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Testing the correlation between norstictic acid content and species evolution in the Cetraria aculeata group in Europe

Published online by Cambridge University Press:  18 January 2017

Tetiana LUTSAK*
Affiliation:
Senckenberg Research Institute and Natural History Museum, 60325 Frankfurt am Main, Germany
Fernando FERNÁNDEZ-MENDOZA
Affiliation:
Institute of Plant Sciences, Karl-Franzens-Universität Graz, A-8010, Graz, Austria
Olga NADYEINA
Affiliation:
Swiss Federal Institute for Forest, Snow and Landscape Research, WSL, CH-8903 Birmensdorf, Switzerland; M. G. Kholodny Institute of Botany, National Academy of Sciences of Ukraine, 01601 Kiev, Ukraine
Ayhan ŞENKARDEŞLER
Affiliation:
Department of Biology, Faculty of Science, Ege University, Bornova, 35100 İzmir, Turkey
Christian PRINTZEN
Affiliation:
Senckenberg Research Institute and Natural History Museum, 60325 Frankfurt am Main, Germany
*

Abstract

Most lichen-forming fungi are characterized by the production of secondary metabolites. Differences in metabolite patterns have frequently served to distinguish lichen taxa with subsequent controversies about the rank of chemical variants (chemotype, variety, subspecies or species). Using a model system, we investigate whether production of norstictic acid within a group of lichenized ascomycetes is correlated with phylogenetic patterns, population differentiation or single and multi-locus haplotypes. Our study is based on DNA sequences of three gene loci (ITS, GPD, mtLSU) together with HPLC (311) and TLC (594) data from a total of 594 samples of three closely related fruticose lichens: Cetraria aculeata and C. muricata without norstictic acid, and C. steppae with norstictic acid. In nature, C. aculeata and C. steppae often occur together and the status of C. steppae as a separate species has been questioned. Our results show geographical but no phylogenetic structure of norstictic acid production and few significant associations between genetic clusters and the occurrence of norstictic acid. All frequently distributed haplotypes display differences in norstictic acid content. The few associations at the population level are most likely a by-product of spatial genetic structure, because norstictic acid was expressed only in individuals from the Mediterranean-Central Asian part of the study area. We conclude that the production of norstictic acid in the C. aculeata group is most likely triggered by the environment (climate, edaphic factors, associated symbionts). Cetraria steppae might be a different evolutionary lineage restricted to warm temperate regions but it is not uniquely characterized by the presence of norstictic acid.

Type
Articles
Copyright
© British Lichen Society, 2017 

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References

Armaleo, D., Zhang, Y. & Cheung, S. (2008) Light might regulate divergently depside and depsidone accumulation in the lichen Parmotrema hypotropum by affecting thallus temperature and water potential. Mycologia 100: 565576.CrossRefGoogle ScholarPubMed
Articus, K., Mattsson, J.-E., Tibell, L., Grube, M. & Wedin, M. (2002) Ribosomal DNA and β-tubulin data do not support the separation of the lichens Usnea florida and U. subfloridana as distinct species. Mycological Research 106: 412418.CrossRefGoogle Scholar
Asplund, J. & Gauslaa, Y. (2007) Content of secondary compounds depends on thallus size in the foliose lichen Lobaria pulmonaria . Lichenologist 39: 273278.CrossRefGoogle Scholar
Brodo, I. M. (1984) Lichenes Canadenses Exsiccati, Fascicle III. Bryologist 87: 97111.CrossRefGoogle Scholar
Crespo, A. & Barreno, E. (1978) Sobre las comunidades terricolas de liquenes vagantes (Sphaerothallio-Xanthoparmelion vagantis al. nov.). Acta Botanica Malacitana 4: 5562.CrossRefGoogle Scholar
Crespo, A. & Lumbsch, H. T. (2010) Cryptic species in lichen-forming fungi. IMA Fungus 1: 167170.CrossRefGoogle ScholarPubMed
Crespo, A. & Pérez-Ortega, S. (2009) Cryptic species and species pairs in lichens: a discussion on the relationship between molecular phylogenies and morphological characters. Anales del Jardín Botánico de Madrid 66: 7181.CrossRefGoogle Scholar
Culberson, C. F. & Culberson, W. L. (1976) Chemosyndromic variation in lichens. Systematic Botany 1: 325339.CrossRefGoogle Scholar
Culberson, W. L. (1967) Analysis of chemical and morphological variation in the Ramalina siliquosa species complex. Brittonia 19: 333352.CrossRefGoogle Scholar
Culberson, W. L., Culberson, C. F. & Johnson, A. (1977) Correlations between secondary-product chemistry and ecogeography in the Ramalina siliquosa group (lichens). Plant Systematics and Evolution 127: 191200.CrossRefGoogle Scholar
Divakar, P. K., Crespo, A., Blanco, O. & Lumbsch, H. T. (2006) Phylogenetic significance of morphological characters in the tropical Hypotrachyna clade of parmelioid lichens (Parmeliaceae, Ascomycota). Molecular Phylogenetics and Evolution 40: 448458.CrossRefGoogle ScholarPubMed
Domaschke, S., Fernández-Mendoza, F., García, M. A., Martín, M. P. & Printzen, C. (2012) Low genetic diversity in Antarctic populations of the lichen-forming ascomycete Cetraria aculeata and its photobiont. Polar Research 31: 113.CrossRefGoogle Scholar
Drummond, A. J., Suchard, M. A., Xie, D. & Rambaut, A. (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29: 19691973.CrossRefGoogle ScholarPubMed
Drummond, A. J., Ashton, B., Buxton, S., Cheung, M. & Cooper, A. (2013) Geneious v7.1.9. Available at: http://www.geneious.com.Google Scholar
Elix, J. A., Corush, J. & Lumbsch, H. T. (2009) Triterpene chemosyndromes and subtle morphological characters characterise lineages in the Physcia aipolia group in Australia (Ascomycota). Systematics and Biodiversity 7: 479487.CrossRefGoogle Scholar
Evanno, G., Regnaut, S. & Goudet, J. (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14: 26112620.CrossRefGoogle ScholarPubMed
Falush, D., Stephens, M. & Pritchard, J. K. (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164: 15671587.CrossRefGoogle ScholarPubMed
Feige, G. B., Lumbsch, T. H., Huneck, S. & Elix, J. A. (1993) The identification of lichen substances by a standardized liquid chromatographic method. Journal of Chromatography 646: 417427.CrossRefGoogle Scholar
Fernández-Mendoza, F. & Printzen, C. (2013) Pleistocene expansion of the bipolar lichen Cetraria aculeata into the Southern Hemisphere. Molecular Ecology 22: 19611983.CrossRefGoogle ScholarPubMed
Fernández-Mendoza, F., Domaschke, S., García, M. A., Jordan, P., Martin, M. P. & Printzen, C. (2011) Population structure of mycobionts and photobionts of the widespread lichen Cetraria aculeata . Molecular Ecology 20: 12081232.CrossRefGoogle ScholarPubMed
Fletcher, A., James, P. W. & Purvis, O. W. (2009) Ramalina . In The Lichens of Great Britain and Ireland (C. W. Smith, A. Aptroot, B. J. Coppins, A. Fletcher, O. L. Gilbert, P. W. James & P. A. Wolseley, eds): 781787. London: British Lichen Society.Google Scholar
Fritz, S. A. & Purvis, A. (2010) Selectivity in mammalian extinction risk and threat types: a new measure of phylogenetic signal strength in binary traits. Conservation Biology 24 : 10421051.CrossRefGoogle ScholarPubMed
Gerritsen, H. (2012) mapplots: data visualisation on maps. R package version 1.5. R-project website. Available at: http://cran.r-project.org/package=mapplots.Google Scholar
Hale, M. E. (1956) Chemical strains of the lichen Parmelia furfuracea . American Journal of Botany 43: 456459.CrossRefGoogle Scholar
Hale, M. E. (1963) Populations of chemical strains in the lichen Cetraria ciliaris . Brittonia 15: 126133.CrossRefGoogle Scholar
Hauck, M., Jurgens, S. R. & Leuschner, C. (2010) Norstictic acid: correlations between its physico-chemical characteristics and ecological preferences of lichens producing this depsidone. Environmental and Experimental Botany 68: 309313.CrossRefGoogle Scholar
Hebert, P. D. N., Cywinska, A., Ball, S. L. & deWaard, J. R. (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London, Series B 270: 313321.CrossRefGoogle ScholarPubMed
Heinken, T. (1999) Dispersal patterns of terricolous lichens by thallus fragments. Lichenologist 31: 603612.CrossRefGoogle Scholar
Hibbett, D. S., Binder, M., Bischoff, J. F., Blackwell, M., Cannon, P. F., Eriksson, O. E., Huhndorf, S., James, T., Kirk, P. M., Lücking, R. et al. (2007) A higher-level phylogenetic classification of the Fungi. Mycological Research 111: 509547.CrossRefGoogle ScholarPubMed
Jakobsson, M. & Rosenberg, N. A. (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23: 18011806.CrossRefGoogle ScholarPubMed
Kärnefelt, I. (1986) The genera Bryocaulon, Coelocaulon and Cornicularia and formerly associated taxa. Opera Botanica 86: 190.Google Scholar
Kelly, L. J., Hollingsworth, P. M., Coppins, B. J., Ellis, C. J., Harrold, P., Tosh, J. & Yahr, R. (2011) DNA barcoding of lichenized fungi demonstrates high identification success in a floristic context. New Phytologist 191: 288300.CrossRefGoogle Scholar
Knoph, J. G., Schmidt, R. & Elix, J. A. (1995) Untersuchungen einiger Arten der Gattung Lecidella mit Hochdruckflüssigkeitschromatographie unter besonderer Berücksichtigung von epiphytischen Proben. Bibliotheca Lichenologica 57: 307326.Google Scholar
Kroken, S. & Taylor, J. W. (2001) A gene genealogical approach to recognize phylogenetic species boundaries in the lichenized fungus Letharia . Mycologia 93: 3853.CrossRefGoogle Scholar
Leavitt, S. D., Johnson, L. & St. Clair, L. L. (2011) Species delimitation and evolution in morphologically and chemically diverse communities of the lichen-forming genus Xanthoparmelia (Parmeliaceae, Ascomycota) in western North America. American Journal of Botany 98: 175188.CrossRefGoogle ScholarPubMed
Lendemer, J. C., Allen, J. L. & Noell, N. (2015) The Parmotrema acid test: a look at species delineation in the P. perforatum group 40 y later. Mycologia 107: 11201129.CrossRefGoogle Scholar
Lohtander, K., Myllys, L., Källersjö, M., Moberg, R., Stenroos, S. & Tehler, A. (2009) New entities in Physcia aipoliaP. caesia group (Physciaceae, Ascomycetes): an analysis based on mtSSU, ITS, group I intron and betatubulin sequences. Annales Botanici Fennici 46: 4353.CrossRefGoogle Scholar
Lücking, R., Dal-Forno, M., Sikaroodi, M., Gillevet, P. M., Bungartz, F., Moncada, B., Yánez-Ayabaca, A., Chaves, J. L., Coca, L. F. & Lawrey, J. D. (2014) A single macrolichen constitutes hundreds of unrecognized species. Proceedings of the National Academy of Sciences of the United States of America 111: 1109111096.CrossRefGoogle ScholarPubMed
Lumbsch, H. T. (1998) Taxonomic use of metabolic data in lichen-forming fungi. In Chemical Fungal Taxonomy (J. D. Frisvad, P. D. Bridge & D. K. Arora, eds): 345387. New York: Marcel Dekker.Google Scholar
Lumbsch, H. T. & Leavitt, S. D. (2011) Goodbye morphology? A paradigm shift in the delimitation of species in lichenized fungi. Fungal Diversity 50: 5972.CrossRefGoogle Scholar
Lumbsch, H. T., Feige, G. B. & Elix, J. A. (1994) Chemical variation in two species of the Lecanora subfusca group (Lecanoraceae, lichenized Ascomycotina). Plant Systematics and Evolution 191: 227236.CrossRefGoogle Scholar
Lumbsch, H., Schmitt, I., Barker, D. & Pagel, M. (2006) Evolution of micromorphological and chemical characters in the lichen-forming fungal family Pertusariaceae . Biological Journal of the Linnean Society 89: 615626.CrossRefGoogle Scholar
Lumbsch, H. T., Ahti, T., Altermann, S., Amo de Paz, G., Aptroot, A., Arup, U., Bárcenas Peña, A., Bawingan, P. A., Benatti, M. N., Betancourt, L. et al. (2011) One hundred new species of lichenized fungi: a signature of undiscovered global diversity. Phytotaxa 18: 1127.CrossRefGoogle Scholar
Lutsak, T., Fernández-Mendoza, F., Kirika, P., Wondafrash, M. & Printzen, C. (2015) Mycobiont-photobiont interactions of the lichen Cetraria aculeata in high alpine regions of East Africa and South America. Symbiosis 68: 2537.CrossRefGoogle Scholar
Mereschkowsky, C. (1921) Diagnoses of some lichens. Annals and Magazine of Natural History, Series 9 8: 246290.CrossRefGoogle Scholar
Muggia, L., Pérez-Ortega, S., Fryday, A., Spribille, T. & Grube, M. (2013) Global assessment of genetic variation and phenotypic plasticity in the lichen-forming species Tephromela atra . Fungal Diversity 64: 233251.CrossRefGoogle Scholar
Myllys, L., Högnabba, F., Lohtander, K., Thell, A., Stenroos, S. & Hyvönen, J. (2005) Phylogenetic relationships of Stereocaulaceae based on simultaneous analysis of beta-tubulin, GAPDH and SSU rDNA sequences. Taxon 54: 605618.CrossRefGoogle Scholar
Nadyeina, O., Lutsak, T., Blum, O., Grakhov, V. & Scheidegger, C. (2013) Cetraria steppae Savicz is conspecific with Cetraria aculeata (Schreb.) Fr. according to morphology, secondary chemistry and ecology. Lichenologist 45: 841856.CrossRefGoogle Scholar
Nash, T. H. III & Zavada, M. (1977) Population studies among Sonoran Desert species of Parmelia subg. Xanthoparmelia (Parmeliaceae). Americal Journal of Botany 64: 664669.CrossRefGoogle Scholar
Nelsen, M. P. & Gargas, A. (2008) Phylogenetic distribution and evolution of secondary metabolites in the lichenized fungal genus Lepraria (Lecanorales: Stereocaulaceae). Nova Hedwigia 86: 115132.CrossRefGoogle Scholar
Nelsen, M. P. & Gargas, A. (2009) Assessing clonality and chemotype monophyly in Thamnolia (Icmadophilaceae). Bryologist 112: 4253.CrossRefGoogle Scholar
Nützmann, H.-W., Reyes-Dominguez, Y., Scherlach, K., Schroeckh, V., Horn, F., Gacek, A., Schümann, J., Hertweck, C., Strauss, J. & Brakhage, A. A. (2011) Bacteria-induced natural product formation in the fungus Aspergillus nidulans requires Saga/Ada-mediated histone acetylation. Proceedings of the National Academy of Sciences of the United States of America 108: 1428214287.CrossRefGoogle ScholarPubMed
Nylander, W. (1866) Hypochlorite of lime and hydrate of potash, two new criteria in the study of lichens. Botanical Journal of the Linnaean Society 9: 358365.CrossRefGoogle Scholar
Orange, A., James, P. W. & White, F. J. (2001) Microchemical Methods for the Identification of Lichens. London: British Lichen Society.Google Scholar
Palice, Z. & Printzen, C. (2004) Genetic variability in tropical and temperate populations of Trapeliopsis glaucolepidea: evidence against long-range dispersal in a lichen with disjunct distribution. Mycotaxon 90: 4354.Google Scholar
Parnmen, S., Rangsiruji, A., Mongkolsuk, P. & Boonpragob, K. (2011) Using phylogenetic and coalescent methods to understand the species diversity in the Cladia aggregata complex (Ascomycota, Lecanorales). PLoS ONE 7: 115.Google Scholar
Pérez-Ortega, S., Fernández-Mendoza, F., Raggio, J., Vivas, M., Ascaso, C., Sancho, L. G., Printzen, C. & de los Ríos, A. (2012) Extreme phenotypic variation in Cetraria aculeata (lichenized Ascomycota): adaptation or incidental modification? Annals of Botany 109: 11331148.CrossRefGoogle ScholarPubMed
Pino-Bodas, R., Burgaz, A. R., Martin, M. P. & Lumbsch, H. T. (2011) Phenotypical plasticity and homoplasy complicate species delimitation in the Cladonia gracilis group (Cladoniaceae, Ascomycota). Organisms Diversity and Evolution 11: 343355.CrossRefGoogle Scholar
Pintado, A., Valladares, F. & Sancho, L. G. (1997) Exploring phenotypic plasticity in the lichen Ramalina capitata: morphology, water relations and chlorophyll content in north- and south-facing populations. Annals of Botany 80: 345353.CrossRefGoogle Scholar
Poelt, J. (1969) Bestimmungsschlüssel Europäischer Flechten. Lehre: Verlag J. Cramer.Google Scholar
Posada, D. (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25: 12531256.CrossRefGoogle ScholarPubMed
Printzen, C. (2010) Lichen systematics: the role of morphological and molecular data to reconstruct phylogenetic relationships. Progress in Botany 71: 233275.Google Scholar
Printzen, C., Ekman, S. & Tonsberg, T. (2003) Phylogeography of Cavernularia hultenii: evidence of slow genetic drift in a widely disjunct lichen. Molecular Ecology 12: 14731486.CrossRefGoogle Scholar
Printzen, C., Domaschke, S., Fernández-Mendoza, F. & Pérez-Ortega, S. (2013) Biogeography and ecology of Cetraria aculeata, a widely distributed lichen with a bipolar distribution. MycoKeys 6: 3353.CrossRefGoogle Scholar
Pritchard, J. K., Stephens, M. & Donnelly, P. J. (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945959.CrossRefGoogle ScholarPubMed
Randlane, T. & Saag, A. (2006) Cetrarioid lichens in Europe – an identification key for the species. In Central European Lichens – Diversity and Threat (A. Lackovičová, A. Guttová, E. Lisická & P. Lizoň, eds): 7584. Ithaca: Mycotaxon Ltd.Google Scholar
Savicz, V. (1924) De lichene terrestri novo Cornicularia steppae mihi nec non lichene Cornicularia tenuissima . Notulae Systematicae ex Instituto Cryptogamico Horti Botanici Petropol 3: 185188.Google Scholar
Schmitt, I. & Lumbsch, H. T. (2004) Molecular phylogeny of the Pertusariaceae supports secondary chemistry as an important systematic character set in lichen-forming ascomycetes. Molecular Phylogenetics and Evolution 33: 4355.CrossRefGoogle ScholarPubMed
Schoch, C. L., Sung, G., Lopez-Giraldez, F., Townsend, J. P., Miadlikowska, J., Hofstetter, V., Robbertse, B., Matheny, P. B., Kauff, F., Wang, Z. et al. (2009) The Ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. Systematic Biology 58: 224239.CrossRefGoogle ScholarPubMed
Schroeckh, V., Scherlach, K., Nützmann, H.-W., Shelest, E., Schmidt-Heck, W., Schuemann, J., Martin, K., Hertweck, C. & Brakhage, A. A. (2009) Intimate bacterial-fungal interaction triggers biosynthesis of archetypal polyketides in Aspergillus nidulans . Proceedings of the National Academy of Sciences of the United States of America 106: 1455814563.CrossRefGoogle ScholarPubMed
Sheard, J. W. (1977) Paleogeography, chemistry and taxonomy of the lichenized ascomycetes Dimelaena and Thamnolia . Bryologist 80: 100118.CrossRefGoogle Scholar
Skult, H. (1993) Notes on the status of Parmelia delisei versus P. pulla and their distribution in Finland. Graphis Scripta 5: 8791.Google Scholar
South, A. (2011) rworldmap: a new R package for mapping global data. The R Journal 3: 3543.CrossRefGoogle Scholar
Spribille, T., Klug, B. & Mayrhofer, H. (2011) A phylogenetic analysis of the boreal lichen Mycoblastus sanguinarius (Mycoblastaceae, lichenized Ascomycota) reveals cryptic clades correlated with fatty acid profiles. Molecular Phylogenetics and Evolution 59: 603614.CrossRefGoogle ScholarPubMed
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28: 27312739.CrossRefGoogle ScholarPubMed
Tehler, A. & Källersjö, M. (2001) Parmeliopsis ambigua and P. hyperopta (Parmeliaceae): species or chemotypes? Lichenologist 33: 403408.CrossRefGoogle Scholar
Thell, A., Stenroos, S., Feuerer, T., Kärnefelt, I., Myllys, L. & Hyvönen, J. (2002) Phylogeny of cetrarioid lichens (Parmeliaceae) inferred from ITS and b-tubulin sequences, morphology, anatomy and secondary chemistry. Mycological Progress 1: 335354.CrossRefGoogle Scholar
Thell, A., Högnabba, F., Elix, J. A., Feuerer, T., Kärnefelt, I., Myllys, L., Randlane, T., Saag, A., Stenroos, S., Ahti, T. et al. (2009) Phylogeny of the cetrarioid core (Parmeliaceae) based on five genetic markers. Lichenologist 41: 489511.CrossRefGoogle Scholar
Velmala, S., Myllys, L., Halonen, P., Goward, T. & Ahti, T. (2009) Molecular data show that Bryoria fremontii and B. tortuosa (Parmeliaceae) are conspecific. Lichenologist 41: 231242.CrossRefGoogle Scholar
Werth, S. & Sork, V. L. (2008) Local genetic structure in a North American epiphitic lichen, Ramalina menziesii (Ramalinaceae). Americal Journal of Botany 95: 568576.CrossRefGoogle Scholar
Wirtz, N., Printzen, C. & Lumbsch, H. T. (2012) Using haplotype networks, estimation of gene flow and phenotypic characters to understand species delimitation in fungi of a predominantly Antarctic Usnea group (Ascomycota, Parmeliaceae). Organisms Diversity and Evolution 12: 1737.CrossRefGoogle Scholar
Zoller, S., Lutzoni, F. & Scheidegger, C. (1999) Genetic variation within and among populations of the threatened lichen Lobaria pulmonaria in Switzerland and implications for its conservation. Molecular Ecology 8: 20492059.CrossRefGoogle ScholarPubMed