Effects of zinc and lead on seed germination of Helichrysum microphyllum subsp. tyrrhenicum, a metal-tolerant plant

  • M. E. Boi
  • M. PorcedduEmail author
  • G. Cappai
  • G. De Giudici
  • G. Bacchetta
Original Paper


The seed germination of Helichrysum microphyllum subsp. tyrrhenicum, an endemic species of Sardinia and Corsica with metal tolerance capability, was evaluated against zinc (Zn; 0, 250, 500 and 1000 mg/L) and lead (Pb; 0, 25, 50 and 100 mg/L) stress. Seeds were collected in three localities: (a) inside a mine dump highly polluted with these metals, (b) outside but close to this area and (c) far from the metal-polluted site. Germination responses were assessed at 10, 15 and 20 °C, and the percentage, time of germination and mortality of seedlings were evaluated. The taxon showed a high capacity to germinate under Zn and Pb stress, and the germination was never completely inhibited; however, the germination decreased with increasing Zn concentrations, but not under Pb stress. Moreover, the seeds from specimens growing in mining sites appeared to be less affected by Zn stress than seeds coming from the other localities. A successful survival of seedlings during the first days of their development under metal stress and under controlled conditions was detected. Our study suggests that this species may give an important contribution to future phytoremediation programs on mining sites, in which it could be spread by seeds in order to form a vegetation cover.


Germination test Heavy metals Mediterranean area Mine areas Phytoremediation 



This work is part of the research project REMINE-REstoration and remediation of abandoned MINE sites, funded by the Fondazione di Sardegna and Regional Sardinian Government (Grant CUP F72F16003160002). We gratefully acknowledge the University of Cagliari for the financial support of the PhD scholarship of Maria Enrica Boi (years 2015–2018).

Author contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by MEB and MP. All authors wrote the original manuscript and contributed substantially to the manuscript improvement and validation.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

13762_2019_2589_MOESM1_ESM.docx (30 kb)
Supplementary material 1 (DOCX 30 kb)


  1. Angiolini C, Bacchetta G, Brullo S, Casti M, Giusso Del Galdo G (2005) The vegetation of mining dumps in SW-Sardinia. Feddes Repert 116(3–4):243–276CrossRefGoogle Scholar
  2. Antunes Viegas D, Palmeira-de-Oliveira A, Salgueiro L, Martinez-de-Oliveira J, Palmeira-de-Oliveira R (2014) Helichrysum italicum: from traditional use to scientific data. J Ethnopharmacol 151(1):54–65CrossRefGoogle Scholar
  3. Aversa G, Balassone G, Boni M, Amalfitano G (2002) The mineralogy of the “calamine” ores in SW Sardinia (Italy): preliminary results. Period Mineral 71(3):201–218Google Scholar
  4. Bacchetta G, Brullo S, Mossa L (2003) Note sul genere Helichrysum Miller (Asteraceae) in Sardegna. Ital Bot 35(1):217–225Google Scholar
  5. Bacchetta G, Casti M, Zavattero L (2007) Analisi della vegetazione del distretto minerario di Montevecchio (Sardegna sud-occidentale). Fitosociologia 44(2):83–108Google Scholar
  6. Bacchetta G, Cao A, Cappai G, Carucci A, Casti M, Fercia ML, Lonis R, Mola F (2012) A field experiment on the use of Pistacia lentiscus L. and Scrophularia canina L. subsp. bicolor (Sm.) Greuter for the phytoremediation of abandoned mining areas. Plant Biosyst 146(4):1054–1063CrossRefGoogle Scholar
  7. Bacchetta G, Cappai G, Carucci A, Tamburini E (2015) Use of native plants for the remediation of abandoned mine sites in mediterranean semiarid environments. Bull Environ Contam Toxicol 94(3):326–333CrossRefGoogle Scholar
  8. Bacchetta G, Boi ME, Cappai G, De Giudici G, Piredda M (2017) Phytoremediation of Sardinian abandoned mine site: a preliminary study on the use of Helichrysum microphyllum Cambess. subsp. tyrrhenicum Bacch., Brullo & Giusso. Proceedings of the 15th international conference on environmental science and technology. Rhodes, Greece. Accessed 13 July 2017
  9. Bacchetta G, Boi ME, Cappai G, De Giudici G, Piredda M, Porceddu M (2018) Metal tolerance capability of Helichrysum microphyllum Cambess. subsp. tyrrhenicum Bacch., Brullo & Giusso: a candidate for phytostabilization in abandoned mine sites. Bull Environ Contam Toxicol 101(6):758–765CrossRefGoogle Scholar
  10. Barbafieri M, Dadea C, Tassi E, Bretzel F, Fanfani L (2011) Uptake of heavy metals by native species growing in a mining area in Sardinia, Italy: discovering native flora for phytoremediation. Int J Phytorem 13(10):985–997CrossRefGoogle Scholar
  11. Baskin CC, Baskin JM (2014) Seeds: ecology, biogeography, and evolution of dormancy and germination. Academic Press, San DiegoGoogle Scholar
  12. Bechstädt T, Boni M (1994) Sedimentological, stratigraphical and ore deposits field guide of the autochthonous Cambro–Ordovician of Southwestern Sardinia, Italy. Servizio Geologico d’Italia, RomeGoogle Scholar
  13. Boni M, Costabile S, De Vivo B, Gasparrini M (1999) Potential environmental hazard in the mining district of southern Iglesiente (SW Sardinia, Italy). J Geochem Explor 67(1):417–430CrossRefGoogle Scholar
  14. Cao A, Cappai G, Carucci A, Muntoni A (2004) Selection of plants for zinc and lead phytoremediation. J Environ Sci Health 39(4):1011–1024CrossRefGoogle Scholar
  15. Cao A, Carucci A, Lai T, Bacchetta G, Casti M (2009) Use of native species and biodegradable chelating agent in phytoremediation of abandoned mining area. J Chem Technol Biotechnol 84(6):884–889CrossRefGoogle Scholar
  16. Cidu R, Frau F, Da Pelo S (2011) Drainage at abandoned mine sites: natural attenuation of contaminants in different seasons. Mine Water Environ 30(2):113–126CrossRefGoogle Scholar
  17. Concas S, Lattanzi P, Bacchetta G, Babafieri M, Vacca A (2015) Zn, Pb and Hg contents of Pistacia lentiscus L. grown on heavy metal-rich soils: implications for phytostabilization. Water Air Soil Pollut 226(10):340–355CrossRefGoogle Scholar
  18. De Giudici G, Medas D, Meneghini C, Casu MA, Giannoncelli A, Iadecola A, Podda S, Lattanzi P (2015) Microscopic bio mineralization processes and Zn bioavailability: a synchrotron-based investigation of Pistacia lentiscus L. root. Environ Sci Pollut Res Int 22(24):19352–19361CrossRefGoogle Scholar
  19. De Giudici G, Pusceddu C, Medas D, Meneghini C, Giannoncelli A, Rimondi V, Podda F, Cidu R, Lattanzi P, Wanty RB, Kimball BA (2017) The role of natural biogeochemical barriers in limiting metal loading to a stream affected by mine drainage. Appl Geochem 76:124–135CrossRefGoogle Scholar
  20. Di Salvatore M, Carafa AM, Carratù G (2008) Assessment of heavy metals phytotoxicity using seed germination and root elongation tests: a comparison of two growth substrates. Chemosphere 73(9):1461–1464CrossRefGoogle Scholar
  21. Doumas P, Munoz M, Banni M, Becerra S, Bruneel O, Casiot C, Cleyet-Marel JC, Gardon J, Noack Y, Sappin-Didier V (2018) Polymetallic pollution from abandoned mines in Mediterranean regions: a multidisciplinary approach to environmental risks. Reg Environ Change 18(3):677–692CrossRefGoogle Scholar
  22. Frau F, Medas D, Da Pelo S, Wanty RB, Cidu R (2015) Environmental effects on the aquatic system and metal discharge to the mediterranean sea from a near-neutral zinc-ferrous sulfate mine drainage. Water Air Soil Pollut 226(3):1–17CrossRefGoogle Scholar
  23. Ginocchio R, León-Lobos P, Arellano EC, Anic V, Ovalle JF, Baker AJM (2017) Soil physicochemical factors as environmental filters for spontaneous plant colonization of abandoned tailing dumps. Environ Sci Pollut Res Int 24(15):13484–13496CrossRefGoogle Scholar
  24. Jadia CD, Fulekar MH (2008) Phytoremediation: the application of vermicompost to remove zinc, cadmium, copper, nickel and lead by sunflower plant. Environ Eng Manag J 7(5):547–558CrossRefGoogle Scholar
  25. Jiménez MN, Fernandez E, Navarro EB, Contini E, Casti M, Bacchetta G (2005) Livelli di metalli pesanti in Dittrichia viscosa (L.) Greuter, Cistus salviifolius L. e Euphorbia cupanii Bertol. ex Moris su suoli contaminati e non contaminati dalle attività estrattive nell’Iglesiente (Sardegna sudoccidentale). Ital Bot 37(1):794–795Google Scholar
  26. Jiménez MN, Bacchetta G, Casti M, Navarro FB, Lallena AM, Fernandèz-Ondono E (2011) Potential use in phytoremediation of three plant species growing on contaminated mine-tailing soils in Sardinia. Ecol Eng 37(2):392–398CrossRefGoogle Scholar
  27. Jiménez MN, Bacchetta G, Casti M, Navarro FB, Lallena AM, Fernandèz-Ondono E (2014) Study of Zn, Cu and Pb content in plants and contaminated soils in Sardinia. Plant Biosyst 148(3):419–428CrossRefGoogle Scholar
  28. Kabata-Pendias A (2011) Trace elements in soils and plants. CRC Press, Boca RatonGoogle Scholar
  29. Kranner I, Colville L (2011) Metals and seeds: biochemical and molecular implications and their significance for seed germination. Environ Exp Bot 72(1):93–105CrossRefGoogle Scholar
  30. Krichen K, Ben Mariem H, Chaieb M (2014) Ecophysiological requirements on seed germination of a Mediterranean perennial grass (Stipa tenacissima L.) under controlled temperatures and water stress. S Afr J Bot 94:210–217CrossRefGoogle Scholar
  31. Lefèvre I, Marchal G, Corréal E, Zanuzzi A, Lutts S (2009) Variation in response to heavy metals during vegetative growth in Dorycnium pentaphyllum Scop. Plant Growth Regul 59(1):1–11CrossRefGoogle Scholar
  32. Leonardi M, Ambryszewska KE, Melai B, Flamini G, Cioni PL, Parri F, Pistelli L (2013) Essential-oil composition of Helichrysum italicum (Roth) G. Don ssp. italicum from Elba Island (Tuscany, Italy). Chem Biodivers 10(3):343–355CrossRefGoogle Scholar
  33. Madzhugina YG, Kuzetsov V, Shevyakova NI (2008) Plants inhabiting polygons formegapolis waste as promising species for phytoremediation. Russ J Plant Physiol 55(3):410–419CrossRefGoogle Scholar
  34. Maheshwari R, Dubey R (2008) Inhibition of ribonuclease and protease activities in germinating rice seeds exposed to nickel. Acta Physiol Plant 30(6):863–872CrossRefGoogle Scholar
  35. Márquez-García B, Márquez C, Sanjosé I, Nieva FJJ, Rodríguez-Rubio P, Muñoz-Rodríguez AF (2013) The effects of heavy metals on germination and seedling characteristics in two halophyte species in Mediterranean marshes. Mar Poll Bull 70(1–2):119–124CrossRefGoogle Scholar
  36. Martínez-Fernández D, Walkera DJ, Romero-Espinara P, Flores P, del Río JA (2011) Physiological responses of Bituminaria bituminosa to heavy metals. J Plant Physiol 168(18):2206–2211CrossRefGoogle Scholar
  37. Medas D, De Giudici G, Casu MA, Musu E, Giannoncelli A, Iadecola A, Meneghini C, Tamburini E, Sprocati AR, Turnau K, Lattanzi P (2015) Microscopic processes ruling the bioavailability of Zn to roots of Euphorbia pithyusa L. pioneer plant. Environ Sci Technol 49(3):1400–1408CrossRefGoogle Scholar
  38. Medas D, De Giudici G, Pusceddu C, Casu MA, Birarda G, Vaccari L, Giannoncelli A, Meneghini C (2017) Impact of Zn excess on biomineralization processes in Juncus acutus grown in mine polluted sites. J Hazard Mater 370:98–107CrossRefGoogle Scholar
  39. Medas D, Boi ME, Bacchetta G, Cappai G, Carlomagno I, Casu MA, De Giudici G, Gianoncelli A, Meneghini C, Piredda M, Podda F, Porceddu M (2018) Mineral evolution at geosphere–biosphere interface: investigation on the endemic shrub Helichrysum microphyllum Cambess. subsp. tyrrhenicum Bacch., Brullo & Giusso growing in abandoned mining area. In: Geosciences for the environment, natural hazard and cultural heritage-Congress SGI-SIMP 2018, pp 545–545Google Scholar
  40. Mendez MO, Maier RM (2008) Phytostabilization of mine tailings in arid and semiarid environments—an emerging remediation technology. Environ Health Perspect 116(3):278–283CrossRefGoogle Scholar
  41. Monaci F, Trigueros D, Dingorance MD, Rossini-Oliva S (2019) Phytostabilization potential of Erica australis L. and Nerium oleander L.: a comparative study in the Riotinto mining area (SW Spain). Environ Geochem Health. CrossRefGoogle Scholar
  42. Picciau R, Serra S, Porceddu M, Bacchetta G (2019) Seed traits and germination behaviour of four Sardinian populations of Helichrysum microphyllum ssp. tyrrhenicum (Asteraceae) along an altitudinal gradient. Plant Biol 21(3):498–506CrossRefGoogle Scholar
  43. Porceddu M, Mattana E, Pritchard HW, Bacchetta G (2013) Thermal niche for in situ seed germination by Mediterranean mountain streams: model prediction and validation for Rhamnus persicifolia seeds. Ann Bot 112(9):1887–1897CrossRefGoogle Scholar
  44. R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.orgGoogle Scholar
  45. RAS - Regione Autonoma della Sardegna (2003) Assessorato della Difesa dell’Ambiente. Piano regionale di gestione dei rifiuti. Piano di bonifica siti inquinati.
  46. Seregin IV, Kozhevnikova AD (2005) Distribution of cadmium, lead, nickel, and strontium in imbibing maize caryopses. Russ J Plant Physiol 52(4):565–569CrossRefGoogle Scholar
  47. Wierzbicka M, Obidzinska J (1998) The effect of lead on seed imbibition and germination in different plant species. Plant Sci 137(2):155–171CrossRefGoogle Scholar
  48. Wong MH (2003) Ecological restoration of mine degraded soils, with emphasis on metal contaminated soils. Chemosphere 50(6):775–780CrossRefGoogle Scholar
  49. Yang Y, Wei X, Lu J, You J, Wang W, Shi R (2010) Lead-induced phytotoxicity mechanism involved in seed germination and seedling growth of wheat (Triticum aestivum L.). Ecotoxicol Environ Saf 73(8):1982–1987CrossRefGoogle Scholar
  50. Zavattero L, Casti M, Bacchetta G, Di Pietro R (2006) Analisi multi temporale del paesaggio del distretto minerario di Monteponi (Sardegna sud-occidentale). Rivista Italiana di telerilevamento 37:137–146Google Scholar

Copyright information

© Islamic Azad University (IAU) 2019

Authors and Affiliations

  1. 1.BG-SAR - Sardinian Germplasm Bank, HBK - Hortus Botanicus KaralitanusUniversity of CagliariCagliariItaly
  2. 2.DiSVA - Department of Life and Environmental Sciences, CCB - Centre for the Conservation of BiodiversityUniversity of CagliariCagliariItaly
  3. 3.DICAAR - Department of Civil and Environmental Engineering and ArchitectureUniversity of CagliariCagliariItaly
  4. 4.DSCG - Department of Chemical and Geological ScienceUniversity of CagliariMonserratoItaly

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