Skip to main content
SpringerLink
Log in

Lead tolerance and accumulation in the gametophytes of the fern Athyrium yokoscense

  • Original Article
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

The fern Athyrium yokoscense is known to be highly tolerant to lead toxicity, and is a lead hyperaccumulator that can accumulate over 1,000 μg g−1 of lead in its dry matter. In this work, we examined whether the gametophytic generation of A. yokoscense also resists lead toxicity like the sporophytic generation. Spore germination in A. yokoscense was more tolerant to Pb2+, compared to that in other fern species, such as Pteridium aquilinum, Lygodium japonicum and Pteris vittata. In addition, the early gametophyte development of A. yokoscense was not much affected by 10 μM Pb2+, as evaluated from the prothallial growth and rhizoid development. We also showed that Athyrium gametophytes could accumulate more than 10,000 μg g−1 of lead, and that the lead was localized in the cytosol and vacuole of rhizoidal cells, as determined by a transmission electron micrograph. These results indicate that Athyrium gametophytes have the ability to accumulate lead in the rhizoids. Furthermore, the gametophytes were found to include a large amount of proanthocyanidins (condensed tannins). Because proanthocyanidins have a latent ability to complex with lead ions, the possible roles of proanthocyanidins in the lead tolerance and accumulation of Athyrium gametophytes are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4A–D
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Antosiewicz D, Wierzbicka M (1999) Localization of lead in Allium cepa L. cells by electron microscopy. J Microsc 195:139–146

    Google Scholar 

  • Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements—a review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126

    Google Scholar 

  • Banks JA (1999) Gametophyte development in ferns. Annu Rev Plant Physiol Plant Mol Biol 50:163–186

    Google Scholar 

  • Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182 (10.1146/annurev.arplant.53.100301.135154)

    Google Scholar 

  • Eun S-O, Youn HS, Lee Y (2000) Lead disturbs microtubule organization in the root meristem of Zea mays. Physiol Plant 110:357–365

    Google Scholar 

  • Francesconi K, Visoottiviseth P, Sridokchan W, Goessler W (2002) Arsenic species in an arsenic hyperaccumulating fern, Pityrogramma calomelanos: a potential phytoremediator of arsenic-contaminated soils. Sci Total Env 284:27–35 (10.1016/S0048-9697(01)00854-3)

    Google Scholar 

  • Gumaelius L, Lahner B, Salt DE, Banks JA (2004) Arsenic hyperaccumulation in gametophytes of Pteris vittata. A new model system for analysis of arsenic hyperaccumulation. Plant Physiol 136:3198–3208 (10.1104/pp.104.044073)

    Google Scholar 

  • Gutmann M, Feucht W (1991) A new method for selective localization of flavan-3-ols in plant tissues involving glycolmethacrylate embedding and microwave irradiation. Histochemistry 96:83–86

    Google Scholar 

  • Hickok LG, Warne TR, Slocum MK (1987) Ceratopteris richardii: applications for experimental plant biology. Am J Bot 74:1304–1316

    Google Scholar 

  • Ho YB, Tai KM (1985) Potential use of a roadside fern (Pteris vittata) to biomonitor Pb and other aerial metal deposition. Bull Env Contam Toxicol 35:430–438

    Google Scholar 

  • Honjo T, Suganuma H, Satomi N (1980) The vegetation of the pollution areas caused by the lead tile in Kanazawa Castle. J Phytogeogr Taxon 27:70–73

    Google Scholar 

  • Honjo T, Hatta A, Taniguchi K (1984) Characterization of heavy metals in indicator plants—studies on the accumulation of lead and tolerance of gregarious fern, Athyrium yokoscense, in the polluted areas from the lead tile of the ruins of Kanazawa Castle, now the campus of Kanazawa University. J Phytogeogr Taxon 32:68–80

    Google Scholar 

  • Krämer U, Cotter-Howells JD, Charnock JM, Baker AJM, Smith JAC (1996) Free histidine as a metal chelator in plants that accumulate nickel. Nature 379:635–638

    Google Scholar 

  • Lavid N, Schwartz A, Yarden O, Tel-Or E (2001) The involvement of polyphenols and peroxidase activities in heavy-metal accumulation by epidermal glands of the waterlily (Nymphaeaceae). Planta 212:323–331 (10.1007/s004250000400)

    Google Scholar 

  • Lees GL, Suttill NH, Gruber MY (1993) Condensed tannins in sainfoin. 1. A histological and cytological survey of plant tissues. Can J Bot 71:1147–1152

    Google Scholar 

  • Lichtenberger O, Neumann D (1997) Analytical electron microscopy as a powerful tool in plant cell biology: examples using electron energy loss spectroscopy and X-ray microanalysis. Eur J Cell Biol 73:378–386

    Google Scholar 

  • Ma JF (2000) Role of organic acids in detoxification of aluminum in higher plants. Plant Cell Physiol 41:383–390

    Google Scholar 

  • Ma LQ, Komar KM, Tu C, Zhang W, Cai Y, Kennelley ED (2001) A fern that hyperaccumulates arsenic. Nature 409:579

    Google Scholar 

  • Marles MAS, Ray H, Gruber MY (2003) New perspectives on proanthocyanidin biochemistry and molecular regulation. Phytochemistry 64:367–383 (10.1016/S0031-9422(03)00377-7)

    Google Scholar 

  • Neumann D, Zur Nieden U, Lichtenberger O, Leopold I (1995) How does Armeria maritima tolerate high heavy metal concentrations? J Plant Physiol 146:704–717

    Google Scholar 

  • Nishizono H, Ichikawa H, Suzuki S, Ishii F (1987a) The role of the root cell wall in the heavy metal tolerance of Athyrium yokoscense. Plant Soil 101:15–20

    Google Scholar 

  • Nishizono H, Suzuki S, Ishii F (1987b) Accumulation of heavy metals in the metal-tolerant fern, Athyrium yokoscense, growing on various environments. Plant Soil 102:65–70

    Google Scholar 

  • Nishizono H, Minemura H, Suzuki S, Ishii F (1988) An inducible copper-thiolate complex in the fern, Athyrium yokoscense: involvement in copper-tolerance of the fern. Plant Cell Physiol 29:1345–1351

    Google Scholar 

  • Nishizono H, Watanabe T, Orii T, Suzuki S (1989) Suppression of inhibitory effects of copper on enzymatic activities by copper-binding substances from Athyrium yokoscense assayed in vitro. Plant Cell Physiol 30:565–569

    Google Scholar 

  • Palma G, Freer J, Baeza J (2003) Removal of metal ions by modified Pinus radiata bark and tannins from water solutions. Water Res 37:4974–4980 (10.1016/j.watres.2003.08.008)

    Google Scholar 

  • Racusen RH (2002) Early development in fern gametophytes: interpreting the transition to prothallial architecture in terms of coordinated photosynthate production and osmotic ion uptake. Ann Bot 89:227–240 (10.1093/aob/mcf032)

    Google Scholar 

  • Raghavan V (1989) Developmental biology of fern gametophytes. Cambridge University Press, Cambridge

  • Salt DE, Smith RD, Raskin I (1998) Phytoremediation. Annu Rev Plant Physiol Plant Mol Biol 49:643–668 (10.1146/annurev.arplant.49.1.643)

    Google Scholar 

  • Sato T, Sakai A (1980) Freezing resistance of gametophytes of the temperate fern, Polystichum retroso-paleaceum. Can J Bot 58:1144–1148

    Google Scholar 

  • Sato T, Sakai A (1981) Cold tolerance of gametophytes and sporophytes of some cool temperate ferns native to Hokkaido. Can J Bot 59:604–608

    Google Scholar 

  • Satomi N (1958) On the relation between Athyrium yokoscense and copper mine. J Phytogeogr Taxon 7:26

    Google Scholar 

  • Singh J, Devi S, Chawla G, Gupta M, Viswanathan PN (1991) Ultrastructural and biochemical effects of cadmium on the aquatic fern Marsilea minuta Linn. Ecotoxicol Env Saf 21:171–181

    Google Scholar 

  • Smith DL (1972) Staining and osmotic properties of young gametophytes of Polypodium vulgare L. and their bearing on rhizoid function. Protoplasma 74:465–479

    Google Scholar 

  • Stoutjesdijk PA, Sale PW, Larkin PJ (2001) Possible involvement of condensed tannins in aluminium tolerance of Lotus pedunculatus. Aust J Plant Physiol 28:1063–1074 (10.1071/PP01012)

    Google Scholar 

  • Sugai M (1999) Developmental biology in fern gametophytes—contributions by Japanese researchers. Plant Morphol 11:32–41

    Google Scholar 

  • Tomizawa K-I, Manabe K, Sugai M (1982) Changes in phytochrome content during imbibition in spores of the fern Lygodium japonicum. Plant Cell Physiol 23:1305–1308

    Google Scholar 

  • Tung G, Temple PJ (1996) Histochemical detection of lead in plant tissues. Env Toxicol Chem 15:906–914

    Google Scholar 

  • Wada M, Kadota A (1989) Photomorphogenesis in lower green plants. Annu Rev Plant Physiol Plant Mol Biol 40:169–191 (10.1146/annurev.pp.40.060189.001125)

    Google Scholar 

  • Wang J, Zhao F-J, Meharg AA, Raab A, Feldmann J, McGrath SP (2002) Mechanisms of arsenic hyperaccumulation in Pteris vittata. Uptake kinetics, interactions with phosphate, and arsenic speciation. Plant Physiol 130:1552–1561 (10.1104/pp.008185)

    Google Scholar 

  • Waterman PG, Mole S (1994) Analysis of phenolic plant metabolites. Blackwell Scientific, Oxford

    Google Scholar 

  • Wenzel WW, Jockwer F (1999) Accumulation of heavy metals in plants grown on mineralised soils of the Austrian Alps. Env Pollut 104:145–155

    Google Scholar 

  • Wierzbicka M (1998) Lead in the apoplast of Allium cepa root tips: ultrastructural studies. Plant Sci 133:105–119

    Google Scholar 

  • Wierzbicka M (1999) The effect of lead on the cell cycle in the root meristem of Allium cepa L. Protoplasma 207:186–194

    Google Scholar 

  • Winkel-Shirley B (2001) Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126:485–493

    Google Scholar 

  • Xian X (1990) Relationship between distribution of cadmium in root tissue and Cd-tolerance of Athyrium yokoscense. J Env Sci Health A25:621–628

    Google Scholar 

  • Yoshihara T, Tsunokawa K, Miyano Y, Arashima Y, Hodoshima H, Shoji K, Shimada H, Goto F (2005) Induction of callus from a metal hypertolerant fern, Athyrium yokoscense, and evaluation of its cadmium tolerance and accumulation capacity. Plant Cell Rep 23:579–585 (10.1007/s00299-004-0877-9)

    Google Scholar 

  • Zhan X-M, Zhao X (2003) Mechanism of lead adsorption from aqueous solutions using an adsorbent synthesized from natural condensed tannin. Water Res 37:3905–3912 (10.1016/S0043-1354(03)00312-9)

    Google Scholar 

  • Zhang W, Cai Y, Downum KR, Ma LQ (2004) Thiol synthesis and arsenic hyperaccumulation in Pteris vittata (Chinese brake fern). Env Pollut 129:69–78 (10.1016/j.envpol.2003.09.020)

    Google Scholar 

Download references

Acknowledgements

We are grateful to Prof. Michizo Sugai (Toyama University) for the kind gift of the spores of Pteridium aquilinum.

Author information

Authors and Affiliations

  1. Department of Environmental Biology and Chemistry, Faculty of Science, Toyama University, 3190 Gofuku, Toyama, 930-8555, Japan

    Hiroyuki Kamachi, Ippei Komori, Yoshimi Sawa, Munenori Noguchi & Hiroshi Inoue

  2. Biotechnology Group, Energy Application R&D Center, Chubu Electric Power Co., Midori-ku, Nagoya, 459-8522, Japan

    Hideo Tamura

  3. Department of Biology, Faculty of Science, Toyama University, 3190 Gofuku, Toyama, 930-8555, Japan

    Ichirou Karahara & Yoshihiro Honma

  4. Center for Far Eastern Studies, Toyama University, 3190 Gofuku, Toyama, 930-8555, Japan

    Naoya Wada

  5. Department of Materials Science and Engineering, Faculty of Engineering, Toyama University, 3190 Gofuku, Toyama, 930-8555, Japan

    Tokimasa Kawabata, Kenji Matsuda & Susumu Ikeno

Authors
  1. Hiroyuki Kamachi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ippei Komori
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hideo Tamura
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yoshimi Sawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ichirou Karahara
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yoshihiro Honma
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Naoya Wada
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Tokimasa Kawabata
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Kenji Matsuda
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Susumu Ikeno
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Munenori Noguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Hiroshi Inoue
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hiroyuki Kamachi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kamachi, H., Komori, I., Tamura, H. et al. Lead tolerance and accumulation in the gametophytes of the fern Athyrium yokoscense. J Plant Res 118, 137–145 (2005). https://doi.org/10.1007/s10265-005-0202-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-005-0202-x

Keywords

Search

Navigation