Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-23T03:42:35.012Z Has data issue: false hasContentIssue false

Genetically divergent algae shape an epiphytic lichen community on Jack Pine in Manitoba

Published online by Cambridge University Press:  08 January 2009

Matthew DOERING
Affiliation:
Department of Biological Sciences, University of Manitoba, Winnipeg, Manitoba, Canada, R3T 2N2. Email: [email protected]
Michele D. PIERCEY-NORMORE
Affiliation:
Department of Biological Sciences, University of Manitoba, Winnipeg, Manitoba, Canada, R3T 2N2. Email: [email protected]

Abstract

Algal genotypes should freely associate with different lichen fungi that grow in the same confined habitat giving the appearance of low levels of selectivity and specificity. If genetic compatibility between algal and fungal partners limits the combination of partners, then some degree of taxonomic specificity should be evident. This study examined the photobiont composition in a community of epiphytic lichens on Jack Pine to investigate selectivity and specificity. The objectives of the study were to infer algal identity, to infer photobiont dispersal, and to investigate the distribution of algal genotypes relative to the fungal partner. Photobiont variability was determined by Restriction Fragment Length Polymorphism (RFLP) and nucleotide sequences of the Internal Transcribed Spacer (ITS) of ribosomal DNA (rDNA). Seven species of lichen-forming fungi are reported to associate with five divergent algal genotypes, with only one species, Evernia mesomorpha, showing some degree of selectivity and specificity. The algae represent at least two species (Trebouxia jamesii and T. impressa) for the area confined to 200cm2 on the north side of 20 Jack Pine trees. Gene flow was inferred in this tightly defined community of lichenized algae. The algal sharing and inferred gene flow may suggest that soredia provide a means of algal transport and distribution among lichen-forming fungi in the habitat.

Type
Research Article
Copyright
Copyright © British Lichen Society 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahmadjian, V. (1988) The lichen algal Trebouxia: does it exist free-living? Plant Systematics and Evolution 158: 243247.Google Scholar
Altschul, S. F., Madden, T. L., Schaffer, A., Zhang, J., Zhang, Z., Miller, W. & Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25: 33893402.Google Scholar
Beck, A. (1999) Photobiont inventory of a lichen community on a heavy-metal-rich rock. Lichenologist 31: 501510.Google Scholar
Beck, A., Friedl, T. & Rambold, G. (1998) Selectivity of photobiont choice in a defined lichen community: inferences from cultural and molecular studies. New Phytologist 139: 709720.Google Scholar
Bubrick, P., Galun, M. & Frensdorff, A. (1984) Observations on free-living Trebouxia De Puymaly and Pseudotrebouxia Archibald, and evidence that both symbionts from Xanthoria parietina (L.) Th. Fr. can be found free-living in nature. New Phytologist 97: 455462.CrossRefGoogle Scholar
Dahkild, A., Kallersjo, M., Lohtander, K. & Tehler, A. (2001) Photobiont diversity in the Physciaceae (Lecanorales) Bryologist 104: 527536.Google Scholar
Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783791.CrossRefGoogle ScholarPubMed
Friedl, T. (1989) Comparative ultrastructure of pyrenoids in Trebouxia (Microthamniales, Chlorophyta). Plant Systematics and Evolution 164: 145159.Google Scholar
Friedl, T., Besendahl, A., Pfeiffer, P. & Bhattacharya, D. (2000) The distribution of group I introns in lichen algae suggests that lichenisation facilitates intron lateral transfer. Molecular Phylogenetics and Evolution 14: 342352.Google Scholar
Galun, M. & Bubrick, P. (1984) Physiological interactions between the partners of the lichen symbiosis. In Encyclopaedia of Plant Physiology, Vol 17. Cellular Interactions. (Linskens, H. F. & Heslop-Harrison, J., eds.): 362401. Berlin: Springer.Google Scholar
Grube, M., DePriest, P. T., Gargas, A. & Hafellner, J. (1995) DNA isolation from lichen ascomata. Mycological Research 99: 13211324.Google Scholar
Guzow-Krzeminska, B. (2006) Photobiont flexibility in the lichen Protoparmeliopsis muralis as revealed by ITS rDNA analyses. Lichenologist 38: 469476.Google Scholar
Hauck, M., Helms, G. & Friedl, T. (2007) Photobiont selectivity in the lichens Hypogymnia physodes and Lecanora conizeaoides. Lichenologist 39: 195204.CrossRefGoogle Scholar
Hawksworth, D. L. & Rose, F. (1970) Qualitative scale for estimating sulphur dioxide air pollution in England and Wales using epiphytic lichens. Nature 227: 145148.Google Scholar
Helms, G., Friedl, T., Rambold, G. & Mayrhofer, H. (2001) Identification of photobionts from the lichen family Physciaceae using algal-specific ITS rDNA sequencing. Lichenologist 33: 7386.CrossRefGoogle Scholar
Honegger, R. (1996) Mycobionts. In Lichen Biology 1st edition (Nash, T. H. III, ed.): 2436. New York: Cambridge University Press.Google Scholar
Honegger, R. (2008) Morphogenesis. In Lichen Biology 2nd edition (Nash, T. H. III, ed.): 6993. New York: Cambridge University Press.Google Scholar
Huelsenbeck, J. P., Ronquist, F., Nielsen, R. & Boliback, J. P. (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294: 23102314.Google Scholar
Kimura, M. (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16: 111120.Google Scholar
Kroken, S. & Taylor, J. W. (2000) Phylogenetic species, reproductive mode, and specificity of the green alga Trebouxia forming lichens with the fungal genus Letharia. Bryologist 103: 645660.Google Scholar
Mukhtar, A., Garty, J. & Galun, M. (1994) Does the lichen alga Trebouxia occur free-living in nature: further immunological evidence. Symbiosis 17: 247253.Google Scholar
Murtagh, G. J., Dyer, P. S. & Crittenden, P. D. (2000) Sex and the single lichen. Nature 404: 564.Google Scholar
Nash, T. H. III. (1996) Introduction. In Lichen Biology (Nash, T. H. III, ed.): 17. New York: Cambridge University Press.Google Scholar
Nelsen, M. P. & Gargas, A. (2008) Dissociation and horizontal transmission of codispersing lichen symbionts in the genus Lepraria (Lecanorales: Stereocaulaceae). New Phytologist 177: 264275.Google Scholar
Ohmura, Y., Kawachi, M., Kasai, F. & Watanabe, M. (2006) Genetic combinations of symbionts in a vegetatively reproducing lichen, Parmotrema tinctorum, based on ITS rDNA sequences. Bryologist 109: 4359.Google Scholar
Opanowicz, M. & Grube, M. (2004) Photobiont genetic variation in Flavocetraria nivalis from Poland. Lichenologist 36: 125131.Google Scholar
Peakall, R. & Smouse, P. E. (2005) GENALEX V6 Genetic Analysis in Excel. Canberra: Australian National University.Google Scholar
Piercey-Normore, M. D. (2004) Selection of algal genotypes by three species of lichen fungi in the genus Cladonia. Canadian Journal of Botany 82: 947961.Google Scholar
Piercey-Normore, M. D. (2006) The lichen-forming ascomycete Evernia mesomorpha associates with multiple genotypes of Trebouxia jamesii. New Phytologist 169: 331344.Google Scholar
Piercey-Normore, M. D. & DePriest, P. T. (2001) Algal switching among lichen symbioses. American Journal of Botany 88: 14901498.Google Scholar
Posada, D. & Crandall, K. A. (1998) Modeltest: testing the mode! of DNA substitution. Bioinformatics 14: 817818.CrossRefGoogle Scholar
Printzen, C. & Ekman, S. (2003) Local population subdivision in the lichen Cladonia subcervicornis as revealed by mitochondrial cytochrome oxidase subunit 1 intron sequences. Mycologia 95: 399406.Google Scholar
Rambaut, A. (2001) Se-Al: Sequence Alignment Editor V2.0. Oxford, UK: University of Oxford.Google Scholar
Rambold, G., Friedl, T. & Beck, A. (1998) Photobionts in lichens: possible indicators of phylogenetic relationships? Bryologist 101: 392397.CrossRefGoogle Scholar
Robertson, J. & Piercey-Normore, M. D. (2007) Gene flow in symbionts of Cladonia arbuscula. Lichenologist 39: 6982.CrossRefGoogle Scholar
Romeike, J., Friedl, T., Helms, G. & Ott, S. (2002) Genetic diversity of algal and fungal partners in four species of Umbilicaria (Lichenised Ascomycetes) along a transect of the Antarctic Peninsula. Molecular Biology and Evolution 19: 12091217.Google Scholar
Ronquist, F. & Huelsenbeck, J. P. (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 15721574.Google Scholar
Slocum, R. D., Ahmadjian, V. & Hildreth, K. C. (1980) Zoosporogenesis in Trebouxia gelatinosa: ultrastructure potential for zoospore release and implications for the lichen association. Lichenologist 12: 173187.Google Scholar
Smith, D. C. & Douglas, A. (1987) The Biology of Symbiosis. Edward Arnold, London.Google Scholar
Swofford, D. L. (2003) PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods), version 4.0, Sunderland, MA: Sinauer Associates.Google Scholar
Tapper, R. (1976) Dispersal and changes in the local distribution of Evernia prunastri and Ramalina farinacea. New Phytologist 77: 725734.Google Scholar
Tschermak-Woess, E. (1978) Myrmecia reticulata as a photobiont and free-living Trebouxia—the problem of Stenocybe septata. Lichenologist 10: 6979.CrossRefGoogle Scholar
Tschermak-Woess, E. (1980) Asterochloris phycobiontica, nov. gen., nova spec., the phycobiont of the lichen Varicellaria carneonivea (Anzi) Erichs. Plant Systematics and Evolution 135: 279294.Google Scholar
Tschermak-Woess, E. (1988) The algal partner. In CRC Handbook of Lichenology. Volume I. (Galun, M., ed.): 3992. Boca Raton: CRC Press.Google Scholar
Walser, J. C. (2004) Molecular evidence for limited dispersal of vegetative propagules in the epiphytic lichen Lobaria pulmonaria. American Journal of Botany 91: 12731276.Google Scholar
Weir, B. S. & Cockerham, C. C. (1984) Estimating F-statistics for the analysis of population structure. Evolution 38: 13581370.Google Scholar
White, T. J., Bruns, T., Lee, S. & Taylor, J. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In PCR Protocols: A Guide to Methods and Applications. (Innis, M. A., Gelfand, D. H., Sninsky, J. J. & White, T. J., eds.): 315322. New York, USA: Academic Press, Inc.Google Scholar
Yahr, R., Vilgalys, R. & DePriest, P. T. (2004) Strong fungal specificity and selectivity for algal symbionts in Florida scrub Cladonia lichens. Molecular Ecology 13: 33673378.Google Scholar