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An Exception to the Rule? Could Photobiont Identity Be a Better Predictor of Lichen Phenotype than Mycobiont Identity?

. 2022 Mar 09 ; 8 (3) : . [epub] 20220309

Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic

Document type Journal Article

Grant support
204069 Charles University Research Centre
EEA and Norway grants 2014-2021 EEA and Norway grants 2014-2021

With rare exceptions, the shape and appearance of lichen thalli are determined by the fungal partner; thus, mycobiont identity is normally used for lichen identification. However, it has repeatedly been shown in recent decades that phenotypic data often does not correspond with fungal gene evolution. Here, we report such a case in a three-species complex of red-fruited Cladonia lichens, two of which clearly differ morphologically, chemically, ecologically and in distribution range. We analysed 64 specimens of C. bellidiflora, C. polydactyla and C. umbricola, mainly collected in Europe, using five variable mycobiont-specific and two photobiont-specific molecular markers. All mycobiont markers exhibited very low variability and failed to separate the species. In comparison, photobiont identity corresponded better with lichen phenotype and separated esorediate C. bellidiflora from the two sorediate taxa. These results can be interpreted either as an unusual case of lichen photomorphs or as an example of recent speciation, in which phenotypic differentiation precedes the separation of the molecular markers. We hypothesise that association with different photobionts, which is probably related to habitat differentiation, may have triggered speciation in the mycobiont species.

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Hawksworth D.L., Grube M. Lichens redefined as complex ecosystems. New Phytol. 2020;227:1281–1283. doi: 10.1111/nph.16630. PubMed DOI PMC

Mark K., Laanisto L., Bueno C.G., Niinemets Ü., Keller C., Scheidegger C. Contrasting co-occurrence patterns of photobiont and Cystobasidiomycete yeast associated with common epiphytic lichen species. New Phytol. 2020;227:1362–1375. doi: 10.1111/nph.16475. PubMed DOI

Grimm M., Grube M., Schiefelbein U., Zühlke D., Bernhardt J., Riedel K. The lichens’ microbiota, still a mystery? Front. Microbiol. 2021;12:714. doi: 10.3389/fmicb.2021.623839. PubMed DOI PMC

Honegger R. Lichen-forming fungi and their photobionts. In: Deising H.B., editor. Plant Relationships. Springer; Berlin/Heidelberg, Germany: 2009. pp. 307–333. The Mycota.

Honegger R. The lichen symbiosis—What is so spectacular about it? Lichenologist. 1998;30:193–212. doi: 10.1006/lich.1998.0140. DOI

Lücking R., Leavitt S.D., Hawksworth D.L. Species in lichen-forming fungi: Balancing between conceptual and practical considerations, and between phenotype and phylogenomics. Fungal Divers. 2021;109:99–154. doi: 10.1007/s13225-021-00477-7. DOI

Spribille T., Tuovinen V., Resl P., Vanderpool D., Wolinski H., Aime M.C., Schneider K., Stabentheiner E., Toome-Heller M., Thor G., et al. Basidiomycete yeasts in the cortex of ascomycete macrolichens. Science. 2016;353:488–492. doi: 10.1126/science.aaf8287. PubMed DOI PMC

Spribille T. Relative symbiont input and the lichen symbiotic outcome. Curr. Opin. Plant Biol. 2018;44:57–63. doi: 10.1016/j.pbi.2018.02.007. PubMed DOI

Moncada B., Coca L.F., Lücking R. Neotropical members of Sticta (lichenized Ascomycota: Lobariaceae) forming photosymbiodemes, with the description of seven new species. Bryologist. 2013;116:169–200. doi: 10.1639/0007-2745-116.2.169. DOI

Magain N., Goffinet B., Sérusiaux E. Further photomorphs in the lichen family Lobariaceae from Reunion (Mascarene archipelago) with notes on the phylogeny of Dendriscocaulon cyanomorphs. Bryologist. 2012;115:243–254. doi: 10.1639/0007-2745-115.2.243. DOI

Goffinet B., Bayer R.J. Characterization of mycobionts of photomorph pairs in the Peltigerineae (lichenized Ascomycetes) based on internal transcribed spacer sequences of the nuclear ribosomal DNA. Fungal Genet. Biol. 1997;21:228–237. doi: 10.1006/fgbi.1997.0977. PubMed DOI

Wirtz N., Printzen C., Lumbsch H.T. Using haplotype networks, estimation of gene flow and phenotypic characters to understand species delimitation in fungi of a predominantly Antarctic Usnea group (Ascomycota, Parmeliaceae) Org. Divers. Evol. 2012;12:17–37. doi: 10.1007/s13127-011-0066-y. DOI

Fryday A.M., Schmitt I., Pérez-Ortega S. The genus Endocena (Icmadophilaceae): DNA evidence suggests the same fungus forms different morphologies. Lichenologis. 2017;49:347–363. doi: 10.1017/S0024282917000317. DOI

Mark K., Saag L., Leavitt S.D., Will-Wolf S., Nelsen M.P., Tõrra T., Saag A., Randlane T., Lumbsch H.T. Evaluation of traditionally circumscribed species in the lichen-forming genus Usnea, section Usnea (Parmeliaceae, Ascomycota) using a six-locus dataset. Org. Divers. Evol. 2016;16:497–524. doi: 10.1007/s13127-016-0273-7. DOI

Pino-Bodas R., Sanderson N., Cannon P., Aptroot A., Coppins B., Orange A., Simkin J. Lecanorales: Cladoniaceae, including the genera Cladonia, Pilophorus and Pycnothelia. Revis. Br. Ir. Lichens. 2021;19:1–45.

Ahti T., Stenroos S., Moberg R. Nordic Lichen Flora, Volume 5: Cladoniaceae. Museum of Evolution, Uppsala University of behalf of Nordic Lichen Society; Göteborg, Sweden: 2013.

Tønsberg T., Ahti T. Cladonia umbricola, a new lichen species from NW Europe and Western North America. Nor. J. Bot. 1980;27:307–309.

Orange A., James P.W., White F.J. Microchemical Methods for the Identification of Lichens. Twayne Publishers; Woodbridge, CT, USA: 2001.

Pino-Bodas R., Martín M.P., Burgaz A.R., Lumbsch H.T. Species delimitation in Cladonia (Ascomycota): A challenge to the dna barcoding philosophy. Mol. Ecol. Resour. 2013;13:1058–1068. doi: 10.1111/1755-0998.12086. PubMed DOI

Kanz B., von Brackel W., Cezanne R., Eichler M., Hohmann M.-L., Teuber D., Printzen C. DNA barcodes for the distinction of reindeer lichens: A case study using Cladonia rangiferina and C. stygia. Herzogia. 2015;28:445–464. doi: 10.13158/heia.28.2.2015.445. DOI

Stielow J.B., Lévesque C.A., Seifert K.A., Meyer W., Iriny L., Smits D., Renfurm R., Verkley G.J.M., Groenewald M., Chaduli D., et al. One fungus, which genes? Development and assessment of universal primers for potential secondary fungal dna barcodes. Persoonia. 2015;35:242–263. doi: 10.3767/003158515X689135. PubMed DOI PMC

Printzen C., Ekman S. Local population subdivision in the lichen Cladonia subcervicornis as revealed by mitochondrial cytochrome oxidase subunit 1 intron sequences. Mycologia. 2003;95:399–406. doi: 10.2307/3761881. PubMed DOI

Stenroos S., Pino-Bodas R., Hyvönen J., Lumbsch H.T., Ahti T. Phylogeny of the family Cladoniaceae (Lecanoromycetes, Ascomycota) based on sequences of multiple loci. Cladistics. 2019;35:351–384. doi: 10.1111/cla.12363. PubMed DOI

Yahr R., Vilgalys R., DePriest P.T. Geographic variation in algal partners of Cladonia subtenuis (Cladoniaceae) highlights the dynamic nature of a lichen symbiosis. New Phytol. 2006;171:847–860. doi: 10.1111/j.1469-8137.2006.01792.x. PubMed DOI

Osyczka P., Lenart-Boroń A., Boroń P., Rola K. Lichen-forming fungi in postindustrial habitats involve alternative photobionts. Mycologia. 2021;113:43–55. doi: 10.1080/00275514.2020.1813486. PubMed DOI

Pino-Bodas R., Stenroos S. Global biodiversity patterns of the photobionts associated with the genus Cladonia (Lecanorales, Ascomycota) Microb. Ecol. 2021;82:173–187. doi: 10.1007/s00248-020-01633-3. PubMed DOI PMC

Yahr R., Vilgalys R., Depriest P.T. Strong fungal specificity and selectivity for algal symbionts in florida scrub Cladonia lichens. Mol. Ecol. 2004;13:3367–3378. doi: 10.1111/j.1365-294X.2004.02350.x. PubMed DOI

Škaloud P., Peksa O. Evolutionary inferences based on ITS RDNA and actin sequences reveal extensive diversity of the common lichen alga Asterochloris (Trebouxiophyceae, Chlorophyta) Mol. Phylogenet. Evol. 2010;54:36–46. doi: 10.1016/j.ympev.2009.09.035. PubMed DOI

Cubero O.F., Crespo A., Fatehi J., Bridge P.D. DNA extraction and PCR amplification method suitable for fresh, herbarium-stored, lichenized, and other fungi. Plant Syst. Evol. 1999;216:243–249. doi: 10.1007/BF01084401. DOI

Gardes M., Bruns T. ITS Primers with enhanced specificity for Basidiomycetes—Application to the identification of mycorrhizae and rusts. Mol. Ecol. 1993;2:113–118. doi: 10.1111/j.1365-294X.1993.tb00005.x. PubMed DOI

White T.J., Bruns T., Lee S.J.W.T., Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M.A., Gelfand D.H., Sninsky J.J., White T.J., editors. PCR Protocols: A Guide to Methods and Applications. Academic Press; San Diego, CA, USA: 1990. pp. 315–322.

Zoller S., Scheidegger C., Sperisen C. PCR primers for the amplification of mitochondrial small subunit ribosomal DNA of lichen-forming Ascomycetes. Lichenologist. 1999;31:511–516. doi: 10.1006/lich.1999.0220. DOI

Zhou S., Stanosz G.R. Primers for amplification of mtSSU rDNA, and a phylogenetic study of Botryosphaeria and associated anamorphic fungi. Mycol. Res. 2001;105:1033–1044. doi: 10.1016/S0953-7562(08)61965-6. DOI

Kroken S., Taylor J.W. Phylogenetic species, reproductive mode, and specificity of the green alga Trebouxia forming lichens with the fungal genus Letharia. Bryologist. 2000;103:645–660. doi: 10.1639/0007-2745(2000)103[0645:PSRMAS]2.0.CO;2. DOI

Cocquyt E., Verbruggen H., Leliaert F., De Clerck O. Evolution and cytological diversification of the green seaweeds (Ulvophyceae) Mol. Biol. Evol. 2010;27:2052–2061. doi: 10.1093/molbev/msq091. PubMed DOI

Hepperle D. SeqAssem. A Sequence Analysis Tool, Contig Assembler and Trace Data Visualization Tool for Molecular Sequences. 2004. [(accessed on 25 November 2021)]. Available online: http://www.sequentix.de.

Kumar S., Stecher G., Tamura K. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 2016;33:1870–1874. doi: 10.1093/molbev/msw054. PubMed DOI PMC

Katoh K., Misawa K., Kuma K., Miyata T. MAFFT: A novel method for rapid multiple sequence alignment based on fast fourier transform. Nucleic Acids Res. 2002;30:3059–3066. doi: 10.1093/nar/gkf436. PubMed DOI PMC

Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 2000;17:540–552. doi: 10.1093/oxfordjournals.molbev.a026334. PubMed DOI

Darriba D., Taboada G.L., Doallo R., Posada D. JModelTest 2: More Models, New heuristics and parallel computing. Nat. Meth. 2012;9:772. doi: 10.1038/nmeth.2109. PubMed DOI PMC

Ronquist F., Teslenko M., van der Mark P., Ayres D.L., Darling A., Höhna S., Larget B., Liu L., Suchard M.A., Huelsenbeck J.P. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 2012;61:539–542. doi: 10.1093/sysbio/sys029. PubMed DOI PMC

Stamatakis A. RAxML Version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–1313. doi: 10.1093/bioinformatics/btu033. PubMed DOI PMC

Swofford D.L. PAUP*: Phylogenetic Analysis Using Parsimony (* and Other Methods) Sinauer Associates; Sunderland, MA, USA: 2002.

Rambaut A. Figtree, a Graphical Viewer of Phylogenetic Trees. Institute of Evolutionary Biology, University of Edinburgh; Edinburgh, UK: 2018. Version 1.4.4.

Paradis E., Schliep K. Ape 5.0: An environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics. 2019;35:526–528. doi: 10.1093/bioinformatics/bty633. PubMed DOI

Pennell M.W., Eastman J.M., Slater G.J., Brown J.W., Uyeda J.C., FitzJohn R.G., Alfaro M.E., Harmon L.J. Geiger v2.0: An expanded suite of methods for fitting macroevolutionary models to phylogenetic trees. Bioinformatics. 2014;30:2216–2218. doi: 10.1093/bioinformatics/btu181. PubMed DOI

Hijmans R.J., Williams E., Vennes C., Hijmans M.R.J. Package ‘geosphere’. [(accessed on 25 November 2021)];Spherical Trigonometry. 2017 Available online: http://cran.nexr.com/web/packages/geosphere/geosphere.pdf.

Revell L.J. Phytools: An R package for phylogenetic comparative biology (and other things) Methods Ecol. Evol. 2012;3:217–223. doi: 10.1111/j.2041-210X.2011.00169.x. DOI

Chambers J.M. SoDA: Functions and examples for “Software for Data Analysis”. 2013. [(accessed on 25 November 2021)]. R Package Version. Available online: https://cran.r-project.org/web/packages/SoDA/SoDA.pdf.

Dixon P. VEGAN, a package of R functions for community ecology—Dixon—2003—Journal of Vegetation Science—Wiley Online Library. J. Veg. Sci. 2003;14:927–930. doi: 10.1111/j.1654-1103.2003.tb02228.x. DOI

Borcard D., Legendre P., Drapeau P. Partialling out the spatial component of ecological variation. Ecology. 1992;73:1045–1055. doi: 10.2307/1940179. DOI

Borcard D., Legendre P., Avois-Jacquet C., Tuomisto H. Dissecting the spatial structure of ecological data at multiple scales. Ecology. 2004;85:1826–1832. doi: 10.1890/03-3111. DOI

Hijmans R.J., Cameron S.E., Parra J.L., Jones P.G., Jarvis A. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 2005;25:1965–1978. doi: 10.1002/joc.1276. DOI

Jackson D.A. Stopping rules in principal components analysis: A comparison of heuristical and statistical approaches. Ecology. 1993;74:2204–2214. doi: 10.2307/1939574. DOI

Vančurová L., Malíček J., Steinová J., Škaloud P. Choosing the right life partner: Ecological drivers of lichen symbiosis. Front. Microbiol. 2021;12:769304. doi: 10.3389/fmicb.2021.769304. PubMed DOI PMC

Škvorová Z., Černajová I., Steinová J., Peksa O., Moya P., Škaloud P. Promiscuity in lichens follows clear rules: Partner switching in Cladonia is regulated by climatic factors and soil chemistry. Front. Microbiol. 2022;12:781585. doi: 10.3389/fmicb.2021.781585. PubMed DOI PMC

Kosecka M., Guzow-Krzemińska B., Černajová I., Škaloud P., Jabłońska A., Kukwa M. New lineages of photobionts in bolivian lichens expand our knowledge on habitat preferences and distribution of Asterochloris algae. Sci. Rep. 2021;11:8701. doi: 10.1038/s41598-021-88110-0. PubMed DOI PMC

Vančurová L., Muggia L., Peksa O., Řídká T., Škaloud P. The complexity of symbiotic interactions influences the ecological amplitude of the host: A case study in Stereocaulon (Lichenized Ascomycota) Mol. Ecol. 2018;27:3016–3033. doi: 10.1111/mec.14764. PubMed DOI

Brodo I.M., Ahti T. Lichens and lichenicolous fungi of the Queen Charlotte Islands, British Columbia, Canada. 2. The Cladoniaceae. Can. J. Bot. 1996;74:1147–1180. doi: 10.1139/b96-139. DOI

Burgaz A.R., Ahti T., Pino-Bodas R. Mediterranean Cladoniaceae. Spanish Lichen Society (SEL); Madrid, Spain: 2020.

James P.W., Cladonia P. The Lichens of Great Britain and Ireland. British Lichen Society; London, UK: 2009. Browne (1756) pp. 309–338.

Armaleo D., Clerc P. Lichen Chimeras: DNA analysis suggests that one fungus forms two morphotypes. Exp. Mycol. 1991;15:1–10. doi: 10.1016/0147-5975(91)90002-U. DOI

Nylander William Addenda nova ad Lichenographiam Europaeam Continuatio quadragesima quarta. Flora. 1865;68:295–301.

Ertz D., Guzow-Krzemińska B., Thor G., Łubek A., Kukwa M. Photobiont switching causes changes in the reproduction strategy and phenotypic dimorphism in the Arthoniomycetes. Sci. Rep. 2018;8:4952. doi: 10.1038/s41598-018-23219-3. PubMed DOI PMC

De Queiroz K. Species: New Interdisciplinary Essays. MIT Press; Cambridge, MA, USA: 1999. The General Lineage Concept of Species and the Defining Properties of the Species Category; pp. 49–89.

Leavitt S.D., Moreau C.S., Lumbsch H.T. Recent Advances in Lichenology. Springer; New Delhi, India: 2015. The dynamic discipline of species delimitation: Progress toward effectively recognizing species boundaries in natural populations; pp. 11–44.

De Queiroz K. The general lineage concept of species, species criteria, and the process of speciation. In: Howard D.J., Berlocher S.H., editors. Endless Forms: Species and Speciation. Oxford University Press; Oxford, UK: 1998. pp. 57–75.

De Queiroz K. Species concepts and species delimitation. Syst. Biol. 2007;56:879–886. doi: 10.1080/10635150701701083. PubMed DOI

Zhao X., Fernández-Brime S., Wedin M., Locke M., Leavitt S.D., Lumbsch H.T. Using multi-locus sequence data for addressing species boundaries in commonly accepted lichen-forming fungal species. Org. Divers. Evol. 2017;17:351–363. doi: 10.1007/s13127-016-0320-4. DOI

Boluda C.G., Rico V.J., Divakar P.K., Nadyeina O., Myllys L., McMullin R.T., Zamora J.C., Scheidegger C., Hawksworth D.L. Evaluating methodologies for species delimitation: The mismatch between phenotypes and genotypes in lichenized fungi (Bryoria sect. Implexae, Parmeliaceae) Pers.-Mol. Phylogeny Evol. Fungi. 2019;42:75–100. doi: 10.3767/persoonia.2019.42.04. PubMed DOI PMC

Leavitt S.D., Lumbsch H.T., Stenroos S., Clair L.L.S. Pleistocene speciation in North American lichenized fungi and the impact of alternative species circumscriptions and rates of molecular evolution on divergence estimates. PLoS ONE. 2013;8:e85240. doi: 10.1371/journal.pone.0085240. PubMed DOI PMC

Steinová J., Stenroos S., Grube M., Škaloud P. Genetic diversity and species delimitation of the zeorin-containing red-fruited Cladonia species (Lichenized Ascomycota) assessed with its rdna and β-tubulin data. Lichenologist. 2013;45:665–684. doi: 10.1017/S0024282913000297. DOI

Pino-Bodas R., Burgaz A.R., Martín M.P., Lumbsch H.T. Phenotypical plasticity and homoplasy complicate species delimitation in the Cladonia gracilis group (Cladoniaceae, Ascomycota) Org. Divers. Evol. 2011;11:343–355. doi: 10.1007/s13127-011-0062-2. DOI

Pino-Bodas R., Burgaz A.R., Ahti T., Stenroos S. Taxonomy of Cladonia angustiloba and related species. Lichenologist. 2018;50:267–282. doi: 10.1017/S002428291800018X. DOI

Pino-Bodas R., Martin M.P., Burgaz A.R. Cladonia subturgida and C. iberica (Cladoniaceae) form a single, morphologically and chemically polymorphic species. Mycol. Prog. 2012;11:269–278. doi: 10.1007/s11557-011-0746-1. DOI

Pino-Bodas R., Burgaz A.R., Martín M.P., Ahti T., Stenroos S., Wedin M., Lumbsch H.T. The phenotypic features used for distinguishing species within the Cladonia furcata complex are highly homoplasious. Lichenologist. 2015;47:287–303. doi: 10.1017/S0024282915000225. DOI

Lagostina E., Dal Grande F., Andreev M., Printzen C. The use of microsatellite markers for species delimitation in Antarctic Usnea subgenus Neuropogon. Mycologia. 2018;110:1047–1057. doi: 10.1080/00275514.2018.1512304. PubMed DOI

Grewe F., Lagostina E., Wu H., Printzen C., Lumbsch H.T. Population genomic analyses of RAD sequences resolves the phylogenetic relationship of the lichen-forming fungal species Usnea antarctica and Usnea aurantiacoatra. MycoKeys. 2018;43:91–113. doi: 10.3897/mycokeys.43.29093. PubMed DOI PMC

Seymour F.A., Crittenden P.D., Wirtz N., Øvstedal D.O., Dyer P.S., Lumbsch H.T. Phylogenetic and morphological analysis of antarctic lichen-forming Usnea species in the group Neuropogon. Antarct. Sci. 2007;19:71–82. doi: 10.1017/S0954102007000107. DOI

Stenroos S., Ahti T. The Lichen family Cladoniaceae in Tierra Del Fuego: Problematic or otherwise noteworthy taxa. Ann. Bot. Fenn. 1990;27:317–327.

Nelsen M.P., Gargas A. Assessing clonality and chemotype monophyly in Thamnolia (Icmadophilaceae) Bryologist. 2009;112:42–53. doi: 10.1639/0007-2745-112.1.42. DOI

Ortiz-Álvarez R., de los Ríos A., Fernández-Mendoza F., Torralba-Burrial A., Pérez-Ortega S. Ecological specialization of two photobiont-specific maritime cyanolichen species of the genus Lichina. PLoS ONE. 2015;10:e0132718. doi: 10.1371/journal.pone.0132718. PubMed DOI PMC

Lutsak T., Fernández-Mendoza F., Kirika P., Wondafrash M., Printzen C. Mycobiont-photobiont interactions of the lichen Cetraria aculeata in high alpine regions of East Africa and South America. Symbiosis. 2016;68:25–37. doi: 10.1007/s13199-015-0351-1. DOI

Blázquez M., Hernández-Moreno L.S., Gasulla F., Pérez-Vargas I., Pérez-Ortega S. The role of photobionts as drivers of diversification in an island radiation of lichen-forming fungi. Front. Microbiol. 2021;12:784182. doi: 10.3389/fmicb.2021.784182. PubMed DOI PMC

Hauck M., Jürgens S.-R., Brinkmann M., Herminghaus S. Surface hydrophobicity causes SO2 tolerance in lichens. Ann. Bot. 2008;101:531–539. doi: 10.1093/aob/mcm306. PubMed DOI PMC

Hamlett C.A.E., Shirtcliffe N.J., Pyatt F.B., Newton M.I., McHale G., Koch K. Passive water control at the surface of a superhydrophobic lichen. Planta. 2011;234:1267–1274. doi: 10.1007/s00425-011-1475-z. PubMed DOI

Steinová J., Škaloud P., Yahr R., Bestová H., Muggia L. reproductive and dispersal strategies shape the diversity of mycobiont-photobiont association in Cladonia lichens. Mol. Phylogenet. Evol. 2019;134:226–237. doi: 10.1016/j.ympev.2019.02.014. PubMed DOI

Cao S., Zhang F., Liu C., Hao Z., Tian Y., Zhu L., Zhou Q. distribution patterns of haplotypes for symbionts from Umbilicaria esculenta and U. muehlenbergii reflect the importance of reproductive strategy in shaping population genetic structure. BMC Microbiol. 2015;15:212. doi: 10.1186/s12866-015-0527-0. PubMed DOI PMC

Otálora M.A.G., Salvador C., Martínez I., Aragón G. Does the reproductive strategy affect the transmission and genetic diversity of bionts in cyanolichens? A case study using two closely related species. Microb. Ecol. 2012;65:517–530. doi: 10.1007/s00248-012-0136-5. PubMed DOI

Cocquyt E., Gile G.H., Leliaert F., Verbruggen H., Keeling P.J., De Clerck O. Complex phylogenetic distribution of a non-canonical genetic code in green algae. BMC Evol. Biol. 2010;10:327. doi: 10.1186/1471-2148-10-327. PubMed DOI PMC

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