lichens. New Phytologist 146: 291299.Google Scholar
Paulsrud, P., Rikkinen, J. & Lindblad, P. (2001) Field experiments on cyanobacterial specificity in Peltigera aphthosa . New Phytologist 152: 117123.Google Scholar
Poelt, J. & Mayrhofer, H. (1988) Über Cyanotrophie bei Flechten. Plant Systematics and Evolution 158: 265281.Google Scholar
Rai, A. N. & Bergman, B. (2002) Cyanolichens. Biology and Environment: Proceedings of the Royal Irish Academy 102: 1922.Google Scholar
Rikkinen, J. (2009) Relations between cyanobacterial symbionts in lichens and plants. Microbiology Monographs 8: 265270.Google Scholar
Rikkinen, J., Oksanen, I. & Lohtander, K. (2002) Lichen guilds share related cyanobacterial symbionts. Science 297: 357.Google Scholar
Scheidegger, C. (1995) Early development of transplanted isidioid soredia of Lobaria pulmonaria in an endangered population. Lichenologist 27: 361374.Google Scholar
Scheidegger, C., Clerc, P., Dietrich, M., Frei, M., Groner, U., Keller, C., Roth, I., Stofer, S. & Vust, M. (2002) Rote Liste der gefährdeten baum- und erdbewohnenden Flechten der Schweiz. Bern: WSL, CJB, BUWAL.Google Scholar
Stenroos, S., Högnabba, F., Myllys, L., Hyvönen, J. & Thell, A. (2006) High selectivity in symbiotic associations of lichenized ascomycetes and cyanobacteria. Cladistics 22: 230238.CrossRefGoogle Scholar
Stocker-Wörgötter, E. (1994) Artificial resynthesis of the photosymbiodeme Peltigera leucophlebia under laboratory conditions. Cryptogamic Botany 4: 300308.Google Scholar
Stocker-Wörgötter, E. (1995) Experimental cultivation of lichens and lichen symbiosis. Canadian Journal of Botany 73: 579589.Google Scholar
Stocker-Wörgötter, E. (2001) Experimental studies of the lichen symbiosis: DNA-analysis, differentiation and secondary chemistry of selected mycobionts, artificial resysthesis of two- and tripartite symbiosis. Symbiosis 30: 207227.Google Scholar
Sundberg, B., Näsholm, T. & Palmqvist, K. (2001) The effect of nitrogen on growth and key thallus components in the two tripartite lichens, Nephroma arcticum and Peltigera aphtosa . Plant, Cell and Environment 24: 517527.Google Scholar
Trembley, M. L., Ringli, C. & Honegger, R. (2002) Morphological and molecular analysis of early stages in the resynthesis of the lichen Baeomyces rufus . Mycological Research 106: 768776.CrossRefGoogle Scholar
Vivas, M., Sacristán, M., Legaz, M. E. & Vicente, C. (2009) The cell recognition model in chlorolichens involving a fungal lectin binding to an algal ligand can be extended to cyanolichens. Plant Biology 12: 615621.Google Scholar
Winter, G. (1877) Lichenologische Notizen: Cephalodien von Sticta und Solorina . Flora 60: 177203, 193–203.Google Scholar