MOLECULAR-GENETIC BASIS OF HIGHER PLANTS TOLERANCE TO, AND ACCUMULATION OF, CADMIUM

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract


 Cadmium (Cd) is one of the most wide-ranged and dangerous pollutants for all living organisms, including plants. At present time the intensive studies of mechanisms of Cd accumulation in plant tissues and plant tolerance to its toxic influence are performed. Data about variation of Cd tolerance and accumulation traits in natural populations of hyperaccumulators species as well as important crops were obtained. A series of mutants with changed sensitivity to Cd was obtained. In recent decade several classes of proteins involving in cell responses to Cd ions were revealed. An important role of microRNA in plant adaptation to Cd was recently demonstrated. Studies of molecular-genetic mechanisms of Cd accumulation and plant tolerance to it are theoretical basis for development of phytoremediation technologies of soil contaminated with heavy metals and breeding of crop varieties with decreased Cd accumulation.

About the authors

Olga A Kulaeva

All-Russia Research Institute for Agricultural Microbiology, Saint-Petersburg, RF

Email: koa1983@yandex.ru Podbelskiy chausse, 3, Saint-Petersburg, Pushkin, 196608, Russia

Viktor E Tsyganov

All-Russia Research Institute for Agricultural Microbiology, Saint-Petersburg, RF

Email: viktor_tsyganov@arriam.spb.ru

References

  1. Серегин И., 2001. Фитохелатины и их роль в деток- сикации кадмия у высших растений // Усп. биол. химии. Т. 41. С. 283-300.
  2. Титов А. Ф., Таланова В. В., Казнина Н. М. и др., 2007. Устойчивость растений к тяжелым металлам. - Петрозаводск: Карельский научный центр РАН, 172 с.
  3. Цыганов В. Е., Заболотный A. И., Будкевич Т. А. и др., 2010. Влияние кадмия на развитие и функционирование клубеньков у лядвенца рогатого (Lotus corniculatus L.) и лядвенца японского (Lotus japonicus (Regel.) K. Larsen) // Ботаника (Исследования). Выпуск 38. С. 343-354.
  4. Arao T., Ae N., 2003. Genotypic variations in cadmium levels of rice grain // Soil Sci. Plant Nutr. Vol. 49. P. 473-479.
  5. Baker A. J. M., 1981. Accumulators and excluders strategies in the response of plants to heavy metals // J. Plant Nutr. Vol. 3. P. 643-654.
  6. Becher M., Talke I., Krall L., Krдmer U., 2004. Crossspecies microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri // Plant J. Vol. 37. P. 251-268.
  7. Belimov A. A., Safronova V. I., Tsyganov V. E. et al., 2003. Genetic variability in tolerance to cadmium and accumulation of heavy metals in pea (Pisum sativum L.) // Euphytica. Vol. 131. P. 25-35.
  8. Belimov A., Safronova V., Demchinskaya S., Dzyuba O., 2007. Intraspecific variability of cadmium tolerance in hydroponically grown Indian mustard (Brassica juncea (L.) Czern.) seedlings // Acta Physiol. Plant. Vol. 29. P. 473-478.
  9. Bell M. J., McLaughlin M. J., Wright G. C., Cruickshank J., 1997. Inter- and intra-specific variation in accumulation of cadmium by peanut, soybean, and navy bean // Aust. J. Agr. Res. Vol. 48. P. 1151-1160.
  10. Berezin I., Mizrachy-Dagry T., Brook E., Mizrahi K., 2008. Overexpression of AtMHX in tobacco causes increased sensitivity to Mg2+, Zn2+, and Cd2+ ions, induction of V-ATPase expression, and a reduction in plant size // Plant Cell Rep. Vol. 27. P. 939-949.
  11. Bert V., Meerts P., Saumitou-Laprade P. et al., 2003. Genetic basis of Cd tolerance and hyperaccumulation in Arabidopsis halleri // Plant Soil. Vol. 249. P. 9-18.
  12. Blanvillain R., Kim J., Wu S., Lima A., 2009. OXIDATIVE STRESS 3 is a chromatin-associated factor involved in tolerance to heavy metals and oxidative stress // Plant J. Vol. 57. P. 654-665.
  13. Brooks R. R., 1998. Plants that hyperaccumulate heavy metals. Wallingfors: CAB Intl., 381 p.
  14. Callahan D. L., Baker A. J. M., Kolev S. D., Wedd A. G., 2006. Metal ion ligands in hyperaccumulating plants // J. Biol. Inorg. Chem. Vol. 11. P. 2-12.
  15. Chan D. Y., Hale B. A., 2004. Differential accumulation of Cd in durum wheat cultivars: uptake and retranslocation as sources of variation // J. Exp. Bot. Vol. 55 P. 2571-2579.
  16. Chen Y., He Y., Yang Y., Yu Y., 2003. Effect of cadmium on nodulation and N2-fixation of soybean in contaminated soils // Chemosphere. Vol. 50. P781-787.
  17. Clarke J. M., Leisle D., Kopytko G. L., 1997. Inheritance of cadmium concentration in five durum wheat crosses // Crop Sci. Vol. 37. P. 1722-1726.
  18. Clemens S., 2001. Molecular mechanisms of plant metal tolerance and homeostasis // Planta. Vol. 212. P. 457-486.
  19. Clemens S., 2006. Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants // Biochimie. Vol. 88. P. 1707-1719.
  20. Cobbett 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 // Plant J. Vol. 16. P. 73-78.
  21. Connolly E. L., Fett J. P., Guerinot M. L., 2002. Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation // Plant Cell. Vol. 14. P. 1347-1357
  22. DalCorso V., Farinati S., Maistri S., Furini A., 2008. How plants cope with cadmium: staking all on metabolism and gene expression // J. Integr. Plant Biol. Vol. 50. P. 1268-1280.
  23. Ding Y., Zhu Ch., 2009. The role of microRNAs in copper and cadmium homeostasis // Biochem. Biophys. Res. Commun. Vol. 386. P. 6-10.
  24. Dolezal O., Cobbett C., 1991. Arabinose kinase-deficient mutant of Arabidopsis thaliana // Plant Physiol. Vol.96. P. 1255-1260.
  25. Dominguez-Solнs J., Gutierrez-Alcalб G., Vega J., Romero L., 2001. The cytosolic O-acetylserine(thiol)lyase gene is regulated by heavy metals and can function in cadmium tolerance // J. Biol. Chem. Vol. 276. P. 9297-9302.
  26. Ebbs S., Lau I, Ahner B., Kochian L., 2002. Phytochelatin synthesis is not responsible for Cd tolerance in the Zn/Cd hyperaccumulator Thlaspi caerulescens // Planta. Vol. 214. P. 635-640.
  27. Fusconi A., Gallo C., Camusso W., 2007. Effects of cadmium on root apical meristems of Pisum sativum L. Cell viability, cell proliferation and microtubule pattern as suitable markers for assessment of stress pollution // Mut. Res. Vol. 632. P. 9-19.
  28. Grant C., Clarke J., Duguidcand S., Chaney R. L., 2008. Selection and breeding of plant cultivars to minimize cadmium accumulation // Sci. Total Environ. Vol. 390. P. 301-310.
  29. Guyon V., Astwood J., Garner E., Dunker A., 2000. Isolation and characterization of cDNAs expressed in the early stages of flavonol-induced pollen germination in petunia // Plant Physiol. Vol. 123. P. 699-710.
  30. Ha S., Howden R., Dietrich W., Bugg S., 1999. Phytochelatin synthase genes from Arabidopsis and the yeast Schizosaccharomyces pombe // Plant Cell. Vol. 11. P. 1153-1163.
  31. Hall J. L., Williams L. E., 2003. Transition metal transporters in plants. J. Exp. Bot. Vol. 54. P. 2601-2613.
  32. Hanikenne M., Talke I. N., Haydon M. J. et al., 2008. Evolution of metal hyperaccumulation required cisregulatory changes and triplication of HMA4 // Nature. Vol. 453. P. 391-395.
  33. Hart J. J., Welch R. M., Norvell W. A. et al., 2005. Zinc effects on cadmium accumulation and partitioning in nearisogenic lines of durum wheat that differ in grain cadmium concentration // New Phytol. Vol. 167. P. 391-401.
  34. Howden R., Cobbett C. S., 1992. Cadmium-sensitive mutants of Arabidopsis thaliana // Plant Physiol. Vol. 100. P. 100-107.
  35. Howden R., Andersen C. R., Goldsbrough P. B., Cobbett C. S., 1995а. A cadmium-sensitive, glutathionedeficient mutant of Arabidopsis thaliana // Plant Physiol. Vol. 107. P. 1067-1073.
  36. Howden R., Goldsbrough P. B., Andersen C. R., Cobbett C. S., 1995b. Cadmium-sensitive, cad1 mutants of Arabidopsis thaliana are phytochelatin deficient // Plant Physiol. Vol. 107. P. 1059-1066.
  37. Kim D., Bovet L., Kushnir S., Noh E., 2006. AtATM3 is involved in heavy metal resistance in Arabidopsis // Plant Physiol. Vol. 140. P. 922-932.
  38. Kim D., Bovet L., Maeshima M., Martinoia E., 2007. The ABC transporter AtPDR8 is a cadmium extrusion pump conferring heavy metal resistance // Plant J. Vol. 50. P. 207-218.
  39. Kim Y., Kim D., Shim D., Song W., 2008. Expression of the novel wheat gene TM20 confers enhanced cadmium tolerance to bakers' yeast // J. Biol. Chem. Vol. 283. P. 15893-15902.
  40. Krotz R. M., Evangelou B. P., Wagner G. J., 1989. Relationships between cadmium, zinc, Cd-binding peptide, and organic acid in tobacco suspension cells // Plant Physiol. Vol. 91. P. 780-787.
  41. Kum Ch., Wong E., Cobbett Ch., 2009. HMA P-type ATPases are the major mechanism for root-to-shoot Cd translocation in Arabidopsis thaliana // New Phytol. Vol. 181. P. 71-78.
  42. Kushnir S., Babiychuk E., Storozhenko S., Davey M., 2001. A mutation of the mitochondrial ABC transporter Sta1 leads to dwarfism and chlorosis in the Arabidopsis mutant starik // Plant Cell. Vol. 13. P. 89-100.
  43. Lane T. W., Saito M. A., George G. N. et al., 2005. A cadmium enzyme from a marine diatom // Nature. Vol. 435. P. 42.
  44. Li L., He Z., Pandey G. K. et al., 2002. Functional cloning and characterization of a plant efflux carrier for multidrug and heavy metal detoxification // J. Biol. Chem. Vol. 277. P. 5360-5368.
  45. Liu J., Zhu Q., Zhang Z. et al., 2005. Variations in cadmium accumulation among rice cultivars and types and the selection of cultivars for reducing cadmium in the diet // J. Sci. Food Agr. Vol. 85. P. 147-153.
  46. Liu M. Q., Yanai J., Jiang R. F. et al., 2008. Does cadmium play a physiological role in the hyperaccumulator Thlaspi caerulescens? // Chemosphere. Vol. 71. P. 1276-1283.
  47. Lombi E., Zhao F. J., Dunham SJ., McGrath S. P. 2000. Cadmium accumulation in populations of Thlaspi caerulescens and Thlaspi goesingense // New Phytol. Vol. 145. P. 11-20.
  48. Macnair M. R., Bert V., Huitson S. B. et al., 1999. Zinc tolerance and hyperaccumulatin are genetically independent characters // Proc. R. Soc. Lond. Biol. Sci. Vol. 266. P. 2175-2179.
  49. Matsuda T., Kuramata M., Takahashi Y. et al., 2009. A novel plant cysteine-rich peptide family conferring cadmium tolerance to yeast and plants // Plant Sign. Behav. Vol. 4:5. P. 419-421.
  50. Mills R., Krijger G., Baccarini P. et al., 2003. Functional expression of AtHMA4, a P1B-type ATPase of the Zn/Co/Cd/Pb subclass // Plant J. Vol. 35. P. 164-176.
  51. Morel M., Crouzet J., Gravot A., 2009. AtHMA3, a P1B-ATPase allowing Cd/Zn/Co/Pb vacuolar storage in Arabidopsis // Plant Physiol. Vol. 149. P. 894-904.
  52. Oomen R. J. F. J., Wu J., Lelievre F. et al., 2009. Functional characterization of NRAMP3 and NRAMP4 from the metal hyperaccumulator Thlaspi caerulescens // New Phytol. Vol. 181. P. 637-650.
  53. Ortiz D. F., Kreppel L., Speiser D. M. et al., 1992. Heavy metal tolerance in the fission yeast requires an ATP-binding cassette-type vacuolar membrane transporter // EMBO J. Vol. 11. P. 3491-3499.
  54. Palmiter R. D., 1998. The elusive function of metallothioneins // Proc. Natl. Acad. Sci. USA. Vol. 95. P. 8428-8430.
  55. Pan A., Yang M., Tie F. et al. 1994. Expression of mouse metallothionein-I gene confers cadmium resistance in transgenic tobacco plants // Plant Mol. Biol. Vol. 24. Р. 341-351.
  56. Peer W. A., Baxter I. R., Richards E. L., Freeman J. L., Murphy A. S., 2005. Phytoremediation and hyperaccumulator plants // Molecular Biology of Metal Homeostasis and Detoxification / Eds. M. J. Tamбs, E. Martinoia, Berlin Heidelberg: Springer-Verlag. P. 299-340.
  57. Pence N. S., Larsen P. B., Ebbs S. D., 2000. The molecular physiology of heavy metal transport in the Zn/ Cd hyperaccumulator // Proc. Natl. Acad. Sci. USA. Vol. 97. P. 4956-4960.
  58. Persans M., Nieman K., Salt D., 2001. Functional activity and role of cation-efflux family members in Ni hyperaccumulation in Thlaspi goesingense // Proc. Natl. Acad. Sci. USA. Vol. 98. P. 9995-10000.
  59. Prйvйral S., Gayet L., Moldes C. et al., 2009. A common highly conserved cadmium detoxification mechanism from bacteria to humans. Heavy metal tolerance conferred by the ATP-binding cassette (ABC) transporter SpHMT1 requires glutathione but not metal-chelating phytochelatin peptides // J. Biol. Chem. Vol. 284. P. 4936-4943.
  60. Reese R., Wagner G., 1987. Effects of buthionine sulfoximine on Cd-binding peptide levels in suspensioncultured tobacco cells treated with Cd, Zn, or Cu // Plant Physiol. Vol. 84. P. 574-577.
  61. Rivera-Becerril F., Calantzis C., Turnau K. et al., 2002. Cadmium accumulation and buffering of cadmium-induced stress by arbuscular mycorrhiza in three Pisum sativum L. genotypes // J. Exp. Bot. Vol. 53. P. 1177-1185.
  62. Rivera-Becerril F., van Tuinen D., Martin-Laurent F. et al., 2005. Molecular changes in Pisum sativum L. roots during arbuscular mycorrhiza buffering of cadmium stress // Mycorrhiza. Vol. 16. P. 51-60.
  63. Rivetta A., Negrini N., Cocucci M., 1997. Involvement of Ca2+-calmodulin in Cd2+ toxicity during the early phases of radish (Raphanus sativus L.) seed germination // Plant Cell Environ. Vol. 20. P. 600-608.
  64. Roosens N., Verbruggen N., Meerts P. et al., 2003. Natural variation in cadmium tolerance and its relationship to metal hyperaccumulation for seven populations of Thlaspi caerulescens from Western Europe // Plant Cell Environ. Vol. 26. P. 1657-1672.
  65. Sanita di Toppi L., Gabbrielli R., 1999. Response to cadmium in higher plants // Environ. Exp. Bot. Vol. 41. P. 105-130.
  66. Sanjaya P., Hsiao P., Su R., Ko S., 2008. Overexpression of Arabidopsis thaliana tryptophan synthase beta 1 (AtTSB1) in Arabidopsis and tomato confers tolerance to cadmium stress // Plant Cell Environ. Vol. 31. P. 1074-1085.
  67. Schat H., Kuiper E., Ten Bookum W. M., Vooijs R., 1993. A general model for the genetic control of copper tolerance in Silene vulgaris: evidence from crosses between plants from different tolerant populations // Heredity. Vol. 70. P. 142-147.
  68. Schat H., Vooijs R., Kuiper E., 1996. Identical major gene loci for heavy metal tolerances that have independently evolved in different local populations and subspecies of Silene vulgaris // Evolution. Vol. 50. P. 1888-1895.
  69. Shaul O., Hilgemann D. W., de-Almeida-Engler J. et al., 1999. Cloning and characterization of a novel Mg2+/ H+ exchanger // EMBO J. Vol. 18. P. 3973-3980.
  70. Singh O., Labana S., Pandey G. et al., 2003. Phytoremediation: an overview of metabolic ion decontamination from soil // Appl. Microb. Biotech. Vol. 61. P. 405-412.
  71. Smith S. E., Macnair M. R., 1998. Hypostatic modifiers cause variation in degree of copper tolerance in Mimulus guttatus // Heredity. Vol. 80. P. 760-768.
  72. Song W-Y., Martinoia E., Lee J. et al., 2004. A novel family Cys-rich membrane proteins mediates cadmium resistance in Arabidopsis // Plant Physiol. Vol. 135. P. 1027-1039.
  73. Suzuki N., Yamaguchi Y., Koizumi N., Sano H., 2002. Functional characterization of a heavy metal binding protein CdI19 from Arabidopsis // Plant J. Vol. 32. P. 165-173.
  74. Talke I. N., Hanikenne M., Krдmer U., 2006. Zinc-dependent global transcriptional control, transcriptional deregulation, and higher gene copy number for genes in metal homeostasis of the hyperaccumulator Arabidopsis halleri // Plant Physiol. Vol. 142. P. 148-167.
  75. Thomine S., LelieБvre F., Debarbieux E. et al., 2003. AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency // Plant J. Vol. 34. P. 685-695.
  76. Thomine S., Wang R., Ward J. M. et al., 2000. Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes // Proc. Natl. Acad. Sci. USA. Vol. 97. P. 4991-4996.
  77. Tilstone G., Macnair M., Smith S., 1997. Does copper tolerance give cadmium tolerance in Mimulus guttatus? // Heredity. Vol. 79. P. 445-452.
  78. Tommey A. M., Shi J., Lindsay W. P. et al., 1991. Expression of the pea gene PsMTa in E. coli - metal binding properties of the expressed protein // FEBS Letters. Vol. 292. P. 48-52.
  79. Tsyganov V., Belimov A., Borisov A. et al., 2007. A chemically induced new pea (Pisum sativum) mutant SGECdt with increased tolerance to, and accumulation of, cadmium // Ann. Bot. Vol. 99. P. 1-11.
  80. Tsyganov V., Zhernakov A., Kulaeva O. et al., 2008. Cadmium influence on legume-Rhizobium symbioses. In: Proceedings of 8th European Nitrogen Fixation Conference. Gent, Belgium. August 30 - September 3, P. 201.
  81. Ueno D., Ma J. F., Iwashita T. et al., 2005. Identification of the form of Cd in the leaves of a superior Cd accumulating ecotype of Thlaspi caerulescens using Cd-NMR // Planta. Vol. 221. P. 928-936.
  82. Van der Zaal B. J., Neuteboom L. W., Pinas J. E. et al., 1999. Over-expression of a novel Arabidopsis gene related to putative zinc-transporter genes from animals can lead to enhanced zinc resistance and accumulation // Plant Physiol. Vol. 119. P. 1047-1055.
  83. Verbruggen N., Hermans Ch., Schat H., 2009. Molecular mechanisms of metal hyperaccumulation in plants // New Phytol. Vol. 181. P. 759-776
  84. Verret F., Gravot A., Auroy P. et al. 2004. Overexpression of AtHMA4 enhances root-to-shoot translocation of zinc and cadmium and plant metal tolerance // FEBS Letters. Vol. 576. P. 306-312.
  85. Vert G., Grotz N., Dйdaldйchamp F., 2002. IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth // Plant Cell. Vol. 14. P. 1223-1233.
  86. Vatamaniuk O. K., Bucher E. A., Sundaram M. V., Rea P. A., 2005. CeHMT-1, a putative phytochelatin transporter, is required for cadmium tolerance in Caenorhabditis elegans // J. Biol. Chem. Vol. 280. P. 23684-23690.
  87. Vatamaniuk O. K., Bucher E. A., Ward J. T., Rea P. A., 2001. A new pathway for heavy metal detoxification in animals: phytochelatin synthase is required for cadmium tolerance in Caenorhabditis elegans // J. Biol. Chem. Vol. 276. P. 20817-20820.
  88. Weber M., Harada E., Vess C. et al., 2004. Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotinamine synthase, a zip transporter and other genes as potential metal hyperaccumulation factors // Plant J. Vol. 37. P. 269-281.
  89. Zha H. G., Jiang R. F., Zhao E. J. et al., 2004. Co-segregation analysis of cadmium and zinc accumulation in Thaspi caerulescens interecotypic crosses // New Phytol. Vol. 163. P. 299-312.
  90. Zhigang A., Cuijie L., Yuangang Z. et. al., 2006. Expression of BjMT2, a metallothionein 2 from Brassica juncea, increases copper and cadmium tolerance in Escherichia coli and Arabidopsis thaliana, but inhibits root elongation in Arabidopsis thaliana seedlings // J. Exp. Bot. Vol. 57. P. 3575-3582.
  91. Zimeri A. M., Dhankher O. P., McCaig B., Meagher R. B., 2005. The plant MT1 metallothioneins are stabilized by binding cadmium and are required for cadmium tolerance and accumulation // Plant Mol. Biol. Vol. 58. P. 839-855.
  92. Zornoza P., Vazquez S., Esteban E. et al., 2002. Cadmium-stress in nodulated white lupin: strategies to avoid toxicity // Plant Physiol. Biochem. Vol. 40. P. 1003-1009.

Statistics

Views

Abstract - 316

PDF (Russian) - 262

Cited-By


PlumX


Copyright (c) 2010 Kulaeva O.A., Tsyganov V.E.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies