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Contributions of cell wall and metal-binding peptide to Cd- and Cu-tolerances in suspension-cultured cells of tomato

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Abstract

Possible roles of cell wall and cytoplasmic peptides in the tolerance of cells to Cu2+ and Cd2+ ions were studied in suspension-cultured cells of tomato (Lycopersicon esculentum L. cv. Palace). Cu2+ and Cd2+ ions inhibited growth of wild type cells at concentrations more than 100 and 200 μM, respectively. Tomato cells readily developed tolerance to Cd2+ ions up to 1 mM but not to Cu2+ ions, after repeated subculturings in the presence of the respective ions. Such a metal-specific adaptation of cells was not due to the difference in the total uptakes between Cd2+ and Cu2+ ions by cells. Wild-type cells accumulated Cd2+ preferentially into the cytoplasmic peptide fraction and Cu2+ into the cell-wall fraction, when grown under the subtoxic metal conditions. Under excess metal conditions, Cd-tolerant cells produced greater amounts of Cd-binding peptides in the cytoplasm and retained lesser amounts of Cd2+ ions in the cell wall than did wild-type cells. In contrast, tomato cells grown in the presence of Cu2+ ions synthesized no detectable amounts of Cu-binding peptides in the cytoplasm and retained most of the Cu2+ in the cell-wall fraction, irrespective of cell lines.

These results suggested that the cytoplasmic peptides rather than cell wall properties have a primary role in the response of tomato cells to excess metal environments.

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Abbreviations

GPC:

gel-permeation chromatography

HPLC:

high performance liquid chromatography

MT:

metallothionein

PC:

phytochelatin

PCMB:

p-chloromercuribenzoate

TFA:

trifluoroacetic acid

TTC:

2,3,5-triphenyltetrazolium chloride

References

  • Bennetzen, J.L. andT.L. Adams. 1984. Selection and characterization of cadmium-resistant suspension cultures of the wild tomatoLycopersicon peruvianum. Plant Cell Rep.3: 258–261.

    Article  CAS  Google Scholar 

  • DeVos, C.H.R., H. Schat, R. Vooijs andW.H.O. Ernst. 1989. Copper-induced damage to the permeability barrier in roots ofSilene cucubalus. J. Plant Physiol.135: 164–169.

    CAS  Google Scholar 

  • Dodds, J.H. andL.W. Roberts. 1985. Cell suspension cultures.In Experiments in Plant Tissue Culture. 2nd ed., pp 104–112, Cambridge Univ. Press, New York.

    Google Scholar 

  • Foy, C.D., R.L. Chaney andM.C. White. 1978. The physiology of metal toxicity in plants. Annu. Rev. Plant Physiol.29: 511–566.

    Article  CAS  Google Scholar 

  • Fujita, M. andT. Kawanishi. 1987. Cd-binding complexes from the root tissues of various higher plants cultivated in a Cd2+-containing medium. Plant Cell Physiol.28: 379–382.

    CAS  Google Scholar 

  • Gekeler, W., E. Grill, E-L. Winnacker andM.H. Zenk. 1989. Survey of the plant kingdom for the ability to bind heavy metals through phytochelatins. Z. Naturforsch44c: 361–369.

    Google Scholar 

  • Grill, E., E.-L. Winnacker andM.H. Zenk. 1985. Phytochelatins: the principal heavymetal complexing peptides of higher plants. Science230: 674–676.

    CAS  PubMed  Google Scholar 

  • —,—and—. 1987. Phytochelatins, a class of heavy-metal-binding peptides from plants, are functionally analogous to metallothioneins. Proc. Natl. Acad. Sci. USA84: 439–443.

    Article  PubMed  CAS  Google Scholar 

  • —,S. Löffler, E.L. Winnacker andM.H. Zenk. 1989. Phytochelatins, the heavy-metal-binding peptides of plants, are synthesized from glutathione by a specific γ-glutamylcysteine dipeptidyl transpeptidase (phytochelatin synthase). Proc. Natl. Acad. Sci. USA.86: 6838–6842.

    Article  PubMed  CAS  Google Scholar 

  • Huang, B., E. Hatch andP.B. Goldsbrough. 1987. Selection and characterization of cadmium tolerant cells in tomato. Plant Sci.52: 211–221.

    Article  CAS  Google Scholar 

  • Inouhe, M., R. Yamamoto andY. Masuda. 1987. UDP-Glucose level as a limiting factor for IAA-induced cell elongation inAvena coleoptile segments. Physiol. Plantarum.69: 49–54.

    Article  CAS  Google Scholar 

  • —,M. Hiyama, H. Tohoyama, M. Joho andT. Murayama. 1989. Cadmium-binding protein in a cadmium-resistant strain ofSaccharomyces cerevisiae. Biochim. Biophys. Acta993: 51–55.

    PubMed  CAS  Google Scholar 

  • —,A. Inagawa, M. Morita, H. Tohoyama, M. Joho andT. Murayama. 1991. Native cadmium-metallothionein from the yeastSaccharomyces cerevisiae: its primary structure and function in heavy-metal resistance. Plant Cell Physiol32: 475–482.

    CAS  Google Scholar 

  • Jackson, P.J., E.J. Roth, P.R. McClure andC.M. Naranjo. 1984. Selection, isolation, and characterization of cadmium-resistantDatura innoxia suspension cultures. Plant Physiol.75: 914–918.

    PubMed  CAS  Google Scholar 

  • Joho, M., A. Ishibe andT. Murayama. 1984. The injurious effect of heavy metal ions on the cell membrane inSaccharomyces cerevisiae. Trans. mycol. Soc. Japan25: 485–488.

    CAS  Google Scholar 

  • Kishinami, I. andJ.M. Widholm. 1986. Selection of copper and zinc resistantNicotiana plumbaginifolia cell suspension cultures. Plant Cell Physiol.27: 1263–1268.

    CAS  Google Scholar 

  • —and—. 1987. Characterization of Cu and Zn resistantNicotiana plumbaginifolia suspension cultures. Plant Cell Physiol.28: 203–210.

    CAS  Google Scholar 

  • Kondo, N., K. Imai, M. Isobe, T. Goto, A. Murasugi, C.W. Nakagawa, andY. Hayashi. 1984. Cadystin A and B, major unit peptides comprising cadmium binding peptides induced in a fission yeast—separation, revision of structures and synthesis. Tetrahedron Lett.25: 3869–3872.

    Article  CAS  Google Scholar 

  • Krotz, R.M., B.P. Evangelou andG.J. Wagner. 1989. Relationships between cadmium, zinc, Cd-peptide, and organic acid in tobacco suspension cells. Plant Physiol.91: 780–787.

    PubMed  CAS  Google Scholar 

  • Mathys, W. 1975. Enzymes of heavy-metal-resistant and non-resistant populations ofSilene cucubalus and their interaction with some heavy metalsin vitro andin vivo. Physiol. Plant.33: 161–165.

    Article  CAS  Google Scholar 

  • Matsumoto, Y., Y. Okada, K.-S. Min, S. Onozaka andK. Tanaka. 1990. Amino acids and peptides. XXVII. Synthesis of phytochelatin-related peptides and examination of their heavy metal-binding properties. Chem. Pharm. Bull.38: 2364–2368.

    PubMed  CAS  Google Scholar 

  • Mehra, R.K. andD.R. Winge. 1991. Metal ion resistance in fungi: Molecular mechanisms and their regulated expression. J. Cell. Biochem.45: 30–40.

    Article  PubMed  CAS  Google Scholar 

  • Murashige, T. andF. Skoog. 1962. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plantarum15: 473–479.

    Article  CAS  Google Scholar 

  • Murasugi, A., C. Wada andY. Hayashi. 1981. Purification and unique properties in UV and CD spectra of Cd-binding peptides 1 fromSchizosaccharomyces pombe. Biochem. Biophys. Res. Commun.103: 1021–1028.

    Article  PubMed  CAS  Google Scholar 

  • Nishizono, H., K. Kubota, S. Suzuki andF. Ishii. 1989. Accumulation of heavy metals in cell walls ofPolygonum cuspidatum roots from metalliferous habitats. Plant Cell Physiol.30: 595–598.

    CAS  Google Scholar 

  • Rauser, W.E. 1990. Phytochelatins. Annu. Rev. Biochem.59: 61–86.

    Article  PubMed  CAS  Google Scholar 

  • Reese, R.N. andG.J. Wagner. 1987. Effects of buthionine sulfoximine on Cd-binding peptide levels in suspension-cultured tobacco cells treated with Cd, Zn, or Cu. Plant Physiol.84: 574–577.

    PubMed  CAS  Google Scholar 

  • Robinson, N.J. 1989. Metal-binding polypeptides in plants.In A.J. Shaw ed., Heavy metal tolerance in plants: Evolutionary aspects. pp. 195–214. CRC Press, Inc., Boca Raton, Florida.

    Google Scholar 

  • Rüegsegger, A., D. Schmutz andC. Brunold. 1990. Regulation of glutathion synthesis by cadmium inPisum sativum L. Plant Physiol.93: 1579–1584.

    Article  PubMed  Google Scholar 

  • Scheller, H.V., B. Huang, E. Hatch andP.B. Goldsbrough. 1987. Phytochelatin synthesis and glutathione levels in response to heavy metals in tomato cells. Plant Physiol.85: 1031–1035.

    PubMed  CAS  Google Scholar 

  • Sheoran, I.S., H.R. Singal andR. Singh. 1990. Effect of cadmium and nickel on photosynthesis and the enzymes of the photosynthetic carbon reduction cycle in pigeonpea (Cajanus cajan L.). Photosynthesis Research23: 345–351.

    Article  CAS  Google Scholar 

  • Steffens, J.C. 1990. The heavy metal-binding peptides of plants. Annu. Rev. Plant Physiol. Plant Mol. Biol.41: 553–575.

    CAS  Google Scholar 

  • Thornton, B. andA.E.S. Macklon. 1989. Copper uptake by ryegrass seedlings; contribution of cell wall adsorption. J. Exp. Bot.40: 1105–1111.

    CAS  Google Scholar 

  • Thurman, D.A. andJ.L. Rankin. 1982. The role of organic acids in zinc tolerance inDeschampsia caespitosa. New Phytol.91: 629–635.

    Article  CAS  Google Scholar 

  • Verkleij, J.A.C. andH. Schat. 1990. Mechanisms of metal tolerance in higher plants.In A.J. Shaw ed., Heavy metal tolerance in plants: Evolutionary aspects. pp 179–193. CRC Press, Inc., Boca Raton, Florida.

    Google Scholar 

  • Wagner, G.J. andR.M., Krotz. 1989. Perspectives on Cd and Zn accumulation, accommodation and tolerance in plant cells: The role of Cd-binding peptide versus other mechanisms.In, D.H. Hamer and D.R. Winge eds Metal ion homeostasis: Molecular biology and chemistry. pp. 325–336. Alan R. Liss, Inc., New York.

    Google Scholar 

  • Woolhouse, H.W. 1983. Toxicity and tolerance in the responses of plants to metals.In Lange, O.L.,et al., eds., Encyclopedia of Plant Physiology, New Series, Vol. 12C. pp. 245–300. Springer-Verlag, New York.

    Google Scholar 

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Inouhe, M., Mitsumune, M., Tohoyama, H. et al. Contributions of cell wall and metal-binding peptide to Cd- and Cu-tolerances in suspension-cultured cells of tomato. Bot Mag Tokyo 104, 217–229 (1991). https://doi.org/10.1007/BF02489454

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