Skip to main content
Log in

Phytochelatin-mediated cadmium tolerance inschizosaccharomyces pombe

  • Special—Bioremediation
  • Published:
In Vitro Cellular & Developmental Biology - Plant Aims and scope Submit manuscript

Summary

Plants and certain fungi respond to heavy metal toxicity with the induced synthesis of metal-binding peptides known as phytochelatins (PCs). With cadmium, PCs can bind the metal to form a low molecular weight PC-Cd complex and a high molecular weight PC-Cd-S2− complex. The sulfide ions enhance the stability and Cd-binding capacity of the metal chelate, and formation of this sulfide-containing complex is associated with enhanced tolerance to cadmium. Molecular analyses of two fission yeast mutants that fail to produce a wild type level of the PC-Cd-S2− complex have determined that a vacuolar membrane transporter and several enzymes of the purine biosynthesis pathway are necessary in vivo for formation of the PC- Cd-S2− complex. A model based on vacuolar sequestration of the PC-Cd complex by an ATP-binding cassette-type transporter and its subsequent maturation into the stable PC-Cd-S2− complex via the actions of two purine biosynthetic enzymes is described.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Abrahamson, S. L.; Speiser, D. M.; Ow, D. W. A gel electrophoresis assay for phytochelatins. Anal. Biochem. 200:239–243; 1992.

    Article  PubMed  CAS  Google Scholar 

  2. Cangelosi, G. A.; Martinetti, G.; Leigh, J. A., et al. Role ofAgrobacterium tumefaciens ChvA protein in export ofβ-1,2-glucan. J. Bacteriol. 171:1609–1615; 1989.

    PubMed  CAS  Google Scholar 

  3. Chen, C. M.; Misra, T. K.; Silver, S., et al. Nucleotide sequence of the structural genes for an anion pump. J. Biol. Chem. 261:15030–15038; 1986.

    PubMed  CAS  Google Scholar 

  4. Dameron, C. T.; Reese, R. N.; Mehra, R. K., et al. Biosynthesis of cadmium sulfide quantum semiconductor crystallites. Nature 338:596–597; 1989.

    Article  CAS  Google Scholar 

  5. Davis, R. H. Compartmental and regulatory mechanisms in the arginine pathway ofNeurospora crassa and Saccharomyces cerevisiae. Microbiol. Rev. 50:280–313; 1986.

    PubMed  CAS  Google Scholar 

  6. Delhaize, E.; Jackson, P. J.; Lujan, L. D., et al. Poly(γ-glutamycysteiny)glycine synthesis inDatura innoxia and binding with cadmium. Plant Physiol. 89:700–706; 1988.

    Google Scholar 

  7. Gekeler, W.; Grill, E.; Winnacker, E.-L., et al. Survey of the plant kingdom for the ability to bind heavy metals through phytochelatins. Z. Naturforsch. Teil C 44:361–369; 1989.

    CAS  Google Scholar 

  8. Grill, E.; Winnacker, E.-L.; Zenk, M. H. Phytochelatins: the principal heavy- metal complexing peptides of higher plants. Science 230:674–676; 1985.

    Article  CAS  PubMed  Google Scholar 

  9. Grill, E.; Gekeler, W.; Winnacker, E.-L., et al. Homo-phytochelatins are heavy metal-binding peptides of homo-glutathione containing Fabales. FEBS Lett. 207:47–50; 1986.

    Article  Google Scholar 

  10. Grill, E.; Winnacker, E.-L.; Zenk, M. H. Phytochelatins, a class of heavy- metal-binding peptides from plants, are functionally analogous to metallothioneins. Proc. Natl. Acad. Sci. USA 84:439–443; 1987.

    Article  PubMed  CAS  Google Scholar 

  11. Grill, E.; Löffler, S.; Winnacker, E.-L., et al. Phytochelatins, the heavy-metal-binding peptides of plants, are synthesized from glutathione by a specificγ-glutamylcysteine dipeptidyl transpeptidase (phytochelatin synthase). Proc. Natl. Acad. Sci. USA 86:6838–6842; 1989.

    Article  PubMed  CAS  Google Scholar 

  12. Hamer, D. H. Metallothionein. Annu. Rev. Biochem. 55:913–939; 1986.

    PubMed  CAS  Google Scholar 

  13. Hayashi, Y.; Nakagawa, C. W.; Mutoh, N., et al. Two pathways in the biosynthesis of cadystins (γEC)nG in the cell-free system of the fission yeast. Biochem. Cell Biol. 69:115–121; 1991.

    Article  PubMed  CAS  Google Scholar 

  14. Hess, J.; Wels, W.; Vogel, M., et al. Nucleotide sequence of a plasmidencoded hemolysin determinant and its comparison with a corresponding chromosomal hemolysin sequence. FEMS Microbiol. Lett. 34:1–11; 1986.

    Article  CAS  Google Scholar 

  15. Jackson, P. J.; Unkefer, C. J.; Doolen, J. A., et al. Poly (γ-glutamylcysteinyl) glycine: its role in cadmium resistance in plant cells. Proc. Natl. Acad. Sci. USA 84:6619–6623; 1987.

    Article  PubMed  CAS  Google Scholar 

  16. Juang, H.-R.; McCue, K. F.; Ow, D. W. Two purine biosynthetic enzymes that are required for cadmium tolerance inSchizosaccharomyces pombe utilize cysteine sulfinate in vitro. Arch. Biochem. Biophys. 304:392–401; 1993.

    Article  PubMed  CAS  Google Scholar 

  17. Juranka, P. F.; Zastawny, R. L.; Ling, V. P-glycoprotein: multidrug resistance and a superfamily of membrane associated transport proteins. FASEB J. 3:2583–2592; 1989.

    PubMed  CAS  Google Scholar 

  18. Kamijo, K.; Taketani, S.; Yokota, S., et al. The 70 kd peroxisomal membrane protein is a member of the Mdr (P-glycoprotein) related ATP binding protein superfamily. J. Biol. Chem. 265:4534–4539; 1990.

    PubMed  CAS  Google Scholar 

  19. Klionski, D. J.; Herman, P. K.; Emr, S. D. The fungal vacuole: composition function and biogenesis. Microbiol. Rev. 54:266–292; 1990.

    Google Scholar 

  20. Kondo, N.; Isobe, M.; Imai, K., et al. Structure of cadystin, the unitpeptide of cadmium binding peptides induced in a fission yeast,Schizosaccharomyces pombe. Tetrahedron Lett. 24:925–928; 1983.

    Article  CAS  Google Scholar 

  21. Kondo, N.; Imai, K.; Isobe, M., et al. 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; 1984.

    Article  CAS  Google Scholar 

  22. Laikind, P. K.; Seegmiller, L. E.; Gruber, H. E. Detection of 5′-phosphribosyl-4-(N-succinylcarboxamide)-5-aminoimidazole in urine by use of the Bratton-Marshall reaction: identification of patients deficient in adenylosuccinate lyase activity. Anal. Biochem. 156:81–90; 1986.

    Article  PubMed  CAS  Google Scholar 

  23. Loeffler, S.; Hochberger, A.; Grill, E., et al. Termination of the phytochelatin synthase reaction through sequestration of heavy metals by the reaction product. FEBS Lett. 258:42–46; 1989.

    Article  CAS  Google Scholar 

  24. Mehra, R. K.; Tarbet, E. B.; Gray, W. R., et al. Metal-specific synthesis of two metallothioneins andγ-glutamyl peptides inCandida glabrata. Proc. Natl. Acad. Sci. USA 85:8815–8819; 1988.

    Article  PubMed  CAS  Google Scholar 

  25. Murasugi, A.; Wada, C.; Hayashi, Y. Cadmium binding peptides induced in the fission yeastSchizosaccharomyces pombe. J. Biochem. 90:1561–1564; 1981.

    PubMed  CAS  Google Scholar 

  26. Murasugi, A.; Wada, C.; Hayashi, Y. Occurrence of acid labile sulfide in cadmium binding peptide 1 from fission yeast. J. Biochem. 93:661–664; 1983.

    PubMed  CAS  Google Scholar 

  27. Mutoh, N.; Hayashi, Y. Isolation of mutants ofSchizosaccharomyces pombe unable to synthesize cadystin, small cadmium-binding peptides. Biochem. Biophys. Res. Commun. 151:32–39; 1988.

    PubMed  CAS  Google Scholar 

  28. Ortiz, D. F.; Kreppel, L.; Speiser, D. M., et al. Heavy metal tolerance in the fission yeast requires an ATP-binding cassette-type vacuolar membrane transporter. EMBO J. 11:3491–3499; 1992.

    PubMed  CAS  Google Scholar 

  29. Porter, D. J. T.; Rudie, N. G.; Bright, H. J. Nitro analogs of substrates for adenylosuccinate synthetase and adenylosuccinate lyase. Arch. Biochem. Biophys. 225:157–163; 1983.

    Article  PubMed  CAS  Google Scholar 

  30. Rauser, W. E. Phytochelatins. Annu. Rev. Biochem. 56:61–86; 1990.

    Article  Google Scholar 

  31. Reese, R. N.; Mehra, R. K.; Tarbet, E. B., et al. Studies on theγ-glutamyl Cu-binding peptide fromSchizosaccharomyces pombe. J. Biol. Chem. 263:4186–4192; 1988.

    PubMed  CAS  Google Scholar 

  32. Reese, R. N.; Winge, D. R. Sulfide stabilization of the cadmium-γ-glutamyl peptide complex ofSchizosaccharomyces pombe. J. Biol. Chem. 263:12832–12835; 1988.

    PubMed  CAS  Google Scholar 

  33. Reese, R. N.; White, C. A.; Winge, D. R. Cadmium-sulfide crystallites in Cd- (γEC)nG peptide complexes from tomato. Plant Physiol. 98:225–229; 1992.

    PubMed  CAS  Google Scholar 

  34. Riordan, J. R.; Rommens, J. M.; Kerem, B. S., et al. Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 245:1066–1071; 1990.

    Article  Google Scholar 

  35. Robinson, N. J. Metal-binding polypeptides in plants. In: Shaw, A. J., ed. Heavy metal tolerance in plants: evolutionary aspects. Boca Raton, FL: CRC Press; 1990:195–214.

    Google Scholar 

  36. Speiser, D. M.; Abrahamson, S. L.; Banuelos, G., et al.Brassica juncea produces a phytochelatin-cadmium-sulfide complex. Plant Physiol. 99:817–821; 1992.

    PubMed  CAS  Google Scholar 

  37. Speiser, D. M.; Ortiz, D. F.; Kreppel, L., et al. Purine biosynthetic genes are required for cadmium tolerance inSchizosaccharomyces pombe. Mol. Cell. Biol. 12:5301–5310; 1992.

    PubMed  CAS  Google Scholar 

  38. Stayton, M. M.; Rudolph, F. B.; Fromm, H. J. Regulation, genetics, and properties of adenylosuccinate synthetase: a review. Curr. Topics Cell. Regul. 22:103–141; 1983.

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  40. Tomsett, A. B.; Thurman, D. A. Molecular biology of metal tolerance of plants. Plant Cell Environ. 11:383–394; 1988.

    Article  CAS  Google Scholar 

  41. Trowsdale, J.; Hanson, I.; Mockridge, I., et al. Sequences encoded in the class II region of the MHC related to the ABC superfamily of transporters. Nature 348:741–744; 1990.

    Article  PubMed  CAS  Google Scholar 

  42. Verkleij, J. A. C.; Koevoets, P.; Van’t Riet, J., et al. Poly (γ-glutamylcysteinyl)glycines or phytochelatins and their role in cadmium tolerance ofSilene vulgaris. Plant Cell Environ. 13:913–921; 1990.

    Article  CAS  Google Scholar 

  43. Vögeli-Lange, R.; Wagner, G. J. Subcellular localization of cadmium and cadmium binding peptides in tobacco leaves. Plant Physiol. 92:1086–1093; 1990.

    Article  PubMed  Google Scholar 

  44. Walker, J. E.; Saraste, M.; Runswick, J., et al. Distantly related sequences in theα-subunits andβ-subunits of ATP synthase, myosin, kinases and other ATP requiring enzymes and a common nucleotide binding fold. EMBO J. 1:945–951; 1982.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Presented in the Session-in-Depth Bioremediation through Biotechnological Means at the 1993 Congress on Cell and Tissue Culture, San Diego, CA, June 5–9, 1993.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ow, D.W. Phytochelatin-mediated cadmium tolerance inschizosaccharomyces pombe . In Vitro Cell Dev Biol - Plant 29, 213–219 (1993). https://doi.org/10.1007/BF02632037

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02632037

Key words

Navigation