Abstract
Asplenium viride is a diploid species, belonging to the largest genus of the cosmopolitan fern family Aspleniaceae and occurring on various types of alkaline rocks. It is known to colonize sites with high concentrations of heavy metals, exhibiting changes in frond morphology. A. viride can sometimes form new substrate-dependent ecotypes that can be morphologically and genetically different from parental populations. This study aimed to evaluate the morphological and genetic diversity of A. viride, and test for a potential correlation between variability and heavy metal concentration. Analysis of A. viride specimens from one metalliferous and five non-metalliferous sites showed elevated concentrations of heavy metals in roots of metalliferous plants. The concentrations were higher in roots than in aboveground organs, especially in the case of Cd and Pb, suggesting an excluder strategy for these metals. Both metalliferous and non-metaliferous sites were populated by plants with similar ploidy levels. The overall genetic diversity was low (HT = 0.25) and concentrated between populations (GST = 0.62). The obtained 2C DNA content ranged from 8.67 pg/2C to 8.69 pg/2C. STRUCTURE analysis revealed two groups among the studied populations which did not correlate with heavy metal concentrations and were not significantly supported by AMOVA. This suggests that factors influencing genetic diversity of A. viride are a consequence of intragametophytic selfing caused by patchy habitats and subsequent founder effects, resulting from long-distance colonization by single spores. The species has a potential to colonize heavy metal polluted sites; however, it does not seem to form genetically distinct ecotypes at those sites.
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References
Brownsey P (1977) A taxonomic revision of the New Zealand species of Asplenium. N Z J Bot 15:39–86. https://doi.org/10.1080/0028825X.1977.10429618
Chang JS, Yoon IH, Kim KW (2009) Heavy metal and arsenic accumulating fern species as potential ecological indicators in As-contaminated abandoned mines. Ecol Indic 9:1275–1279. https://doi.org/10.1016/j.ecolind.2009.03.011
Clark J, Hidalgo O, Pellicer J, Liu H, Marquardt J, Robert Y, Christenhusz M, Zhang S, Gibby M, Leitch IJ, Schneider H (2015) Genome evolution of ferns: evidence for relative stasis of genome size across the fern phylogeny. New Phytol 210:1072–1082. https://doi.org/10.1111/nph.13833
Coulaud J, Barghi N, Lefèbvre C, Siljak-Yakovlev S (1999) Cytogenetic variation in populations of Armeria maritima (Mill.) Willd. in relation to geographical distribution and soil stress tolerances. Can. J. Bot., 77: 673–685. https://doi.org/10.1139/cjb-77-5-673
Czapik R (2002) Embryological and cytological variability of plants in polluted environment. Polish Botanical Studies (Vol. 15). Kraków: Szafer Institute of Botany Polish Academy of Sciences
DalCorso G (2012) Heavy Metal Toxicity in Plants. In: Furini A (ed) Plants and Heavy Metals. Springer Netherlands, Dordrecht, pp 1–25
de Groot GA, During HJ, Ansell SW, Schneider H, Bremer P, Wubs ERJ (2012a) Diverse spore rains and limited local exchange shape fern genetic diversity in a recently created habitat colonized by long-distance dispersal. Ann Bot 109:965–978. https://doi.org/10.1093/aob/mcs013
de Groot G, Arjen, Verduyn B, Wubs EJ, Erkens RH, During HJ (2012b) Inter-and intraspecific variation in fern mating systems after long-distance colonization: the importance of selfing. BMC Plant Biol 12:3. https://doi.org/10.1186/1471-2229-12-3
Dissanayake DMREA, Wijesinghe WMKEH, Iqbal SS, Priyantha N, Iqbal MCM (2016) Isotherm and kinetic study on Ni(II) and Pb(II) biosorption by the fern Asplenium nidus L. Ecol Eng 88:237–241. https://doi.org/10.1016/j.ecoleng.2015.12.028
Doležel J, Bartoš J (2005) Plant DNA flow cytometry and estimation of nuclear genome size. Ann Bot 95:99–110. https://doi.org/10.1093/aob/mci005
Doležel J, Sgorbati S, Lucretti S (1992) Comparison of three DNA fluorochromes for flow cytometric estimation of nuclear DNA content in plants. Physiol Plant 85:625–631. https://doi.org/10.1111/j.1399-3054.1992.tb04764.x
Dyer RJ, Savolainen V, Schneider H (2012) Apomixis and reticulate evolution in the Asplenium monanthes fern complex. Ann Bot 110:1515–1529. https://doi.org/10.1093/aob/mcs202
Earl DA, VonHoldt BM (2012) STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. https://doi.org/10.1007/s12686-011-9548-7
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50
Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578. https://doi.org/10.1111/j.1471-8286.2007.01758.x
Galbraith DW, Harkins KR, Maddox JM, Ayres NM, Sharma DP, Firoozabady E (1983) Rapid flow cytometric analysis of the cell cycle in intact plant tissues. Science 220:1049–1051. https://doi.org/10.1126/science.220.4601.1049
Hildebrandt U, Hoef-Emden K, Backhausen S, Bothe H, Bożek M, Siuta, Kuta E (2006) The rare, endemic zinc violets of Central Europe originate from Viola lutea Huds. Plant Sys Evol 257:205–222. https://doi.org/10.1007/s00606-005-0387-4
Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267. https://doi.org/10.1093/molbev/msj030
Ivanova D, Piȩkoś-Mirkowa H (2003) Chromosome numbers of Polish ferns. Acta Biol Crac Ser Bot 45:93–99
James KE, Schneider H, Ansell SW, Evers M, Robba L, Uszynski G (2008) Diversity Arrays Technology (DArT) for pan-genomic evolutionary studies of non-model organisms. PLoS ONE 3:e1682. https://doi.org/10.1371/journal.pone.0001682
Johnston WR, Proctor J (1979) Ecological studies on the Lime Hill serpentine, Scotland. Trans Bot Soc Edinb 43:145–150. https://doi.org/10.1080/03746607908685347
Kabata-Pendias A, Pendias H (2011) Trace elements in soils and plants, 4th edn. Taylor and Francis Group, Boca Raton London New York
Koivunen S, Saikkonen K, Vuorisalo T, Mutikainen P (2004) Heavy metals modify costs of reproduction and clonal growth in the stoloniferous herb Potentilla anserina. Evol Ecol 18:541–561. https://doi.org/10.1007/s10682-004-5143-7
Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) Clumpak: A program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15:1179–1191. https://doi.org/10.1111/1755-0998.12387
Kramer KU, Viane RLL (1990) Aspleniaceae. Pp 52–57 in Kramer, K.U. and Green, P.S. (eds.), Pteridophytes and Gymnosperms. Berlin: Springer Berlin Heidelberg. https://doi.org/10.1007/978-3-662-02604-5_14
Kwiatkowska M, Zabicka J, Migdalek G, Zabicki P, Cubała M, Bohdanowicz J (2019) Comprehensive characteristics and genetic diversity of the endemic Australian Viola banksii (section Erpetion, Violaceae). Aust J Bot 67:81–98. https://doi.org/10.1071/BT18233
Lepp NW (2001) Bryophytes and Pteridophytes. In: Prasad MNV (ed) Metals in the Environment: Analysis by Biodiversity. Marcel Dekker, Inc, New York, Basel, pp 159–170
Liu WJ, Kim KW, Zhu YG, Lee SW, Chang PC, Kwak JH (2006) A survey of arsenic and other heavy metals in vegetation from markets or mine tailings. J Environ Sci (China) 18:287–291
Marin PD, Tatić B (2001) Serpentine soil and plant diversity, with emphasis balkan Peninsula. Bocconea 13:145–150
Markert B (1992) Establishing of “Reference Plant” for inorganic characterization of different plant species by chemical fingerprinting. Water Air Soil Pollut 64:533–538. https://doi.org/10.1007/BF00483363
Meyer CL, Kostecka AA, Saumitou-Laprade P, Créach A, Castric V, Pauwels M, Frérot H (2010) Variability of zinc tolerance among and within populations of the pseudometallophyte species Arabidopsis halleri and possible role of directional selection. New Phytol 185(1):130–142. https://doi.org/10.1111/j.1469-8137.2009.03062.x
Migdałek G, Nowak J, Saługa M, Cieślak E, Szczepaniak M, Ronikier M (2017) No evidence of contemporary interploidy gene flow between the closely related European woodland violets Viola reichenbachiana and V. riviniana (sect. Viola, Violaceae). Plant Biol 19:542–551. https://doi.org/10.1111/plb.12571
Minister of the Environment (2016) Regulation of the Minister of the Environment of 1 September 2016 on the Method of the Contamination Assessment of the Earth Surface. In Journal of Laws of 2016; Item 1395, Wydawnictwo Sejmowe: Warsaw, Poland (In Polish)
Mróz L, Rudecki AL (2009) Comparison of chemical composition of two co-occurring chasmophytes, Asplenium ruta-muraria L. (Pteridophyta) and Cymbalaria muralis Gaer., Mey. and Scher. (Spermatophyta) from habitats differing in air pollution. Pol J Environ Stud 18:853–863
Nei M(1973) Analysis of gene diversity in subdivided populations. Proceedings of the National Academy of Sciences, 70: 3321–3323
Nei M, Li WH(1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proceedings of the National Academy of Sciences, 76: 5269–5273
Pavel AB, Vasile CI (2012) PyElph - a software tool for gel images analysis and phylogenetics. BMC Bioinformatics 13:9. https://doi.org/10.1186/1471-2105-13-9
Perrie LR, Shepherd LD, De Lange PJ, Brownsey PJ (2010) Parallel polyploid speciation: Distinct sympatric gene-pools of recurrently derived allo-octoploid Asplenium ferns. Mol Ecol 19:2916–2932. https://doi.org/10.1111/j.1365-294X.2010.04705.x
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Proctor J, Woodell SRJ (1971) The Plant Ecology of Serpentine: I. Serpentine Vegetation of England and Scotland. J Ecol 59:375–395
Przedpełska E, Wierzbicka M (2007) Arabidopsis arenosa (Brassicaceae) from a lead-zinc waste heap in southern Poland - A plant with high tolerance to heavy metals. Plant Soil 299:43–53. https://doi.org/10.1007/s11104-007-9359-5
Punz WF, Sieghardt H (1993) The response of roots of herbaceous plant species to heavy metals. Environ Exp Bot 33:85–98. https://doi.org/10.1016/0098-8472(93)90058-N
Punz W, Kovacs G, Körber-Ulrich SM, Thonke A, Wieländer B, Wieshofer I(1994) Schwermetallstandorte im mittleren Alpenraum und ihre Vegetation - neue Befunde. Verhandlungen der Zoologisch-Botanischen Gesellschaft Österreich, 131: 1–26
Rogers SO, Bendich AJ (1994) Extraction of total cellular DNA from plants, algae and fungi. Plant Mol Biol 183–190. https://doi.org/10.1007/978-94-011-0511-8_12
Roux JP (1993) The genus Asplenium L. (Aspleniaceae: Pteridophyta) in the Tristan-Gough Island Group. Kew Bull 48:79–97. https://doi.org/10.2307/4115750
Schlüter PM (2013) FAMD - Fingerprint Analysis with Missing Data 1.31 Manual. University of Zurich, Zurich
Schlüter PM, Harris SA (2006) Mol Ecol Notes 6:569–572. https://doi.org/10.1111/j.1471-8286.2006.01225.x. Analysis of multilocus fingerprinting data sets containing missing data
Schneider H, Navarro-Gomez A, Russell SJ, Ansell S, Grundmann M, Vogel J (2013) Exploring the utility of three nuclear regions to reconstruct reticulate evolution in the fern genus Asplenium. J Syst Evol 51:142–153. https://doi.org/10.1111/j.1759-6831.2012.00226.x
Schneller JJ, Holderegger R (1996) Genetic variation in small, isolated fern populations. J Veg Sci 7:113–120. https://doi.org/10.2307/3236423
Slatkin M, Barton NH (1989) A comparison of three indirect methods for estimating average levels of gene flow. Evolution 43(7):1349–1368. https://doi.org/10.2307/2409452
Sleep A(1985) Speciation in relation to edaphic factors in the Asplenium adiantum-nigrum group. Proceedings of the Royal Society of Edinburgh. Section B. Biological Sciences, 86: 325–334. https://doi.org/10.1017/S0269727000008290
Słomka A, Sutkowska A, Szczepaniak M, Malec P, Mitka J, Kuta E (2011) Increased genetic diversity of Viola tricolor L. (Violaceae) in metal-polluted environments. Chemosphere 83:435–442. https://doi.org/10.1016/j.chemosphere.2010.12.081
Smith AR, Pryer KM, Schuettpelz E, Korall P, Schneider H, Wolf PG (2006) A classification for extant ferns. Taxon 55:705–731. https://doi.org/10.2307/25065646
Soare LC, Visoiu E, Bejan C, Dobrescu CM, Fierascu I, Iosub I, Paunescu A (2015) Research on the in vitro bioaccumulation capacity of lead in some pteridophyte species of the Romanian flora. Rev Chim 66:2017–2020
Soltis DE, Soltis PS, Bennett MD, Leitch IJ (2003) Evolution of genome size in the angiosperms. Am J Bot 90:1596–1603. https://doi.org/10.3732/ajb.90.11.1596
Temsch EM, Temsch W, Ehrendorfer-Schratt L, Greilhuber J(2010) Heavy metal pollution, selection, and genome size: the species of the žerjav study revisited with flow cytometry. Journal of Botany, 2010: 1–11. https://doi.org/10.1155/2010/596542
Trewick S, Morgan-Richards M, Russell SJ, Henderson S, Rumsey FJ, Pintér I (2002) Polyploidy, phylogeography and Pleistocene refugia of the rockfern Asplenium ceterach: Evidence from chloroplast DNA. Mol Ecol 11:2003–2012. https://doi.org/10.1046/j.1365-294X.2002.01583.x
Valentine DH, Moore DM(1993) Aspleniaceae. Pp. 18–23 in Tutin, T.G.N.A., Burges, A.O., Chater, J.R., Edmondson, V.H., Heywood, Moore, D.M., Valentine, D.H., Walters, S.M. and Webb, D.A. (eds.), Flora Europaea 1. Cambridge: Cambridge University Press
Van de Peer Y, De Wachter R(1994) TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Computer applications in the biosciences: CABIOS, 10: 569–570
Vogel JC, Rumsey FJ, Schneller JJ, Barret JA, Gibby M (1999a) Where are the glacial refugia in Europe? Evidence from pteridophytes. Biol J Linn Soc 66:23–37. https://doi.org/10.1111/j.1095-8312.1999.tb01915.x
Vogel JC, Rumsey FJ, Russell SJ, Cox CJ, Holmes JS, Bujnoch W (1999b) Genetic structure, reproductive biology and ecology of isolated populations of Asplenium csikii (Aspleniaceae, pteridophyta). Heredity 83:604–612. https://doi.org/10.1038/sj.hdy.6886120
Werth CR, Guttman SI, Eshbaugh WH (1985) Recurring origins of allopolyploid species in Asplenium. Science 228:731–733. https://doi.org/10.1126/science.228.4700.731
Woch MW (2015) Characteristics of landscape features related tomining and metallurgy in the Olkusz region. In: Godzik B (ed) Natural and historical values of the Olkusz Ore-bearing region Kraków. W. Szafer Institute of Botany, Polish Academy of Sciences, pp 43–53
Woch M, Stefanowicz AM, Stanek M (2017) Waste heaps left by historical Zn-Pb ore mining are hotspots of species diversity of beech forest understory vegetation. Sci Total Environ 599–600:32–41. https://doi.org/10.1016/j.scitotenv.2017.04.197
Yeh FC, Yang RC, Boyle T (1999) PopGene Version 131: Microsoft Windows-based freeware for population genetic analysis. University of Alberta and Centre for International Forestry Research, pp 11–23
Zając A, Zając M (2001) Distribution atlas of vascular plant in Poland. Laboratory of Computer Corology Institute of Botany Jagiellonian University, Kraków
Acknowledgements
The research was funded by the Institute of Biology of the Nicolaus Copernicus University in Toruń, the Institute of Biology of the Pedagogical University of Kraków, the Department of Agricultural Biotechnology of Bydgoszcz University of Science and Technology, and the W. Szafer Institute of Botany of the Polish Academy of Sciences.
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The research was funded by the Institute of Biology of the Nicolaus Copernicus University in Toruń, the Institute of Biology of the Pedagogical University of Kraków, the Department of Agricultural Biotechnology, the Faculty of Agriculture and Biotechnology of the Bydgoszcz University of Science and Technology, and the W. Szafer Institute of Botany of the Polish Academy of Sciences.
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MWW and GM conceived the idea and wrote the manuscript with input from IJ, AMS, and MP. AMS, GM, and MWW secured funding to support the work. GM, IJ, and AMS performed all the analyses and produced figures and tables. MWW and MP performed the field sampling, taxonomic revision, specimens collection, and conserved material to analyses.
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Woch, M.W., Migdałek, G., Jedrzejczyk, I. et al. The genetic diversity of Asplenium viride (Aspleniaceae) fern colonizing heavy metal-polluted sites. Plant Growth Regul 98, 359–369 (2022). https://doi.org/10.1007/s10725-022-00864-3
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DOI: https://doi.org/10.1007/s10725-022-00864-3