Bryophytes and heavy metals: a review

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Bryophytes, a group of terrestrial plants widely used in biomonitoring, are reviewed for their relation to heavy metals. In the present article, we summarized the knowledge on heavy metals pollution and accumulation effects on bryophytes. Mechanisms of tolerance and resistance are given as well.

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  • Agarwal S. K. 2009: Heavy metal pollution (Vol. 4). APH publishing New Delhi.

  • Basile A. Cogoni A. E. Bassi P. Fabrizi E. Sorbo S. Giordano S. Cobianchi R. C. 2001: Accumulation of Pb and Zn in gametophytes and sporophytes of the moss Funaria hygrometrica (Funariales). Annals of Botany 87 537–543.

  • Basile A. Sorbo S. Aprile G. Conte B. Cobianchi R.C. Pisani T. Loppi S. 2009: Heavy metal deposition in the Italian “triangle of death” determined with the moss Scorpiurum circinatum. Environmental Pollution 157 2255–2260.

  • Basile A. Sorbo S. Pisani T. Paoli L. Munzi S. Loppi S. 2012: Bioacumulation and ultrastructural effects of Cd Cu Pb and Zn in the moss Scorpiurum circinatum (Brid.) Fleisch. & Loeske. Environmental Pollution 166 208–211.

  • Berg T. Røyset O. Steinnes E. 1995: Moss (Hylocomium splendens) used as biomonitor of atmospheric trace element deposition: estimation of uptake efficiencies. Atmospheric Environment 29 353–360.

  • Berg T. Steinnes E. 1997: Use of mosses (Hylocomium splendens and Pleuroziumschreberi) as biomonitors of heavy metal deposition: from relative to absolute deposition values. Environmental Pollution 98 61–71.

  • Boquete M. T. Bermúdez-Crespo J. Aboal J. R. Carballeira A. Fernández J. Á. 2014: Assessing the effects of heavy metal contamination on the proteome of the moss Pseudoscleropodium purum cross-transplanted between different areas. Environmental Science and Pollution Research 21 2191–2200.

  • Bruns I. Sutter K. Menge S. Neumann D. Krauss G. J. 2001: Cadmium lets increase the glutathione pool in bryophytes. Journal of Plant Physiology 158 79–89.

  • Canivet L. Dubot P. Garcon G. Denayer F. O. 2015: Effects of engineered iron nanoparticles on the bryophyte Physcomitrella patens (Hedw.) Bruch & Schimp. after foliar exposure. Ecotoxicology and Environmental Safety 113 499–505.

  • Carginale V. Sorbo S. Capasso C. Trinchella F. Cafiero G. Basile A. 2004: Accumulation localisation and toxic effects of cadmium in the liverwort Lunularia cruciata. Protoplasma 223 53–61.

  • Castello M. 2007: A comparison between two moss species used as transplants for airborne trace element biomonitoring in NE Italy. Environmental Monitoring and Assessment 133 267–276.

  • Chakrabortty S. Paratkar G. T. 2006: Biomonitoring of trace element air pollution using mosses. Aerosol and Air Quality Research 6 247–258.

  • Choudhury S. Panda S. K. 2005: Toxic effects oxidative stress and ultrastructural changes in moss Taxithelium nepalense (Schwaegr.) Broth. under chromium and lead phytotoxicity. Water Air Soil Pollution 167 73–90.

  • Claveri B. Morhain E. Mouvet C. 1994: A methodology for the assessment of accidental copper pollution using the aquatic moss Rhynchostegium riparioides. Chemosphere 28 2001–2010.

  • Couto J. A. Fernández J. A. Aboal J. R. Carballeira A. 2004: Active biomonitoring of element uptake with terrestrial mosses: a comparison of bulk and dry deposition. Science of the Total Environment 324 211–222.

  • Čeburnis D. Valiulis D. 1999: Investigation of absolute metal uptake efficiency from precipitation in moss. Science of the Total Environment 226 247–253.

  • Degola F. De Benedictis M. Petraglia A. Massimi A. Fattorini L. Sorbo S. Basile A. di Toppi L. S. 2014: A Cd/Fe/Znresponsive phytochelatin synthase is constitutively present in the ancient liverwort Lunularia cruciata (L.) Dumort. Plant and Cell Physiology 55 1884–1891.

  • Fernández J. A. Vazquez M. D. Lopez J. Carballeira A. 2006: Modelling the extra and intracellular uptake and discharge of heavy metals in Fontinalis antipyretica transplanted along a heavy metal and pH contamination gradient. Environmental Pollution 139 21–31.

  • Fernández J. Á. Pérez-Llamazares A. Carballeira A. Aboal J. R. 2013: Temporal variability of metal uptake in different cell compartments in mosses. Water Air Soil Pollution 224 1–9.

  • González A. G. Pokrovsky O. S. 2014: Metal adsorption on mosses: toward a universal adsorption model. Journal of Colloid and Interface Science 415 169–178.

  • Järup L. 2003: Hazards of heavy metal contamination. British Medical Bulletin 68 167–182.

  • Kelly M. G. Girton C. Whitton B. A. 1987: Use of moss-bags for monitoring heavy metals in rivers. Water Research 21 1429–1435.

  • Klos A. Czora M. Rajfur M. Wacławek M. 2012: Mechanisms for translocation of heavy metals from soil to epigeal mosses. Water Air Soil Pollution 223 1829–1836.

  • Koz B. Cevik U. 2014: Lead adsorption capacity of some moss species used for heavy metal analysis. Ecological Indicators 36 491–494.

  • Krzesłowska M. 2011: The cell wall in plant cell response to trace metals: polysaccharide remodeling and its role in defense strategy. Acta Physiologiae Plantarum 33 35–51.

  • Krzesłowska M. Rabeda I. Lewandowski M. Samardakiewicz S. Basinska A. Napieralska A. Mellerowicz E.J. Woznyl A. 2013: Pb induces plant cell wall modifications – in particular – the increase of pectins able to bind metal ions level. E3S Web of Conferences 1 26008.

  • Leblanc F. Rao D. N. 1974: A review of the literature on bryophytes with respect to air pollution. Bulletin de la Société Botanique de France 121(supl.2) 237–255.

  • Lee Jr R. E. Von Lehmden D. J. 1973: Trace metal pollution in the environment. Journal of the Air Pollution Control Association 23 853–857.

  • Little P. Martin M. H. 1974: Biological monitoring of heavy metal pollution. Environmental Pollution 6 1–19.

  • Maevskaya S. M. Kardash A. R. Demkiv O. T. 2001: Absorption of cadmium and lead ions by gametophyte of the moss Plagiomnium undulatum. Russian Journal of Plant Physiology 48 820–824.

  • Markert B. Weckert V. 1989: Use of Polytrichum formosum (moss) as a passive biomonitor for heavy metal pollution (cadmium copper lead and zinc). Science of the Total Environment 86 289–294.

  • Martin M. H. Coughtrey P. J 1982: Biological monitoring of heavy metal pollution: land and air. Applied Science London.

  • Nagajyoti P. C. Lee K. D. Sreekanth T. V. M. 2010: Heavy metals occurrence and toxicity for plants: a review. Environmental Chemistry Letters 8 199–216.

  • Nickrent D. L. Parkinson C. L. Palmer J. D. Duff R. J. 2000: Multigene phylogeny of land plants with special reference to bryophytes and the earliest land plants. Molecular Biology and Evolution 17 1885–1895.

  • Nieboer E. Richardson D. H. 1980: The replacement of the nondescript term ‘heavy metals’ by a biologically and chemically significant classification of metal ions. Environmental Pollution Series B Chemical and Physical 1 3–26.

  • Onianwa P. C. 2001: Monitoring atmospheric metal pollution: a review of the use of mosses as indicators. Environmental Monitoring and Assessment 71 13–50.

  • Panda S. K. Choudhury S. 2005: Changes in nitrate reductase activity and oxidative stress response in the moss Polytrichum commune subjected to chromium copper and zinc phytotoxicity. Brazilian Journal of Plant Physiology 17 191–197.

  • Pérez-Llamazares A. Aboal J. R. Carballeira A. Fernández J. A. 2011: Cellular location of K Na Cd and Zn in the moss Pseudoscleropodium purum in an extensive survey. Science of the Total Environment 409 1198–1204.

  • Rau S. Miersch J. Neumann D. Weber E. Krauss G. J. 2007: Biochemical responses of the aquatic moss Fontinalis antipyretica to Cd Cu Pb and Zn determined by chlorophyll fluorescence and protein levels. Environmental and Experimental Botany 59 299–306.

  • Reski R. 1998: Development genetics and molecular biology of mosses. Botanica Acta 111 1–15.

  • Rother M. Krauss G.J. Grass G. Wesenberg D. 2006: Sulphate assimilation under Cd2+ stress in Physcomitrella patens–combined transcript enzyme and metabolite profiling. Plant Cell and Environment 29 1801–1811.

  • Rühling Å. Tyler G. 1970: Sorption and retention of heavy metals in the woodland moss Hylocomium splendens (Hedw.) Br. et Sch. Oikos 21 92–97.

  • Sabovljević M. Skudnik M. Vujičić M. Pantović J. Nikolić N. Jeran Z. Batič F. Sabovljević A. 2014: Rain simulation with heavy metal deposition: effects of exposure duration and lead concentration on survival and development of the moss Hypnum cupressiforme. 6th Slovenian symposium on plant biology with international participation Hoce by Maribor Book of Abstracts 30.

  • Salemaa M. Derome J. Helmisaari H. S. Nieminen T. Vanha-Majamaa I. 2004: Element accumulation in boreal bryophytes lichens and vascular plants exposed to heavy metal and sulphur deposition in Finland. Science of the Total Environment 324 141–160.

  • Sassmann S. Wernitznig S. Lichtscheidl I. K. Lang I. 2010: Comparing copper resistance in two bryophytes: Mielichhoferia elongata Hornsch. versus Physcomitrella patens Hedw. Protoplasma 246 119–123.

  • Schröder W. Holy M. Pesch R. Harmens H. Ilyin I. Steinnes E. Alber R. Aleksiayenak Y. Blum O. Coşkun M. Dam M. 2010: Are cadmium lead and mercury concentrations in mosses across Europe primarily determined by atmospheric deposition of these metals? Journal of Soils and Sediments 10 1572–1584.

  • Shakya K. Chettri M. K. Sawidis T. 2008: Impact of heavy metals (copper zinc and lead) on the chlorophyll content of some mosses. Archives of Environmental Contamination and Toxicology 54 412–421.

  • Shaw J. 1987: Evolution of heavy metal tolerance in bryophytes. II. An ecological and experimental investigation of the” copper moss Scopelophila cataractae (Pottiaceae). American Journal of Botany 74 813–821.

  • Shaw J. Beer S. C. Lutz J. 1989: Potential for the evolution of heavy metal tolerance in Bryum argenteum a moss. I. Variation within and among populations. Bryologist 92 73–80.

  • Shaw J. Renzaglia K. 2004: Phylogeny and diversification of bryophytes. American Journal of Botany 91 1557–1581.

  • Shaw A. J. Szövényi P. Shaw B. 2011: Bryophyte diversity and evolution: windows into the early evolution of land plants. American Journal of Botany 98 352–369.

  • Singh R. Gautam N. Mishra A. Gupta R. 2011: Heavy metals and living systems: an overview. Indian Journal of Pharmacology 43 246–253.

  • Soudzilovskaia N. A. Cornelissen J. H. During H. J. van Longtestijn R. S. Lang S. I. Aerts R. 2010: Similar cation exchange capacities among bryophyte species refute a presumed mechanism of peatland acidification. Ecology 91 2716–2726.

  • Strotbek C. Krinninger S. Frank W. 2013: The moss Physcomitrella patens: methods and tools from cultivation to targeted analysis of gene function. International Journal of Developmental Biology 57 553–564.

  • Sun S. Q. He M. Cao T. Zhang Y. C. Han W. 2009: Response mechanisms of antioxidants in bryophyte (Hypnum plumaeforme) under the stress of single or combined Pb and/or Ni. Environmental Monitoring and Assessment 149 291–302.

  • Sun S. Q. He M. Cao T. Yusuyin Y. Han W. Li J. L. 2010: Antioxidative responses related to H2O2 depletion in Hypnum plumaeforme under the combined stress induced by Pb and Ni. Environmental Monitoring and Assessment 163 303–312.

  • Sutter K. Jung K. Krauss G. J. 2002: Effects of heavy metals on the nitrogen metabolism of the aquatic moss Fontinalis antipyretica L. ex Hedw. Environmental Science and Pollution Research 9 417–421.

  • Tipping E. Vincent C. D. Lawlor A. J. Lofts S. 2008: Metal accumulation by stream bryophytes related to chemical speciation. Environmental Pollution 156 936–943.

  • Tremper A. H. Agneta M. Burton S. Higgs D. E. 2004: Field and laboratory exposures of two moss species to low level metal pollution. Journal of Atmospheric Chemistry 49 111–120.

  • Varela Z. Roiloa S. R. Fernández J. A. Retuerto R. Carballeira A. Aboal J. R. 2013: Physiological and growth responses of transplants of the moss Pseudoscleropodium purum to atmospheric pollutants. Water Air & Soil Pollution 224 1–10.

  • Vazquez M. D. Lopez J. Carballeira A. 1999: Uptake of heavy metals to the extracellular and intracellular compartments in three species of aquatic bryophyte. Ecotoxicology and Environmental Safety 44 12–24.

  • Vukojević V. Sabovljević A. Sabovljević M. 2004: Effect of ferri(III)citrate and potassium hexacyanoferrate(III) on growth of the moss Bryum argenteum Hedw in vitro. Archives of Biological Sciences 56 75–78.

  • Wells J. M. Brown D. H. 1987: Factors affecting the kinetics of intra-and extracellular cadmium uptake by the moss Rhytidiadelphus squarrosus. New Phytologist 105 123–137.

  • Wells J. M. Brown D. H. 1990: Ionic control of intracellular and extracellular Cd uptake by the moss Rhytidiadelphus squarrosus (Hedw.) Warnst. New Phytologist 116 541–553.

  • Wells J. M. Brown D. H. Beckett R. P. 1995: Kinetic analysis of Cd uptake in Cd-tolerant and intolerant populations of the moss Rhytidiadelphus squarrosus (Hedw.) Warnst and the lichen Peltigera membranacea (Ach.) Nyl. New phytologist 129 477–486.

  • Wolterbeek B. 2002: Biomonitoring of trace element air pollution: principles possibilities and perspectives. Environmental Pollution 120 11–21.

  • Yadav S. K. 2010: Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. South African Journal of Botany 76 167–179.

  • Zechmeister H. G. Dirnböck T. Hülber K. Mirtl M. 2007: Assessing airborne pollution effects on bryophytes–lessons learned through long-term integrated monitoring in Austria. Environmental Pollution 147 696–705.

  • Zechmeister H. G. Hohenwallner D. Riss A. Hanus-Illnar A. 2003: Variations in heavy metal concentrations in the moss species Abietinella abietina (Hedw.) Fleisch. according to sampling time within site variability and increase in biomass. Science of the Total Environment 301 55–65.

  • Zengin F. K. Munzuroglu O. 2005: Effects of some heavy metals on content of chlorophyll proline and some antioxidant chemicals in bean (Phaseolus vulgaris L.) seedlings. Acta Biologica Cracoviensia Series Botanica 47 157–164.

  • Zvereva E. L. Kozlov M. V. 2011: Impacts of industrial polluters on bryophytes: a meta-analysis of observational studies. Water Air & Soil Pollution 218 573–586.

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