{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,1]],"date-time":"2026-09-01T23:46:48Z","timestamp":1788306408054,"version":"build-2803163510"},"reference-count":130,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2023,2,28]],"date-time":"2023-02-28T00:00:00Z","timestamp":1677542400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004281","name":"National Science Center","doi-asserted-by":"publisher","award":["2019\/33\/B\/NZ8\/00896"],"award-info":[{"award-number":["2019\/33\/B\/NZ8\/00896"]}],"id":[{"id":"10.13039\/501100004281","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Tolerance to heavy metals in plants is a model process used to study adaptations to extremely unfavorable environments. One species capable of colonizing areas with high contents of heavy metals is Armeria maritima (Mill.) Wild. A. maritima plants growing in metalliferous areas differ in their morphological features and tolerance levels to heavy metals compared to individuals of the same species growing in non-metalliferous areas. The A. maritima adaptations to heavy metals occur at the organismal, tissue, and cellular levels (e.g., the retention of metals in roots, enrichment of the oldest leaves with metals, accumulation of metals in trichomes, and excretion of metals by salt glands of leaf epidermis). This species also undergoes physiological and biochemical adaptations (e.g., the accumulation of metals in vacuoles of the root\u2019s tannic cells and secretion of such compounds as glutathione, organic acids, or HSP17). This work reviews the current knowledge on A. maritima adaptations to heavy metals occurring in zinc\u2013lead waste heaps and the species\u2019 genetic variation from exposure to such habitats. A.\u00a0maritima is an excellent example of microevolution processes in plants inhabiting anthropogenically changed areas.<\/jats:p>","DOI":"10.3390\/ijms24054650","type":"journal-article","created":{"date-parts":[[2023,2,28]],"date-time":"2023-02-28T03:00:38Z","timestamp":1677553238000},"page":"4650","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":10,"title":["Micro-Evolutionary Processes in Armeria maritima at Metalliferous Sites"],"prefix":"10.3390","volume":"24","author":[{"given":"Ma\u0142gorzata","family":"Wierzbicka","sequence":"first","affiliation":[{"name":"Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Agnieszka","family":"Abratowska","sequence":"additional","affiliation":[{"name":"Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Olga","family":"Bemowska-Ka\u0142abun","sequence":"additional","affiliation":[{"name":"Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dorota","family":"Panufnik-M\u0119drzycka","sequence":"additional","affiliation":[{"name":"Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pawe\u0142","family":"W\u0105sowicz","sequence":"additional","affiliation":[{"name":"Icelandic Institute of Natural History, Borgir vid Nordurslod, 600 Akureyri, Iceland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1075-7854","authenticated-orcid":false,"given":"Monika","family":"Wr\u00f3bel","sequence":"additional","affiliation":[{"name":"Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Damian","family":"Trzybi\u0144ski","sequence":"additional","affiliation":[{"name":"Biological and Chemical Research Centre, University of Warsaw, \u017bwirki I Wigury 101, 02-089 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0277-294X","authenticated-orcid":false,"given":"Krzysztof","family":"Wo\u017aniak","sequence":"additional","affiliation":[{"name":"Faculty of Chemistry, University of Warsaw, Pasteura 1, 02-093 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,2,28]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1023\/A:1013378014069","article-title":"Trends and rates of microevolution in plants","volume":"112\u2013113","author":"Bone","year":"2001","journal-title":"Genetica"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1016\/S0006-3207(02)00279-3","article-title":"Evolutionarily enlightened management","volume":"111","author":"Ashley","year":"2003","journal-title":"Biol. Conserv."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"2105","DOI":"10.1016\/j.chemosphere.2006.12.024","article-title":"Micro\u2212evolution due to pollution: Possible consequences for ecosystem responses to toxic stress","volume":"67","author":"Medina","year":"2007","journal-title":"Chemosphere"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1613","DOI":"10.1002\/ajb2.1170","article-title":"Can plants evolve to meet a changing climate? The potential of field experimental evolution studies","volume":"105","author":"Mitchell","year":"2018","journal-title":"Am. J. Bot."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"840","DOI":"10.1086\/705680","article-title":"Meta-analysis shows that rapid phenotypic change in angiosperms in response to environmental change is followed by stasis","volume":"194","year":"2019","journal-title":"Am. Nat."},{"key":"ref_6","unstructured":"Shaw, A. (1990). Heavy Metal Tolerance in Plants: Evolutionary Aspects, CRC Press Inc.. Available online: https:\/\/books.google.pl\/books?hl=pl&lr=&id=kvsPo4Et5scC&oi=fnd&pg=PA285&dq=Microevolutionary+processes+on+contaminated+deposits&ots=wF857IxRSZ&sig=jtmIj3x4wrOf9lcaVwis-spyqCU&redir_esc=y#v=onepage&q=Microevolutionary%20processes%20on%20contaminated%20deposits&f=false."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1023\/A:1013368628607","article-title":"An introduction to microevolution: Rate, pattern, process","volume":"112","author":"Hendry","year":"2001","journal-title":"Genetica"},{"key":"ref_8","first-page":"7","article-title":"Microevolutionary changes in ecotypes of calamine waste heap vegetation near Olkusz, Poland: A review","volume":"44","author":"Wierzbicka","year":"2002","journal-title":"Acta Biol. Crac. Ser. Bot."},{"key":"ref_9","first-page":"251","article-title":"Evolution of metal tolerance in higher plants","volume":"80","author":"Ernst","year":"2006","journal-title":"For. Snow Landsc. Res."},{"key":"ref_10","unstructured":"Szarek-\u0141ukaszewska, G. (2020). Buckler Mustard (Biscutella laevigata L.) an Extraordinary Plant on Ordinary Mine Heaps near Olkusz. W., Szafer Institute of Botany, Polish Academy of Sciences. Available online: https:\/\/www.botany.pl\/images\/ibwyd\/Monografie\/Biscutella_tekst_plusOkladka.pdf."},{"key":"ref_11","unstructured":"Hendry, A.P. (2020). Eco-Evolutionary Dynamics, Princeton University Press. Available online: https:\/\/books.google.pl\/books?hl=pl&lr=&id=tPrDDwAAQBAJ&oi=fnd&pg=PP1&ots=T4PWdar5Ed&sig=oRKGylPE6wS67CSYQa_a9mccaO0&redir_esc=y#v=onepage&q&f=false."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1016\/j.ecoenv.2003.12.009","article-title":"Highly toxic thallium in plants from the vicinity of Olkusz (Poland)","volume":"59","author":"Wierzbicka","year":"2004","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_13","unstructured":"Godzik, B. (2015). Natural and Historical Values of the Olkusz Ore-Bearing Region. W., Szafer Institute of Botany, Polish Academy of Sciences."},{"key":"ref_14","unstructured":"Szarek-\u0141ukaszewska, G. (2020). Buckler Mustard (Biscutella laevigata L.) an Extraordinary Plant on Ordinary Mine Heaps near Olkusz. W., Szafer Institute of Botany, Polish Academy of Sciences."},{"key":"ref_15","first-page":"19","article-title":"Response of Armeria maritima (Mill.) Willd. to Cd, Zn and Pb","volume":"46","author":"Wierzbicka","year":"2004","journal-title":"Acta Biol. Crac. Ser. Bot."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1016\/S0269-7491(99)00262-6","article-title":"Strategies of heavy metal uptake by three plant species growing near a metal smelter","volume":"109","author":"Balabane","year":"2000","journal-title":"Environ. Pollut."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1016\/S1164-5563(02)00006-7","article-title":"Effects of metal contamination on the activity and diversity of springtails in an ancient Pb-Zn mining area at Plombieres, Belgium","volume":"39","author":"Lock","year":"2003","journal-title":"Eur. J. Soil Biol."},{"key":"ref_18","first-page":"29","article-title":"Concentration of alkaline and heavy metals in Biscutella laevigata L. and Plantago lanceolata L. growing on calamine spoils (S. Poland)","volume":"44","year":"2002","journal-title":"Acta Biol. Crac. Ser. Bot."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1007\/s11104-007-9359-5","article-title":"Arabidopsis arenosa (Brassicaceae) from a lead\u2013zinc waste heap in southern Poland\u2014A plant with high tolerance to heavy metals","volume":"299","author":"Wierzbicka","year":"2007","journal-title":"Plant Soil"},{"key":"ref_20","first-page":"7","article-title":"Thallium hyperaccumulation in Polish populations of Biscutella laevigata (Brassicaceae)","volume":"58","author":"Wierzbicka","year":"2016","journal-title":"Acta Biol. Crac. Ser. Bot."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1016\/S0269-7491(98)00209-7","article-title":"Mutual effects of soil organic matter dynamics and heavy metals fate in a metallophyte grassland","volume":"105","author":"Balabane","year":"1999","journal-title":"Environ. Pollut."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1016\/S0269-7491(97)00139-5","article-title":"Speciation of lead in contaminated soils","volume":"98","author":"McBride","year":"1997","journal-title":"Environ. Pollut."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"586","DOI":"10.1111\/j.1438-8677.2011.00536.x","article-title":"Morphological and genetic distinctiveness of the metallicolous and non-metallicolous populations of Armeria maritima s. l. (Plumbaginaceae) in Poland","volume":"14","author":"Abratowska","year":"2012","journal-title":"Plant Biol."},{"key":"ref_24","unstructured":"Wierzbicka, M. (2015). Ecotoxicology. Plants, Soil, Metals [Ekotoksykologia. Ro\u015bliny, Gleby, Metale], Warsaw University Press. (In Polish)."},{"key":"ref_25","unstructured":"Godzik, B. (2015). Natural and Historical Values of the Olkusz Ore-Bearing Region. W., Szafer Institute of Botany, Polish Academy of Sciences."},{"key":"ref_26","unstructured":"Godzik, B. (2015). Natural and Historical Values of the Olkusz Ore-Bearing Region. W., Szafer Institute of Botany, Polish Academy of Sciences."},{"key":"ref_27","unstructured":"Godzik, B. (2015). Natural and Historical Values of the Olkusz Ore-Bearing Region. W., Szafer Institute of Botany, Polish Academy of Sciences."},{"key":"ref_28","unstructured":"Godzik, B. (2015). Natural and Historical Values of the Olkusz Ore-Bearing Region. W., Szafer Institute of Botany, Polish Academy of Sciences."},{"key":"ref_29","unstructured":"Wierzbicka, M. (2015). Ecotoxicology. Plants, Soil, Metals [Ekotoksykologia. Ro\u015bliny, Gleby, Metale], Warsaw University Press. (In Polish)."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1016\/j.jplph.2017.08.014","article-title":"Divergent biology of facultative heavy metal plants","volume":"219","author":"Bothe","year":"2017","journal-title":"J. Plant Physiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0065-2504(08)60202-0","article-title":"Heavy metal tolerance in plants","volume":"7","author":"Antonovics","year":"1971","journal-title":"Adv. Ecol. Res."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Prasad, M. (2004). Heavy Metal Stress in Plants. From Biomolecules to Ecosystems, Springer. Available online: https:\/\/books.google.pl\/books?hl=pl&lr=&id=6S_wCAAAQBAJ&oi=fnd&pg=PA1&dq=Heavy+Metal+Stress+in+Plants.+From+biomolecules+to+ecosystems&ots=WdG9h9c5Ih&sig=7x03r6oE_jei17vxj_XE91vM9Ow&redir_esc=y#v=onepage&q=Heavy%20Metal%20Stress%20in%20Plants.%20From%20biomolecules%20to%20ecosystems&f=false.","DOI":"10.1007\/978-3-662-07743-6"},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Batty, L., and Hallberg, K. (2010). Ecology of Industrial Pollution, British Ecological Society. Available online: https:\/\/books.google.pl\/books?hl=pl&lr=&id=t4yauYHrCRoC&oi=fnd&pg=PA7&dq=Metallophytes:+the+unique+biological+resource,+its+ecology+and+conservational+status+in+Europe,+central+Africa+and+Latin+America&ots=DxxvKHi1E3&sig=LJGA29_L_ZQ9DaFWo1Lq88JtcM0&redir_esc=y#v=onepage&q&f=false.","DOI":"10.1017\/CBO9780511805561"},{"key":"ref_34","unstructured":"Wierzbicka, M. (2015). Ecotoxicology. Plants, Soil, Metals [Ekotoksykologia. Ro\u015bliny, Gleby, Metale], Warsaw University Press. (In Polish)."},{"key":"ref_35","unstructured":"Wierzbicka, M. (2015). Ecotoxicology. Plants, Soil, Metals [Ekotoksykologia. Ro\u015bliny, Gleby, Metale], Warsaw University Press. (In Polish)."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.envexpbot.2016.03.001","article-title":"Plant adaptation to metal polluted environments\u2014Physiological, morphological, and evolutionary insights from Biscutella laevigata","volume":"127","author":"Waldmann","year":"2016","journal-title":"Environ. Exp. Bot."},{"key":"ref_37","first-page":"139","article-title":"The adaptation of plants to growth on a calamine waste heap in Boles\u0142aw near Olkusz","volume":"2","author":"Wierzbicka","year":"2002","journal-title":"Kosmos"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"123","DOI":"10.3897\/phytokeys.160.53937","article-title":"A new taxon within Biscutella laevigata L. (Brassicaceae) endemic to calamine areas in southern Poland","volume":"160","author":"Wierzbicka","year":"2020","journal-title":"PhytoKeys"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1038\/sj.hdy.6800835","article-title":"Evolution in closely adjacent plant populations X: Long\u2212term persistence of prereproductive isolation at a mine boundary","volume":"97","author":"Antonovics","year":"2006","journal-title":"Heredity"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"704","DOI":"10.1016\/S0176-1617(11)81937-1","article-title":"How does Armeria maritima tolerate high heavy metal concentrations?","volume":"146","author":"Neumannnn","year":"1995","journal-title":"J. Plant Physiol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1078\/0176-1617-00553","article-title":"Ultrastructural localization of zinc in zinc\u2013tolerant Armeria maritima ssp","volume":"159","author":"Heumann","year":"2002","journal-title":"halleri by autometallography. J. Plant Physiol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1055\/s-2003-40729","article-title":"Genetic variation within and among metal-tolerant and non-tolerant populations of Armeria maritima (Mill.) Willd. sl (Plumbaginaceae) in Central and Northeast Germany","volume":"5","author":"Baumbach","year":"2003","journal-title":"Plant Biol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1007\/s00606-007-0593-3","article-title":"Genetic differentiation of metallicolous and non\u2212metallicolous Armeria maritima (Mill.) Willd. taxa (Plumbaginaceae) in Central Europe","volume":"269","author":"Baumbach","year":"2007","journal-title":"Plant Syst. Evol."},{"key":"ref_44","first-page":"105","article-title":"Does Armeria maritima subsp","volume":"19","author":"Wierzbicka","year":"2005","journal-title":"halleri (Plumbaginaceae) occur in Poland? Pol. Bot. Stud."},{"key":"ref_45","first-page":"217","article-title":"Armeria maritima\u2014The plant species adapted to growth on soils polluted by heavy metals","volume":"2","author":"Abratowska","year":"2006","journal-title":"Kosmos"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1016\/j.ecoenv.2007.01.010","article-title":"Armeria maritima from a calamine heap\u2014Initial studies on physiologic\u2014Metabolic adaptations to metal enriched soil","volume":"69","author":"Olko","year":"2008","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_47","unstructured":"Wierzbicka, M. (2015). Ecotoxicology. Plants, Soil, Metals [Ekotoksykologia. Ro\u015bliny, Gleby, Metale], Warsaw University Press. (In Polish)."},{"key":"ref_48","first-page":"57","article-title":"Uptake and localization of cadmium by Biscutella laevigata, a cadmium hyperaccumulator","volume":"46","author":"Pielichowska","year":"2004","journal-title":"Acta Biol. Crac. Ser. Bot."},{"key":"ref_49","first-page":"227","article-title":"Physiological and genetic differentiation between metallicolous and non-metallicolous diploid populations of Alpine Biscutella laevigata (Brassicacae) in the Tatra Mountains and the Northern Carpathian Foreland","volume":"51","author":"Pielichowska","year":"2014","journal-title":"Ann. Bot. Fenn."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1007\/s11104-014-2171-0","article-title":"Patterns of genetic divergence among populations of the pseudometallophyte Biscutella laevigata from southern Poland","volume":"383","author":"Parisod","year":"2014","journal-title":"Plant Soil"},{"key":"ref_51","first-page":"1","article-title":"Microevolution on anthropogenically changed areas on the example of Biscutella laevigata plants from calamine waste heap in Poland","volume":"7","author":"Wierzbicka","year":"2017","journal-title":"J. Anal. Toxicol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1023\/A:1020612930364","article-title":"The adaptation of Dianthus carthusianorum L. (Caryophyllaceae) to growth on a zinc\u2013lead heap in southern Poland","volume":"246","author":"Wierzbicka","year":"2002","journal-title":"Plant Soil"},{"key":"ref_53","first-page":"45","article-title":"Localization of lead in root tip of Dianthus carthusianorum","volume":"46","author":"Wierzbicka","year":"2004","journal-title":"Acta Biol. Crac. Ser. Bot."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1249","DOI":"10.1016\/j.chemosphere.2012.09.068","article-title":"Morphological, physiological and genetic variation between metallicolous and nonmetallicolous populations of Dianthus carthusianorum","volume":"90","author":"Dresler","year":"2013","journal-title":"Chemosphere"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1016\/j.phytochem.2014.01.008","article-title":"Accumulation and tolerance of lead in two contrasting ecotypes of Dianthus carthusianorum","volume":"100","author":"Tukiendorf","year":"2014","journal-title":"Phytochemistry"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1007\/s006060170049","article-title":"Thlaspi s. str. (Brassicaceae) versus Thlaspi sl: Morphological and anatomical characters in the light of ITS nrDNA sequence data","volume":"227","author":"Koch","year":"2001","journal-title":"Plant Syst. Evol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1111\/j.1469-8137.2006.01923.x","article-title":"Life history variation in the heavy metal tolerant plant Thlaspi caerulescens growing in a network of contaminated and noncontaminated sites in southern France: Role of gene flow, selection and phenotypic plasticity","volume":"173","author":"Petit","year":"2007","journal-title":"New Phytol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1016\/S0269-7491(98)00012-8","article-title":"The adaptation of Silene vulgaris to growth on a calamine waste heap (S. Poland)","volume":"101","author":"Wierzbicka","year":"1998","journal-title":"Environ. Pollut."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1007\/s00606-005-0387-4","article-title":"The rare, endemic zinc violets of Central Europe originate from Viola lutea Huds","volume":"257","author":"Hildebrandt","year":"2006","journal-title":"Plant Syst. Evol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"1610","DOI":"10.1016\/j.jplph.2007.11.004","article-title":"Metalliferous and non-metalliferous populations of Viola tricolor represent similar mode of antioxidative response","volume":"165","author":"Kuta","year":"2008","journal-title":"J. Plant Physiol."},{"key":"ref_61","first-page":"123","article-title":"Was reduced pollen viability in Viola tricolor L. the result of heavy metal pollution or rather the tests applied?","volume":"52","author":"Kawalec","year":"2010","journal-title":"Acta Biol. Crac. Ser. Bot."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"1191","DOI":"10.1016\/j.jplph.2011.01.033","article-title":"Violets of the section Melanium, their colonization by arbuscular mycorrhizal fungi and their occurrence on heavy metal heaps","volume":"168","author":"Kuta","year":"2011","journal-title":"J. Plant Physiol."},{"key":"ref_63","first-page":"7","article-title":"Influence of a heavy-metal-polluted environment on Viola tricolor genome size and chromosome number","volume":"53","author":"Wolny","year":"2011","journal-title":"Acta Biol. Crac. Ser. Bot."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1016\/j.chemosphere.2010.12.081","article-title":"Increased genetic diversity of Viola tricolor L. (Violaceae) in metal-polluted environments","volume":"83","author":"Sutkowska","year":"2011","journal-title":"Chemosphere"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"204","DOI":"10.1016\/j.envexpbot.2011.07.003","article-title":"Heavy metals in soil affect reproductive processes more than morphological characters in Viola tricolor","volume":"75","author":"Karcz","year":"2012","journal-title":"Environ. Exp. Bot."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"924","DOI":"10.1111\/plb.12143","article-title":"Morphological versus genetic diversity of Viola reichenbachiana and V. riviniana (sect. Viola, Violaceae) from soils differing in heavy metal content","volume":"16","author":"Kuta","year":"2014","journal-title":"Plant Biol."},{"key":"ref_67","first-page":"63","article-title":"The heavy-metal vegetation of north-western mainland Europe","volume":"123","author":"Brown","year":"2001","journal-title":"Bot. Jahrb. Syst. Pflanzengesch. Pflanzengeogr."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1127\/0340-269X\/2008\/0038-0255","article-title":"Vegetation response to high concentrations of heavy metals in the Harz Mountains, Germany","volume":"38","author":"Becker","year":"2008","journal-title":"Phytocoenologia"},{"key":"ref_69","unstructured":"Tutin, T.G., Heywood, V.H., Burges, N.A., Valentine, D.H., Ball, P.W., Walters, S.M., Chater, A.O., Webb, D.A., DeFilipps, R.A., and Ferguson, I.K. (1972). Flora Europaea: Diapensiaceae to Myoporaceae, Cambridge University Press. Available online: https:\/\/books.google.pl\/books\/about\/Flora_Europaea.html?id=u8jDAoMGPd8C&redir_esc=y."},{"key":"ref_70","unstructured":"GBIF (2020). Catalogue of Life, The Global Biodiversity Information Facility. Checklist Dataset."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"7","DOI":"10.5586\/asbp.1946.001","article-title":"The genus Armeria Willd. in Poland (La genre Armeria en Pologne)","volume":"17","author":"Szafer","year":"1946","journal-title":"Acta Soc. Bot. Pol."},{"key":"ref_72","unstructured":"Wierzbicka, M. (2015). Ecotoxicology. Plants, Soil, Metals [Ekotoksykologia. Ro\u015bliny, Gleby, Metale], Warsaw University Press. (In Polish)."},{"key":"ref_73","first-page":"1","article-title":"Zeigerwerte von pflanzen in Mitteleuropa","volume":"18","author":"Ellenberg","year":"1991","journal-title":"Scr. Geol."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"573","DOI":"10.2307\/2261536","article-title":"Armeria maritima (Mill.) Willd. (Statice armeria L.; S. maritima Mill.)","volume":"81","author":"Woodell","year":"1993","journal-title":"J. Ecol."},{"key":"ref_75","unstructured":"Rutkowski, L. (1998). Key for Identification of Vascular Plants in Polish Lowlands [Klucz do Oznaczania Ro\u015blin Naczyniowych Polski Ni\u017cowej], Polish Scientific Publisher. Available online: https:\/\/agris.fao.org\/agris-search\/search.do?recordID=US201300054709."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1111\/j.1469-8137.1974.tb04620.x","article-title":"Population variation and taxonomy in Armeria maritima with special reference to heavy-metal-tolerant populations","volume":"73","year":"1974","journal-title":"New Phytol."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1111\/j.1469-8137.1976.tb01513.x","article-title":"Breeding system and population structure of Armeria maritima (Mill.) Willd. on a zinc-lead mine","volume":"77","year":"1976","journal-title":"New Phytol."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1111\/j.1469-8137.1975.tb02619.x","article-title":"Some aspects of pollination ecology of Armeria maritima (Mill.) Willd. in Britain","volume":"74","author":"Eisikowitch","year":"1975","journal-title":"New Phytol."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1038\/hdy.1992.91","article-title":"Gene flow and population structure in Armeria maritima","volume":"69","author":"Philipp","year":"1992","journal-title":"Heredity"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"349","DOI":"10.2307\/2406635","article-title":"The evolution, functioning and breakdown of heteromorphic incompatibility systems. I. The Plumbaginaceae","volume":"20","author":"Baker","year":"1966","journal-title":"Evolution"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"96","DOI":"10.1038\/243096a0","article-title":"Outbreeding and inbreeding in a zinc\u2013lead mine population of Armeria maritima","volume":"243","year":"1973","journal-title":"Nature"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1111\/j.1469-8137.1989.tb02384.x","article-title":"The population genetics of Armeria maritima (Mill.) Willd. on the river South Tyne, UK","volume":"112","author":"Richards","year":"1989","journal-title":"New Phytol."},{"key":"ref_83","first-page":"15","article-title":"The evolution and breakdown of the heteromorphic incompatibility system of Armeria maritima revisited","volume":"4","author":"Vekemans","year":"1990","journal-title":"Evol. Trends Plant Sci."},{"key":"ref_84","unstructured":"Zarzycki, K., Trzci\u0144ska-Tacik, H., R\u00f3\u017ca\u0144ski, W., Szal\u0105g, Z., Wo\u0142ek, J., and Korzeniak, U. (2002). Ecological Indicator Values of Vascular Plants of Vascular Plants of Poland. W., Szafer Institute of Botany, Polish Academy of Sciences. Available online: https:\/\/www.nhbs.com\/ecological-indicator-values-of-vascular-plants-of-poland-book."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"759","DOI":"10.1111\/j.1469-8137.2008.02748.x","article-title":"Molecular mechanisms of metal hyperaccumulation in plants","volume":"181","author":"Verbruggen","year":"2009","journal-title":"New Phytol."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1111\/j.1365-3040.1987.tb02075.x","article-title":"Lead accumulation and its translocation barriers in roots of Allium cepa L.\u2014Autoradiographic and ultrastructural studies","volume":"10","author":"Wierzbicka","year":"1987","journal-title":"Plant Cell Environ."},{"key":"ref_87","unstructured":"Schuurmann, G., and Markert, B. (1998). Exotoxicology. Ecological Fundamentals, Chemical Exposure and Biological Effects, VU University Amsterdam. Available online: https:\/\/research.vu.nl\/en\/publications\/effects-of-heavy-metals-in-plants-at-the-cellular-and-organismic-."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"3325","DOI":"10.1093\/emboj\/18.12.3325","article-title":"Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast","volume":"18","author":"Clemens","year":"1999","journal-title":"EMBO J."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1016\/S1360-1385(02)02295-1","article-title":"A long way ahead: Understanding and engineering plant metal accumulation","volume":"7","author":"Clemens","year":"2002","journal-title":"Trends Plant Sci."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"731","DOI":"10.1007\/s00425-004-1392-5","article-title":"Subcellular localization of Cd and Zn in the leaves of a Cd\u2212hyperaccumulating ecotype of Thlaspi caerulescens","volume":"220","author":"Ma","year":"2005","journal-title":"Planta"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1023\/A:1021225721605","article-title":"Mechanisms of copper tolerance by Armeria maritima in Dolfrwynog Bog, North Wales\u2013Initial studies","volume":"25","author":"Brewin","year":"2003","journal-title":"Environ. Geochem. Health"},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1111\/j.1438-8677.1992.tb01332.x","article-title":"Metal tolerance in plants","volume":"41","author":"Schat","year":"1992","journal-title":"Acta Bot. Neerl."},{"key":"ref_93","doi-asserted-by":"crossref","unstructured":"Prasad, M.N.V., and Strza\u0142ka, K. (2002). Physiology and Biochemistry of Metal Toxicity and Tolerance in Plants, Springer.","DOI":"10.1007\/978-94-017-2660-3"},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1034\/j.1399-3054.1998.1040110.x","article-title":"Distribution of cadmium in leaves of cadmium tolerant and sensitive ecotypes of Silene vulgaris","volume":"104","author":"Chardonnens","year":"1998","journal-title":"Physiol. Plant."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1104\/pp.119.1.305","article-title":"Cellular compartmentation of zinc in leaves of the hyperaccumulator Thlaspi caerulescens","volume":"119","author":"Zhao","year":"1999","journal-title":"Plant Physiol."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1007\/s004250000366","article-title":"Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri","volume":"212","author":"Lombi","year":"2000","journal-title":"Planta"},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1046\/j.1365-3040.2000.00569.x","article-title":"Zinc hyperaccumulation and cellular distribution in Arabidopsis halleri","volume":"23","author":"Zhao","year":"2000","journal-title":"Plant Cell Environ."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1007\/BF00039552","article-title":"Isolation of a Vicia faba metallothionein-like gene: Expression in foliar trichomes","volume":"26","author":"Foley","year":"1994","journal-title":"Plant Mol. Biol."},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"11108","DOI":"10.1073\/pnas.190334497","article-title":"Glutathione biosynthesis in Arabidopsis trichome cells","volume":"97","author":"Gotor","year":"2000","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1093\/jxb\/37.4.461","article-title":"Structural aspects of the salt glands of the Plumbaginaceae","volume":"37","author":"Faraday","year":"1986","journal-title":"J. Exp. Bot."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"1129","DOI":"10.1093\/jxb\/37.8.1129","article-title":"Functional aspects of the salt glands of the Plumbaginaceae","volume":"37","author":"Faraday","year":"1986","journal-title":"J. Exp. Bot."},{"key":"ref_102","unstructured":"Baker, D.A., and Hall, J.L. (1988). Solute Transport in Plant Cells and Tissues, Longman Scientific and Technical. Available online: https:\/\/www.amazon.com\/Transport-Tissues-Monographs-surveys-biosciences\/dp\/0582005809."},{"key":"ref_103","unstructured":"Wierzbicka, M., Bodzon, K., Trzybi\u0144ski, D., Bagiedka, M., and Wo\u017aniak, K. (Environ. Pollut., 2022). The pathway of lead in Armeria maritima shoots and its disposal by salt glands, Environ. Pollut., paper sent to print; will be completed."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1007\/s004250000399","article-title":"Accumulation of heavy metals in epidermal glands of the waterlily (Nymphaeaceae)","volume":"212","author":"Lavid","year":"2001","journal-title":"Planta"},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1007\/s004250100610","article-title":"Phenols and phenol oxidases are involved in cadmium accumulation in the water plants Nymphoides peltata (Menyanthaceae) and Nymphaeae (Nymphaeaceae)","volume":"214","author":"Lavid","year":"2001","journal-title":"Planta"},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1007\/s004250000400","article-title":"The involvement of polyphenols and peroxidase activities in heavy-metal accumulation by epidermal glands of the waterlily (Nymphaeaceae)","volume":"212","author":"Lavid","year":"2001","journal-title":"Planta"},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"674","DOI":"10.1126\/science.230.4726.674","article-title":"Phytochelatins: The principal heavy-metal complexing peptides of higher plants","volume":"230","author":"Grill","year":"1985","journal-title":"Science"},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1016\/0168-9452(90)90129-C","article-title":"Changes in glutathione and phytochelatins in roots of maize seedlings exposed to cadmium","volume":"70","author":"Tukendorf","year":"1990","journal-title":"Plant Sci."},{"key":"ref_109","first-page":"175","article-title":"The role of glutathione in detoxification of cadmium and excess of copper in spinach plants","volume":"15","author":"Tukendorf","year":"1993","journal-title":"Acta Physiol. Plant."},{"key":"ref_110","doi-asserted-by":"crossref","unstructured":"Prasad, M.N.V. (2004). Heavy Metal Stress in Plants, Springer.","DOI":"10.1007\/978-3-662-07743-6"},{"key":"ref_111","doi-asserted-by":"crossref","unstructured":"Sherameti, I., and Varma, A. (2011). Detoxification of Heavy Metals, Springer.","DOI":"10.1007\/978-3-642-21408-0"},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"547","DOI":"10.1016\/S0176-1617(99)80296-X","article-title":"Metal stress response and tolerance of cultured cells from Silene vulgaris and Lycopersicon peruvianum: Role of heat stress proteins","volume":"154","author":"Wollgiehn","year":"1999","journal-title":"J. Plant Physiol."},{"key":"ref_113","doi-asserted-by":"crossref","unstructured":"Baumbach, H. (2012). Metallophytes and Metallicolous Vegetation: Evolutionary Aspects, Taxonomic Changes and Conservational Status in Central Europe. Perspectives on Nature Conservation\u2014Patterns, Pressures and Prospects, InTech. Available online: https:\/\/www.intechopen.com\/books\/perspectives-on-nature-conservation-patterns-pressures-and-prospects\/metallophytes-and-metallicolous-vegetation-evolutionary-aspects-taxonomic-changes-and-conservational.","DOI":"10.5772\/30846"},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"3","DOI":"10.21248\/mfk.254","article-title":"Dynamik, genetische Struktur und Schutz kleiner Populationen\u2014Das Beispiel von Armeria maritima ssp. hornburgensis","volume":"7","author":"Baumbach","year":"2002","journal-title":"Mitt. Zur Florist. Kart. Sachs.-Anhalt."},{"key":"ref_115","first-page":"41","article-title":"Zur Situation von Armeria maritima ssp. Hornburgensis\u2014Aktuelle Daten zu Populationsgr\u00f6\u00dfe, Demographie und Taxonomie","volume":"11","author":"Baumbach","year":"2006","journal-title":"Mitt. Zur Florist. Kart. Sachs.-Anhalt."},{"key":"ref_116","unstructured":"Baumbach, H. (2005). Genetic Differentiation of Central-European Heavy-Metal Tolerant Populations of Silene vulgaris, Minuartia verna and Armeria maritima, Considering Biogeography, Physiology and Mining History [Genetische Differenzierung Mitteleurop\u00e4ischer Schwermetallsippen von Silene vulgaris, Minuartia verna und Armeria maritima unter Ber\u00fccksichtigung Biogeographischer, Montanhistorischer und Physiologischer Aspekte]. [Ph.D. Thesis, J. Cramer]. Available online: https:\/\/www.schweizerbart.de\/publications\/detail\/isbn\/9783443643119\/Genetische_Differenzierung_mitteleuropaischer_Schw."},{"key":"ref_117","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1002\/fedr.200811179","article-title":"Neue taxonomische Erkenntnisse zu den Charakterarten der Schwermetallvegetation und m\u00f6gliche Konsequenzen f\u00fcr den Schutz von Schwermetallstandorten","volume":"119","author":"Baumbach","year":"2008","journal-title":"Feddes Repert."},{"key":"ref_118","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1007\/s000360050017","article-title":"On the evolution of heavy-metal tolerant populations in Armeria maritima: Evidence from allozyme variation and reproductive barriers","volume":"10","author":"Vekemans","year":"1997","journal-title":"J. Evol. Biol."},{"key":"ref_119","first-page":"270","article-title":"Isozyme variation at the populational level in Armeria maritima","volume":"125","author":"Vekemans","year":"1992","journal-title":"Belg. J. Bot."},{"key":"ref_120","first-page":"31","article-title":"Variation \u00e9lectrophor\u00e9tique des est\u00e9rases des feuilles d\u2019Armeria maritima (Mill.) Willd.: Quelques aspects taxonomiques et \u00e9volutifs","volume":"114","author":"Kakes","year":"1981","journal-title":"Bull. Soc. R. Bot. Belg. Bull. K. Belg. Bot. Ver."},{"key":"ref_121","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1111\/j.1601-5223.1996.00237.x","article-title":"Variation in nuclear DNA content at the species level in Armeria maritima","volume":"124","author":"Vekemans","year":"1996","journal-title":"Hereditas"},{"key":"ref_122","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1016\/0305-1978(95)97456-7","article-title":"Flavonoid profiles variation in Armeria maritima (Mill.) Willd","volume":"23","author":"Lauranson","year":"1995","journal-title":"Biochem. Syst. Ecol."},{"key":"ref_123","first-page":"673","article-title":"Cytogenetic variation in populations of Armeria maritima (Mill.) Willd. in relation to geographical distribution and soil stress tolerances","volume":"77","author":"Coulaud","year":"1999","journal-title":"Can. J. Bot."},{"key":"ref_124","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1016\/j.pbi.2007.04.012","article-title":"The plant genome\u2019s methylation status and response to stress: Implications for plant improvement","volume":"10","author":"Lukens","year":"2007","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref_125","doi-asserted-by":"crossref","unstructured":"Meccariello, R. (2019). Epigenetics, IntechOpen.","DOI":"10.5772\/intechopen.77825"},{"key":"ref_126","doi-asserted-by":"crossref","first-page":"246","DOI":"10.3389\/fpls.2019.00246","article-title":"A role for epigenetic regulation in the adaptation and stress responses of non\u2212model plants","volume":"10","author":"Thiebaut","year":"2019","journal-title":"Front. Plant Sci."},{"key":"ref_127","doi-asserted-by":"crossref","first-page":"1807","DOI":"10.1007\/s13762-019-02215-8","article-title":"Heavy metal stress and responses in plants","volume":"16","author":"Ghori","year":"2019","journal-title":"Int. J. Environ. Sci. Technol."},{"key":"ref_128","doi-asserted-by":"crossref","first-page":"419","DOI":"10.1007\/s10661-019-7528-7","article-title":"The relative impact of toxic heavy metals (THMs) (arsenic (As), cadmium (Cd), chromium (Cr)(VI), mercury (Hg), and lead (Pb)) on the total environment: An overview","volume":"191","author":"Zeeshanur","year":"2019","journal-title":"Environ. Monit. Assess."},{"key":"ref_129","doi-asserted-by":"crossref","unstructured":"Furini, A. (2012). Plants and Heavy Metals, Springer.","DOI":"10.1007\/978-94-007-4441-7"},{"key":"ref_130","doi-asserted-by":"crossref","first-page":"1958","DOI":"10.1021\/acs.jafc.9b07468","article-title":"Emerging roles of microRNAs in plant heavy metal tolerance and homeostasis","volume":"68","author":"Ding","year":"2020","journal-title":"J. Agric. Food Chem."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/5\/4650\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T18:43:44Z","timestamp":1760121824000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/5\/4650"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,2,28]]},"references-count":130,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2023,3]]}},"alternative-id":["ijms24054650"],"URL":"https:\/\/doi.org\/10.3390\/ijms24054650","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,2,28]]}}}