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Polymorphic fungus-specific microsatellite markers of Bactrospora dryina reveal multiple colonizations of trees

Published online by Cambridge University Press:  14 November 2017

Olga NADYEINA ,
Daria ZARABSKA-BOŻEJEWICZ ,
Andrea WIEDMER ,
Carolina CORNEJO  and
Christoph SCHEIDEGGER
Olga NADYEINA
Affiliation:
Biodiversity and Conservation Biology, Swiss Federal Institute for Forest, Snow and Landscape Research, WSL, Zürcherstr. 111, CH-8903 Birmensdorf, Switzerland. Email: [email protected]
Daria ZARABSKA-BOŻEJEWICZ
Affiliation:
Biodiversity and Conservation Biology, Swiss Federal Institute for Forest, Snow and Landscape Research, WSL, Zürcherstr. 111, CH-8903 Birmensdorf, Switzerland. Email: [email protected] Institute of Agricultural and Forest Environment, Polish Academy of Sciences, ul. Bukowska 19, 60-809 Poznań, Poland
Andrea WIEDMER
Affiliation:
Biodiversity and Conservation Biology, Swiss Federal Institute for Forest, Snow and Landscape Research, WSL, Zürcherstr. 111, CH-8903 Birmensdorf, Switzerland. Email: [email protected]
Carolina CORNEJO
Affiliation:
Biodiversity and Conservation Biology, Swiss Federal Institute for Forest, Snow and Landscape Research, WSL, Zürcherstr. 111, CH-8903 Birmensdorf, Switzerland. Email: [email protected]
Christoph SCHEIDEGGER
Affiliation:
Biodiversity and Conservation Biology, Swiss Federal Institute for Forest, Snow and Landscape Research, WSL, Zürcherstr. 111, CH-8903 Birmensdorf, Switzerland. Email: [email protected]
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Abstract

Bactrospora dryina is an epiphytic lichen-forming fungus specifically related to old-growth floodplain forests, which have dramatically declined in Europe over the past centuries. In order to promote conservation management of such forest remnants, we aimed to study population genetics of this rare and threatened lichen. The newly developed 16 microsatellite markers are specific for the mycobiont of B. dryina and reliably amplify either single fruiting bodies or a sterile thallus. This allows the use of these markers for the identification of sterile crusts and for quantification of recent dispersal of the species into restored habitats. We tested the markers in 264 samples collected from 10 pedunculate oak trees growing in three localities in north-eastern Switzerland. All markers were polymorphic and showed two to five alleles per locus, and unbiased gene diversity varied from 0·06 to 0·71 over three populations. The relatively low number of alleles in B. dryina is possibly the consequence of colonization of secondary habitats created by forest management. Although oaks were largely covered with a single, continuous B. dryina colony, the microsatellite markers identified single or complex multi-genotype colonizations per tree. For future population genetic studies, we recommend collection of 5–15 specimens from one tree which would enable detection of 60–80% of the multilocus genotypes present. Hierarchical AMOVA revealed high variation (70%) on host trees, and a relatively high differentiation (12%) among the three locations in NE Switzerland indicated limited gene flow between those regions. Thus, the newly developed markers showed their applicability in population genetics at different spatial scales. They will play an important role in monitoring habitat restoration for the conservation of B. dryina and associated forests and riverscapes.

Keywords

Ascomycetesepiphytic lichengenetic differentiationmolecular species identificationrare speciesTrentepohlia
Type
Articles
Information
The Lichenologist , Volume 49 , Issue 6 , November 2017 , pp. 561 - 577
Copyright
© British Lichen Society, 2017 

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References

Baloch, E. & Grube, M. (2009) Pronounced genetic diversity in tropical epiphyllous lichen fungi. Molecular Ecology 18: 2185–2197.CrossRefGoogle ScholarPubMed
Belinchón, R., Martínez, I., Aragón, G., Escudero, A. & De la Cruz, M. (2011) Fine spatial pattern of an epiphytic lichen species is affected by habitat conditions in two forest types in the Iberian Mediterranean region. Fungal Biology 115: 1270–1278.Google Scholar
Belinchón, R., Ellis, C. J. & Yahr, R. (2014) Microsatellite loci in two epiphytic lichens with contrasting dispersal modes: Nephroma laevigatum and N. parile (Nephromataceae). Applications in Plant Sciences 2: 1400080.Google Scholar
Cieśliński, S., Czyżewska, K. & Fabiszewski, J. (2006) Red list of the lichens in Poland. In Red List of Plants and Fungi in Poland (Z. Mirek, K. Zarzycki, W. Wojewoda & Z. Szeląg, eds): 71–89. Kraków: W. Szafer Institute of Botany, Polish Academy of Sciences.Google Scholar
Cutter, A. D. (2006) Nucleotide polymorphism and linkage disequilibrium in wild populations of the partial selfer Caenorhabditis elegans . Genetics 172: 171–184.CrossRefGoogle ScholarPubMed
DePriest, P. (1993) Variation in the Cladonia chlorophaea complex I: morphological and chemical variation in Southern Appalachian populations. Bryologist 96: 555–563.Google Scholar
Devkota, S., Cornejo, C., Werth, S., Chaudhary, R. P. & Scheidegger, C. (2014) Characterization of microsatellite loci in the Himalayan lichen fungus Lobaria pindarensis (Lobariaceae). Applications in Plant Sciences 2: 1300101.CrossRefGoogle ScholarPubMed
Egea, J. M. & Torrente, P. (1993) The lichen genus Bactrospora . Lichenologist 25: 211–255.CrossRefGoogle Scholar
Excoffier, L., Laval, G. & Schneider, S. (2005) ARLEQUIN (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1: 47–50.Google Scholar
Faircloth, B. C. (2008) MSATCOMMANDER: detection of microsatellite repeat arrays and automated, locus‐specific primer design. Molecular Ecology Resources 8: 92–94.CrossRefGoogle ScholarPubMed
Gjerde, I., Blom, H. H., Heegaard, E. & Sætersdal, M. (2015) Lichen colonization patterns show minor effects of dispersal distance at landscape scale. Ecography 38: 939–948.CrossRefGoogle Scholar
Groom, M. J., Meffe, G. K. & Carroll, C. R. (2006) Principles of Conservation Biology. Third Edition. Sunderland, Massachusetts: Sinauer Associates.Google Scholar
Guzow-Krzemińska, B. & Stocker-Wörgötter, E. (2013) Development of microsatellite markers in Protoparmeliopsis muralis (lichenized Ascomycete) – a common lichen species. Lichenologist 45: 791–798.Google Scholar
Hedenås, H., Bolyukh, V. O. & Jonsson, B. G. (2003) Spatial distribution of epiphytes on Populus tremula in relation to dispersal mode. Journal of Vegetation Science 14: 233–242.CrossRefGoogle Scholar
Hilfiker, H. (2000) Bactrospora dryina – eine seltene Flechte an alten Eichen. Mitteilungen der Thurgauischen Naturforschenden Gesellschaft 56: 7–14.Google Scholar
Hilmo, O., Rocha, L., Holien, H. & Gauslaa, Y. (2011) Establishment success of lichen diaspores in young and old boreal rainforests: a comparison between Lobaria pulmonaria and L. scrobiculata . Lichenologist 43: 241–255.Google Scholar
Hsieh, T., Ma, K. & Chao, A. (2016) iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods in Ecology and Evolution 7: 1451–1456.Google Scholar
Kamvar, Z. N., Tabima, J. F. & Grünwald, N. J. (2014) Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2: e281.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
Küster, H. (1998) Geschichte des Waldes: Von der Urzeit bis zur Gegenwart . München: C. H. Beck.Google Scholar
Laundon, J. (1978) Haematomma chemotypes form fused thalli. Lichenologist 10: 221–225.CrossRefGoogle Scholar
Löbel, S., Snäll, T. & Rydin, H. (2006) Species richness patterns and metapopulation processes – evidence from epiphyte communities in boreo-nemoral forests. Ecography 29: 169–182.Google Scholar
Mansournia, M. R., Bingyun, W., Matsushita, N. & Hogetsu, T. (2012) Genotypic analysis of the foliose lichen Parmotrema tinctorum using microsatellite markers: association of mycobiont and photobiont, and their reproductive modes. Lichenologist 44: 419–440.Google Scholar
Motiejünaite, J., Czyzewska, K. & Cieśliński, S. (2004) Lichens – indicators of old-growth forests in biocentres of Lithuania and North-East Poland. Botanica Lithuanica 10: 59–74.Google Scholar
Murtagh, G. J., Dyer, P. S. & Crittenden, P. D. (2000) Reproductive systems: sex and the single lichen. Nature 404: 564.CrossRefGoogle Scholar
Nadyeina, O., Cornejo, C., Boluda, C. G., Myllys, L., Rico, V. J., Crespo, A. & Scheidegger, C. (2014 a) Characterization of microsatellite loci in lichen-forming fungi of Bryoria section Implexae (Parmeliaceae). Applications in Plant Sciences 2: 1400037.CrossRefGoogle ScholarPubMed
Nadyeina, O., Dymytrova, L., Naumovych, A., Postoyalkin, S., Werth, S., Cheenacharoen, S. & Scheidegger, C. (2014 b) Microclimatic differentiation of gene pools in the Lobaria pulmonaria symbiosis in a primeval beech landscape. Molecular Ecology 23: 5164–5178.Google Scholar
Naiman, R. J., Décamps, H. & McClain, M. E. (2005) Riparia: Ecology, Conservation, and Management of Streamside Communities. Amsterdam: Elsevier.Google Scholar
Nordborg, M. (2000) Linkage disequilibrium, gene trees and selfing: an ancestral recombination graph with partial self-fertilization. Genetics 154: 923–929.CrossRefGoogle ScholarPubMed
Nyland, R. D. (1996) Silviculture: Concepts and Applications. Long Grove, Illinois: Waveland Press.Google Scholar
Pasinelli, G., Weggler, M. & Mulhauser, B. (2008) Aktionsplan Mittelspecht Schweiz. Artenförderung Vögel Schweiz. Umwelt-Vollzug Nr. 0805. Bern, Sempach & Zürich: Bundesamt für Umwelt, Schweizerische Vogelwarte, Schweizer Vogelschutz SVS/BirdLife Schweiz.Google Scholar
Piercey-Normore, M. D. & DePriest, P. T. (2001) Algal switching among lichen symbioses. American Journal of Botany 88: 1490–1498.Google Scholar
Prieto, M., Romera, L., Merinero, S., Aragón, G. & Martínez, I. (2015) Development and characterization of fungal specific microsatellite markers in the lichen Lobarina scrobiculata (Lobariaceae, Ascomycota). Lichenologist 47: 183–186.Google Scholar
Prigodina-Lukošienė, I. & Naujalis, J. (2009) Rare lichen associations on common oak (Quercus robur) in Lithuania. Biologia 64: 48–52.Google 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: 399–406.Google Scholar
R Core Team (2014) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. URL: http://www.R-project.org/ Google Scholar
Ranius, T., Niklasson, M. & Berg, N. (2009) Development of tree hollows in pedunculate oak (Quercus robur). Forest Ecology and Management 257: 303–310.Google Scholar
Rois-Diaz, M., Mosquera-Losada, R. & Rigueiro-Rodriguez, A. (2006) Biodiversity indicators on silvopastoralism across Europe. EFI Technical Report 21. Helsinki: European Forest Institute.Google Scholar
Rozen, S. & Skaletsky, H. (1999) Primer3 on the WWW for general users and for biologist programmers. In Bioinformatics: Methods and Protocols. Methods in Molecular Biology Vol. 132 (S. Misener & S. A. Krawetz, eds): 365–386. Totowa, New Jersey: Humana Press.Google Scholar
Scheidegger, C. & Werth, S. (2009) Conservation strategies for lichens: insights from population biology. Fungal Biology Reviews 23: 55–66.Google Scholar
Scheidegger, C., Groner, U., Keller, C. & Stofer, S. (2002) Biodiversity assessment tools – lichens. In Monitoring With Lichens – Monitoring Lichens (P. L. Nimis, P. Wolseley & C. Scheidegger, eds): 359–365. Dordrecht: Kluwer Academic Publishers.Google Scholar
Scheidegger, C., Bilovitz, P. O., Werth, S., Widmer, I. & Mayrhofer, H. (2012) Hitchhiking with forests: population genetics of the epiphytic lichen Lobaria pulmonaria in primeval and managed forests in southeastern Europe. Ecology and Evolution 2: 2223–2240.CrossRefGoogle ScholarPubMed
Scheidegger, C., Ziegler, M. & Helbling, L. (2014) Artenförderung per Transplantation. Pro Natura Magazin 1: 32–33.Google Scholar
Scherzinger, W. (1996) Naturschutz im Wald. Qualitätsziele Einer Dynamischen Waldentwicklung (Praktischer Naturschutz). Stuttgart: Eugen Ulmer KG.Google Scholar
Schuelke, M. (2000) An economic method for the fluorescent labeling of PCR fragments. Nature Biotechnology 18: 233–234.Google Scholar
Singh, G., Dal Grande, F., Cornejo, C., Schmitt, I. & Scheidegger, C. (2012) Genetic basis of self-incompatibility in the lichen-forming fungus Lobaria pulmonaria and skewed frequency distribution of mating-type idiomorphs: implications for conservation. PLoS ONE 7: e51402.CrossRefGoogle ScholarPubMed
Skult, H. (1984) The Parmelia omphalodes (Ascomycetes) complex in Eastern Fennoscandia. Annales Botanici Fennici 21: 117–142.Google Scholar
Snäll, T., Riberiro, P. J. & Rydin, H. (2003) Spatial occurrence and colonisations in patch-tracking metapopulations: local conditions versus dispersal. Oikos 103: 566–578.Google Scholar
Snäll, T., Pennanen, J., Kivistö, L. & Hanski, I. (2005) Modelling epiphyte metapopulation dynamics in a dynamic forest landscape. Oikos 109: 209–222.Google Scholar
Sork, V. L. & Werth, S. (2014) Phylogeography of Ramalina menziesii, a widely distributed lichen-forming fungus in western North America. Molecular Ecology 23: 2326–2339.Google Scholar
Speich, D. (2002) Linth Kanal: Die Korrigierte Landschaft– 200 Jahre Geschichte. Glarus: Baeschlin.Google Scholar
Tockner, K. & Stanford, J. A. (2002) Riverine flood plains: present state and future trends. Environmental Conservation 29: 308–330.Google Scholar
Tõrra, T., Cornejo, C., Cheenacharoen, S., Dal Grande, F., Marmor, L. & Scheidegger, C. (2014) Characterization of fungus-specific microsatellite markers in the lichen fungus Usnea subfloridana (Parmeliaceae). Applications in Plant Sciences 2: 1400034.Google Scholar
Türk, R. & Hafellner, J. (1999) Rote Liste gefährdeter Flechten (Lichenes) Österreichs. In Rote Listen Gefährdeter Pflanzen Österreichs (H. Niklfeld, ed.): 187–228. Graz: Medien Service.Google Scholar
Wagner, H. H., Werth, S., Kalwij, J. M., Bolli, J. C. & Scheidegger, C. (2006) Modelling forest recolonization by an epiphytic lichen using a landscape genetic approach. Landscape Ecology 21: 849–865.Google Scholar
Walser, J. C., Sperisen, C., Soliva, M. & Scheidegger, C. (2003) Fungus-specific microsatellite primers of lichens: application for the assessment of genetic variation on different spatial scales in Lobaria pulmonaria . Fungal Genetics and Biology 40: 72–82.Google Scholar
Walser, J. C., Gugerli, F., Holderegger, R., Kuonen, D. & Scheidegger, C. (2004) Recombination and clonal propagation in different populations of the lichen Lobaria pulmonaria . Heredity 93: 322–329.Google Scholar
Werth, S., Wagner, H. H., Gugerli, F., Holderegger, R., Csencsics, D., Kalwij, J. M. & Scheidegger, C. (2006 a) Quantifying dispersal and establishment limitation in a population of an epiphytic lichen. Ecology 87: 2037–2046.Google Scholar
Werth, S., Wagner, H. H., Holderegger, R., Kalwij, J. M. & Scheidegger, C. (2006 b) Effect of disturbances on the genetic diversity of an old-forest associated lichen. Molecular Ecology 15: 911–921.Google Scholar
Werth, S., Cornejo, C. & Scheidegger, C. (2013) Characterization of microsatellite loci in the lichen fungus Lobaria pulmonaria (Lobariaceae). Applications in Plant Sciences 1: 1200290.CrossRefGoogle ScholarPubMed
Wickham, H. (2016) ggplot2: Elegant Graphics for Data Analysis. Dordrecht: Springer.Google Scholar
Widmer, I., Dal Grande, F., Excoffier, L., Holderegger, R., Keller, C., Mikryukov, V. S. & Scheidegger, C. (2012) European phylogeography of the epiphytic lichen fungus Lobaria pulmonaria and its green algal symbiont. Molecular Ecology 21: 5827–5844.Google Scholar
Wirth, V., Hauck, M. A., Brackel, W. von, Cezanne, R. A., De Bruyn, U., Dürhammer, O., Eichler, M., Gnüchtel, A., John, V., Litterski, B. et al. (2011) Rote Liste und Artenverzeichnis der Flechten und flechtenbewohnenden Pilze Deutschlands. Naturschutz und Biologische Vielfalt 70: 7–122.Google Scholar
Wirth, V., Hauck, M. & Schultz, M. (2013) Die Flechten Deutschlands. Stuttgart (Hohenheim): Eugen Ulmer KG.Google Scholar
Yoshimura, I., Yamamoto, Y., Nakano, T. & Finnie, J. (2002) Isolation and culture of lichen photobionts and mycobionts. In Protocols in Lichenology: Culturing, Biochemistry, Physiology and Use in Biomonitoring (I. C. Kranner, R. P. Beckett & A. K. Varma, eds): 3–33. Berlin-Heidelberg: Springer.CrossRefGoogle Scholar
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