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Diversity of Ramalina sinensis and its photobiont in local populations

Published online by Cambridge University Press:  24 August 2012

P. M. FRANCISCO DE OLIVEIRA ,
B. TIMSINA  and
M. D. PIERCEY-NORMORE
P. M. FRANCISCO DE OLIVEIRA
Affiliation:
Center for Molecular Biology and Genetic Engineering (CBMEG), State University of Campinas, Campinas, SP, Brazil.
B. TIMSINA
Affiliation:
Department of Biological Sciences, University of Manitoba, Winnipeg, MB, Canada. Email: pierceyn@cc.umanitoba.ca
M. D. PIERCEY-NORMORE*
Affiliation:
Department of Biological Sciences, University of Manitoba, Winnipeg, MB, Canada. Email: pierceyn@cc.umanitoba.ca
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Abstract

Ramalina sinensis is a widespread lichen in the Northern Hemisphere with sparse local populations, and its potential to adapt to changing environmental conditions is unknown. The objectives of this study were to determine whether geographical distance reflects fungal phylogenetic patterns, and to infer algal identity and its pattern of geographical distribution. Twenty-three samples of R. sinensis were collected from three geographical regions in Manitoba. The internal transcribed spacer of ribosomal DNA (ITS rDNA) was sequenced from each of the algal and fungal partners, and phylogenetic analyses were performed. Algal haplotypes were estimated and placed on a map of the geographical regions. Although the fungal partner showed no geographical segregation within Manitoba, the divergence of three samples added to the phylogeny from GenBank suggested that a pattern may be evident if broader geographical distances were examined. The photobiont sequence was determined to be most similar to that of Trebouxia impressa and T. potteri, two widely distributed algal species. The algal partner showed no geographical structure with sequence polymorphism or haplotype analyses. The abundance of sexual reproduction might explain widespread occurrence and the absence of geographical segregation of the fungus. This study suggests that the diversity in each of the symbionts of R. sinensis should not be a limiting factor for adaptation.

Keywords

adaptationlichensexual reproduction
Type
Research Article
Information
The Lichenologist , Volume 44 , Issue 5 , September 2012 , pp. 649 - 660
Copyright
Copyright © British Lichen Society 2012

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References

Beck, A., Kasalicky, T. & Rambold, G. (2002) Myco-photobiontal selection in a Mediterranean cryptogam community with Fulgensia fulgida . New Phytologist 153: 317–326.Google Scholar
Boch, S., Prati, D., Werth, S., Rüetschi, J. & Fischer, M. (2011) Lichen endozoochory by snails. PLoS ONE 6: e18770.Google Scholar
Brodo, I. M., Duran Sharnoff, S. & Sharnoff, S. (2001) Lichens of North America. New Haven & London: Yale University Press.Google Scholar
Clement, M., Posada, D. & Crandall, K. A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9: 1657–1660.Google Scholar
Cordeiro, L. M. C., Reis, R. A., Cruz, L. M., Stocker-Wörgötter, E., Grube, M. & Iacomini, M. (2005) Molecular studies of photobionts of selected lichens from coastal vegetation of Brazil. FEMS Microbiology Ecology 54: 381–390.Google Scholar
Culberson, C. (1972) Improved conditions and new data for the identification of lichen products by a standardized thin layer chromatographic method. Journal of Chromatography 72: 113–125.Google Scholar
Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791.Google Scholar
Friedl, T. & Büdel, B. (2008) Photobionts. In Lichen Biology. Second Edition. (Nash, T. H. III, ed.): 7–26. Cambridge: Cambridge University Press.Google Scholar
Gardes, M. & Bruns, T. D. (1993) ITS primers with enhanced specificity for basidiomycetes – application to the identification of mycorrhizae and rusts. Molecular Ecology 2: 113–118.Google Scholar
Goffinet, B. & Bayer, R. J. (1997) Characterization of mycobionts of photomorph pairs in the Peltigeraceae (lichenized Ascomycetes) based on internal transcribed spacer sequences of the nucler ribosomal DNA. Fungal Genetics and Biology 21: 228–237.Google Scholar
Grube, M., DePriest, P. T., Gargas, A. & Hafellner, J. (1995) DNA isolation from lichen ascomata. Mycological Research 99: 1321–1324.Google Scholar
Guzow-Krzeminska, B. (2006) Photobiont flexibility in the lichen Protoparmeliopsis muralis as revealed by ITS rDNA analyses. Lichenologist 38: 469–476.Google Scholar
Handa, S., Ohmura, Y., Nakano, T. & Nakahara-Tsubota, M. (2007) Airbourne green microalgae (Chlorophyta) in snowfall. Hikobia 15: 109–120.Google Scholar
Hauck, M., Helms, G. & Friedl, T. (2007) Photobiont selectivity in the lichens Hypogymnia physodes and Lecanora conizeaoides . Lichenologist 39: 195–204.Google Scholar
Hedenås, H., Lundin, K. & Ericson, L. (2006) Interaction between a lichen and a fungal parasite in a successional community: implications for conservation. Journal of Vegetation Science 17: 207–216.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: 73–86.Google Scholar
Hermansson, J. & Kudryatseva, D. (1995) Notes on the lichens of the Pechoro-Ilych Zapovednik, Komi Republic, Russia. Graphis Scripta 7: 67–78.Google Scholar
Honegger, R. (1996) Morphogenesis. In Lichen Biology (Nash, T. H. III, ed.): 65–87. Cambridge: Cambridge University Press.Google Scholar
Huelsenbeck, J. P., Ronquist, F., Nielsen, R. & Bollback, J. P. (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294: 2310–2314.Google Scholar
Joneson, S. (2003) Studies in Ramalina (Ascomycotina, Lecanorales) with emphasis on the R. almquistii species complex. M.Sc. thesis, University of Washington.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: 645–660.Google Scholar
LaGreca, S. (1999) A phylogenetic evaluation of the Ramalina americana chemotype complex (lichenized Ascomycota, Ramalinaceae) based on rDNA ITS sequence data. Bryologist 102: 602–618.Google Scholar
Li, W. C., Guo, S. Y. & Guo, L. D. (2007) Endophytic fungi VII. Three new records from lichens in China. Mycosystema 26: 32–35.Google Scholar
Lücking, R., Lawrey, 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: 1409–1418.Google Scholar
Meier, F. A., Scherrer, S. & Honegger, R. (2002) Faecal pellets of lichenivorous mites contain viable cells of the lichen-forming ascomycete Xanthoria parietina and its green algal photobiont, Trebouxia arboricola . Biological Journal of the Linnean Society 76: 259–268.Google Scholar
Muggia, L., Zellnig, G., Rabensteiner, J. & Grube, M. (2010) Morphological and phylogenetic study of algal partners associated with the lichen-forming fungus Tephromela atra from the Mediterranean region. Symbiosis 51: 149–160.Google Scholar
Mukhtar, A., Garty, J. & Galun, M. (1994) Does the lichen alga Trebouxia occur free-living in nature: further immunological evidence. Symbiosis 17: 247–253.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: 264–275.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: 43–59.Google Scholar
Orange, A., James, P. W. & White, F. J. (2001) Microchemical Methods for the Identification of Lichens. London: British Lichen Society.Google Scholar
Otálora, M. A. G., Martínez, I., O'Brien, H., Molina, M. C., Aragón, G. & Lutzoni, F. (2010) Multiple origins of high reciprocal symbiotic specificity at an intercontinental spatial scale among gelatinous lichens (Collemataceae, Lecanoromycetes). Molecular Phylogenetics and Evolution. 56: 1089–1095.Google Scholar
Peksa, O. J. & Skaloud, P. (2011) Do photobionts influence the ecology of lichens? A case study of environmental preferences in symbiotic green alga Asterochloris (Trebouxiophyceae). Molecular Ecology 20: 3936–3948.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: 947–961.Google Scholar
Piercey-Normore, M. D. (2006) The lichen-forming ascomycete Evernia mesomorpha associates with multiple genotypes of Trebouxia jamesii . New Phytologist 169: 331–344.Google Scholar
Piercey-Normore, M. D. & DePriest, P. T. (2001) Algal switching among lichen symbioses. American Journal of Botany 88: 1490–1498.Google Scholar
Posada, D. & Crandall, K. A. (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14: 817–818.Google Scholar
Rambaut, A. (2001) Se-Al: Sequence Alignment Editor V2.0. Oxford: University of Oxford.Google Scholar
Ronquist, F. & Huelsenbeck, J. P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.Google Scholar
Stocker-Worgotter, E., Elix, J. A. & Grube, M. (2004) Secondary chemistry of lichen-forming fungi: chemosyndromic variation and DNA analyses of cultures and chemotypes in the Ramalina farinacea complex. Bryologist 107: 152–162.Google Scholar
Summerfield, T. C., Galloway, D. J. & Eaton-Rye, J. J. (2002) Species of cyanolichens from Pseudocyphellaria with indistinguishable ITS sequences have different photobionts. New Phytologist 155: 121–129.Google Scholar
Swofford, D. L. (2003) PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods), version 4.0. Sunderland, Massachusetts: Sinauer Associates.Google Scholar
Takeshita, S. (2001) A taxonomic revision of the genus Trebouxia (Trebouxiophyceae, Chlorophyta). Hikobia 13: 425–455.Google Scholar
Vilgalys, R. & Hester, M. (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Journal of Bacteriology 172: 4238–4246.Google Scholar
Wagner, H. H., Holderegger, R., Werth, S., Gugerli, F., Hoebee, S. E. & Scheidegger, C. (2005) Variogram analysis of the spatial genetic structure of continuous populations using multilocus microsatellite data. Genetics 169: 1739–1752.Google Scholar
Werth, S. & Sork, V. L. (2008) Local genetic structure in a North American epiphytic lichen, Ramalina menziesii (Ramalinaceae). American Journal of Botany 95: 568–576.Google Scholar
Werth, S. & Sork, V. L. (2010) Identity and genetic structure of the photobiont of the epiphytic lichen Ramalina menziesii on three oak species in Southern California. American Journal of Botany 97: 821–830.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.): 315–322. New York: Academic Press.Google Scholar
Yahr, R., Vilgalys, R. & DePriest, P. T. (2006) Geographic variation in algal partners of Cladonia subtenuis (Cladoniaceae) highlights the dynamic nature of a lichen symbiosis. New Phytologist 171: 847–860.Google Scholar