Functional characterisation of two phytochelatin synthases in rice (Oryza sativa cv. Milyang 117) that respond to cadmium stress
Tóm tắt
Abstract Cadmium (Cd) is one of the most toxic heavy metals and a non‐essential element to all organisms, including plants; however, the genes involved in Cd resistance in plants remain poorly characterised.To identify Cd resistance genes in rice, we screened a rice cDNA expression library treated with CdCl2 using a yeast (Saccharomyces cerevisiae) mutant ycf1 strain (DTY167) and isolated two rice phytochelatin synthases (OsPCS5 and OsPCS15).The genes were strongly induced by Cd treatment and conferred increased resistance to Cd when expressed in the ycf1 mutant strain. In addition, the Cd concentration was twofold higher in yeast expressing OsPCS5 and OsPCS15 than in vector‐transformed yeast, and OsPCS5 and OsPCS15 localised in the cytoplasm. Arabidopsis thaliana plants overexpressing OsPCS5/‐15 paradoxically exhibited increased sensitivity to Cd, suggesting that overexpression of OsPCS5/‐15 resulted in toxicity due to excess phytochelatin production in A. thaliana.These data indicate that OsPCS5 and OsPCS15 are involved in Cd tolerance, which may be related to the relative abundances of phytochelatins synthesised by these phytochelatin synthases.
Từ khóa
#Cadmium #heavy metal tolerance #Oryza sativa #phytochelatin synthase #YCF1Tài liệu tham khảo
Blum R., Meyer K.C., Wünschmann J., Lendzian K.J., Grill E. (2010) Cytosolic action of phytochelatin synthase. Plant Physiology, 153, 159–169.
Clemens S. (2006) Evolution and function of phytochelatin synthases. Journal of Plant Physiology, 163, 319–332.
Clemens S., Kim E.J., Neumann D., Schroeder J.I. (1999) Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast. EMBO Journal, 18, 3325–3333.
Clough S.J., Bent A.F. (1998) Floral dip: a simplified method for Agrobacterium‐mediated transformation of Arabidopsis thaliana. The Plant Journal, 16, 735–743.
Cobbett C.S. (2000a) Phytochelatins and their roles in heavy metal detoxification. Plant Physiology, 123, 825–832.
Cobbett C.S. (2000b) Phytochelatin biosynthesis and function in heavy‐metal detoxification. Current Opinion in Plant Biology, 3, 211–216.
Cobbette C.S., May M.J., Howden R., Rolls B. (1998) The glutathione‐deficient, cadmium‐sensitive mutant, cad2‐1, of Arabidopsis thaliana is deficient in γ‐glutamylcysteine synthetase. The Plant Journal, 16, 73–78.
Cunningham S.D., Betri W.R., Huang J.W. (1995) Phytoremediation of contaminated soils. Trends in Biotechnology, 13, 393–397.
DalCorso G., Farinati S., Maistri S., Furini A. (2008) How plants cope with cadmium: staking all on metabolism and gene expression. Journal of Integrative Plant Biology, 50, 1268–1280.
Domínguez‐Solís J.R., Gutiérrez‐Alcalá G., Romero L.C., Gotor C. (2001) The cytosolic O‐acetylserine(thiol)lyase gene is regulated by heavy metals and can function in cadium tolerance. Journal of Biological Chemistry, 276, 9297–9302.
Gasic K., Korban S.S. (2007) Expression of Arabidopsis phytochelatin synthase in Indian mustard (Brassica juncea) plants enhances tolerance for Cd and Zn. Planta, 225, 1277–1285.
Ghosh M., Shen J., Rosen B.P. (1999) Pathways of As (III) detoxification in Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences of the United States of America, 96, 5001–5006.
Gietz R.D., Schiestl R.H. (1995) Transforming yeast with DNA. Methods in Molecular Biology, 5, 255–269.
Gisbert C., Ros R., De Haro A., Walker D.J., Bernal M.P., Serrano R., Navarro‐Aviñó J. (2003) A plant genetically modified that accumulates Pb is especially promising for phytoremediation. Biochemical and Biophysical Research Communications, 303, 440–445.
Grill E., Winnacker E.L., Zenk M.H. (1985) Phytochelatin: the principal heavy‐metal complexing peptides of higher plants. Science, 230, 674–676.
Grill E., Loeffer S., Winnacker E.L., Zenk M.H. (1989) Phytochelatins, the heavy‐metal‐binding peptides of plants, are synthesized from glutathione by a specific γ‐glutamylcysteine dipeptidyl transpeptidase (phytochelatin synthase). Proceedings of the National Academy of Sciences of the United States of America, 86, 6838–6842.
Ha S.B., Smith A.P., Howden R., Dietrich W.M., Bugg S., O'Connel M.J., Goldsbrough P.B., Cobbett C.S. (1999) Phytochelatin synthase genes from Arabidopsis and the yeast Schizosaccharomyces pombe. The Plant Cell, 11, 1153–1164.
Hayashi Y., Nakagawa C.W., Mutoh N. (1991) Two pathways in the biosynthesis of cadystins (γ‐EC)n‐G in the cell‐free system of the fission yeast. Biochemistry and Cell Biology, 69, 115–121.
He S.Y., He Z.L., Yang X.E., Stoffella P.J., Baligar V.C. (2015) Soil biogeochemistry, plant physiology, and phytoremediation of cadmium‐contaminated soils. Advances in Agronomy, 134, 135–225.
Herbette S., Taconnat L., Hugouvieux V., Piette L., Magniette M.‐L.M., Cuine S., Auroy P., Richaud P., Forestier C., Bourguignon J., Renou J.‐P., Vavasseur A., Leonhardt N. (2006) Genome‐wide transcriptome profiling of the early cadmium response of Arabidopsis roots and shoots. Biochimie, 88, 1751–1765.
Howden R., Cobbette C.S. (1992) Cadmium sensitive mutants of Arabidopsis thaliana. Plant Physiology, 99, 100–107.
Howden R., Goldsbrough P.B., Andersen C.R., Cobbette C.S. (1995) Cadmium‐sensitive, cad1 mutants of Arabidopsis thaliana are phytochelatin deficient. Plant Physiology, 107, 1059–1066.
Kim Y.‐Y., Kim D.‐Y., Shim D., Song W.‐Y., Lee J., Schroeder J.I., Kim S., Moran N., Lee Y. (2008) Expression of the novel wheat gene TM20 confers enhanced cadmium tolerance to baker's yeast. Journal of Biological Chemistry, 283, 15893–15902.
Krämer U. (2005) Phytoremediation: novel approaches to cleaning up polluted soils. Current Opinion in Biotechnology, 16, 133–141.
Lee S., Moon J.S., Ko T.S., Petros D., Goldsbrough P.B., Korban S.S. (2003a) Overexpression of Arabidopsis phytochelatin synthase paradoxically leads to hypersensitivity to cadmium stress. Plant Physiology, 131, 656–663.
Lee S., Petros D., Moon J.S., Ko T.S., Goldsbrough P.B., Korban S.S. (2003b) Higher levels of ectopic expression of Arabidopsis phytochelatin synthase do not lead to increased cadmium tolerance and accumulation. Plant Physiology and Biochemistry, 41, 903–910.
Li Z.‐S., Szczypka M., Lu Y.‐P., Thiele D.J., Rea P.A. (1996) The yeast cadmium factor protein (YCF1) is a vacuolar glutathione S‐conjugate pump. Journal of Biological Chemistry, 271, 6509–6517.
Li Z.‐S., Lu Y.‐P., Zhen R.‐G., Szczypka M., Thiele D.J., Rea P.A. (1997) A new pathway for vacuolar cadmium sequestration in Saccharomyces cerevisiae: YCF1‐catalyzed transport of bis(glutathionato)cadmium. Proceedings of the National Academy of Sciences of the United States of America, 94, 42–47.
Li Y., Dhankher O.P., Carreira L., Lee D., Chen A., Schroeder J.I., Balish R.S., Meagher R.B. (2004) Overexpression of phytochelatin synthase in Arabidopsis leads to enhanced arsenic tolerance and cadmium hypersensitivity. Plant and Cell Physiology, 45, 1787–1797.
Li J.C., Guo J.B., Xu W.Z., Ma M. (2006) Enhanced cadmium accumulation in transgenic tobacco expressing the phytochelatin synthase gene of Cynodon dactylon. Journal of Integrative Plant Biology, 48, 928–937.
Li J.C., Guo J.B., Xu W.Z., Ma M. (2007) RNA interference‐mediated silencing of phytochelatin synthase gene reduce cadmium accumulation in rice seeds. Journal of Integrative Plant Biology, 49, 1032–1037.
Liao V.H.‐C., Dong J., Freedman J.H. (2002) Molecular characterization of a novel, cadmium‐inducible gene from the nematode Caenorhabditis elegans. Journal of Biological Chemistry, 277, 42049–42059.
Maitani T., Kubota H., Sato K., Yamada T. (1996) The composition of metals bound to class III metallothionein (phytochelatin and its desglycyl peptide) induced by various metals in root cultures of Rubia tinctorum. Plant Physiology, 110, 1145–1150.
Martinez M., Bernal P., Almela C., Vélez D., Agustin G.P., Serrano R., Avinó N.J. (2006) An engineered plant that accumulates higher levels of heavy metals than Thlaspi caerulescens, with yields of 100 times more biomass in mine soils. Chemosphere, 64, 478–485.
Mengel K., Kirkby E.A. (2001) Principles of plant nutrition (5thedition). Kluwer Academic, Dordrecht, the Netherlands.
Merle S.S., Cuiné S., Carrier P., Pradines L.C., Luu D.T., Peltier G. (2003) Enhanced toxic metal accumulation in engineered bacterial cells expressing Arabidopsis thaliana phytochelatin synthase. Applied and Environmental Microbiology, 69, 490–494.
Murashige T., Skoog F. (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiologia Plantarum, 15, 473–497.
Nriagu J.O., Pacyna J.M. (1988) Quantitative assessment of worldwide contamination of air, water and soils by trace metals. Nature, 333, 134–139.
Ortiz D.F., Kreppel L., Speiser D.M., Dcheel G., McDonald G., Ow D.W. (1992) Heavy metal tolerance in the fission yeast requires an ATP‐binding cassette‐type vacuolar membrane transporter. EMBO Journal, 11, 3491–3499.
Oven M., Page J.E., Zenk M.H., Kutchan T.M. (2002) Molecular characterization of the homo‐phytochelatin synthase of soybean Glycine max: relation to phytochelatin synthase. Journal of Biological Chemistry, 277, 4747–4754.
Park H.C., Kang Y.H., Chun H.J., Koo J.C., Cheong Y.H., Kim C.Y., Kim M.C., Chung W.S., Kim J.C., Yoo J.H., Koo Y.D., Koo S.C., Lim C.O., Lee S.Y., Cho M.J. (2002) Characterization of a stamen‐specific cDNA encoding a novel plant defensin in Chinese cabbage. Plant Molecular Biology, 50, 59–69.
Pomponi M., Censi V., Girolamo D.V., Paolis A.D., Toppi L.D., Aromolo R., Costantino P., Cardarelli M. (2006) Overexpression of Arabidopsis phytochelatin synthase in tobacco plants enhances Cd2+ tolerance and accumulation but not translocation to the shoot. Planta, 223, 180–190.
Raskin I., Smith R.D., Salt D.E. (1997) Phytoremediation of metals: using plants to remove pollutants from the environment. Current Opinion in Biotechnology, 8, 221–226.
Rauser W.E. (1990) Phytochelatins. Annual Review of Biochemistry, 59, 61–86.
Rauser W.E. (1999) Structure and function of metal chelators produced by plants: the case for organic acids, amino acids, phytin and metallothioneins. Cell Biochemistry and Biophysics, 32, 19–48.
Rea P.A., Li Z.S., Lu Y.P., Drozdowicz Y.M., Martinoia E. (1998) From vacuolar GS‐X pumps to multispecific ABC transporters. Annual Review of Plant Physiology and Plant Molecular Biology, 49, 727–760.
Salt D.E. (1995) MgATP‐dependent transport of phytochelatins across the tonoplast of oat roots. Plant Physiology, 107, 1293–1301.
Salt D.E., Smith R.D., Raskin I. (1998) Phytoremediation. Annual Review of Plant Physiology and Plant Molecular Biology, 49, 643–668.
Schmöger M.E., Oven M., Grill E. (2000) Detoxification of arsenic by phytochelatins in plants. Plant Physiology, 122, 793–801.
Shen G.‐M., Zhu C., Du Q.‐Z. (2010) Genome‐wide identification of PHYTOCHELATIN and PHYTOCH_SYNTH domain‐containing phytochelatin family from rice. Electronic Journal of Biology, 6, 73–79.
Song W.E., Chen S.B., Liu J.F., Chen L., Song N.N., Li N., Liu B. (2015) Variation of Cd concentration in various rice cultivars and derivation of cadmium toxicity thresholds for paddy soil by species‐sensitivity distribution. Journal of Integrative Agriculture, 14, 1845–1854.
Steffens J.C. (1990) The heavy metal‐binding peptides of plants. Annual Review of Plant Physiology and Plant Molecular Biology, 41, 553–575.
Thompson J.D., Higgins D.G., Gibson T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position‐specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673–4680.
Toppi L.S.D., Gabbrielli R. (1999) Response to cadmium in higher plants. Environmental and Experimental Botany, 41, 105–130.
Van Assche F., Clijsters H. (1990) Effects of metals on enzyme activity in plants. Plant, Cell and Environment, 13, 195–206.
Vatamaniuk O.K., Mari S., Lu Y.P., Rea P.A. (1999) AtPCS1, a phytochelatin synthase from Arabidopsis: isolation and in vitro reconstitution. Proceedings of the National Academy of Sciences of the United States of America, 96, 7110–7115.
Vatamaniuk O.K., Mari S., Lu Y.P., Rea P.A. (2000) Mechanism of heavy metal ion activation of phytochelatin (PC) synthase: blocked thiols are sufficient for PC synthase‐catalyzed transpeptidation of glutathione and related thiol peptides. Journal of Biological Chemistry, 275, 31451–31459.
Verbruggen N., Hermans C., Schat H. (2009) Mechanisms to cope with arsenic or cadmium excess in plants. Current Opinion in Plant Biology, 12, 364–372.
Wang F., Wang Z., Zhu C. (2012) Heteroexpression of the wheat phytochelatin synthase gene (TaPCS1) in rice enhances cadmium sensitivity. Acta Biochimica et Biophysica Sinica, 44, 886–893.
Wojas S., Clemens S., Hennig J., Sklodowska A., Kopera E., Schat H., Bal W., Antosiewicz D.M. (2008) Overexpression of phytochelatin synthase in tobacco: distinctive effects of AtPCS1 and CePCS genes on plant response to cadmium. Journal of Experimental Botany, 59, 2205–2219.
Xu S., Wang X., Chen J. (2007) Zinc finger protein 1 (ThZF1) from salt cress (Thellungiella halophila) is a Cys‐2/His‐2‐type transcription factor involved in drought and salt stress. Plant Cell Reports, 26, 497–506.
Zenk M.H. (1996) Heavy metal detoxification in higher plants – a review. Gene, 179, 21–30.
Zhu Y.L., Pilon‐Smits E.A.H., Jouanin L., Terry N. (1999a) Overexpression of glutathione synthetase in Indian mustard enhances cadmium accumulation and tolerance. Plant Physiology, 119, 73–79.
Zhu Y.L., Pilon‐Smits E.A.H., Tarun A.S., Weber S.U., Jouanin L., Terry N. (1999b) Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing γ‐glutamylcysteine synthetase. Plant Physiology, 121, 1169–1177.
