Advertisement

Mechanisms Underlying Heavy Metal Tolerance in Arbuscular Mycorrhizas

  • Manuel González-Guerrero
  • Karim Benabdellah
  • Nuria Ferrol
  • Concepción Azcón-AguilarEmail author
Chapter

Abstract

Arbuscular mycorrhizal fungi are able to tolerate a wide range of metal concentrations in soils. A number of passive and active molecular processes are employed by these fungi to maintain metal homeostasis. The main passive mechanism is the binding of metals to the fungal walls, responsible for a significant percentage of the metal retained. Meanwhile in the cytosol, a number of chelators (metallothioneins, glutathione) bind the metals very efficiently. Heavy metal transporters collaborate with the intracellular chelators to actively reduce the levels of metal by pumping metal out of the cytosol. Additionally, the fungus strives to reduce the free radicals produced by heavy metals. In this chapter, we discuss the most recent progress in the identification and characterization of the elements involved in maintaining metal homeostasis in arbuscular mycorrhizal fungi, as well as how the heavy metal control systems of the plant are affected by the development of the symbiosis.

Keywords

Arbuscular Mycorrhizal Fungus Mycorrhizal Fungus Arbuscular Mycorrhiza Ectomycorrhizal Fungus Mycorrhizal Plant 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

The authors are grateful to the Consejería de Innovación, Ciencia y Empresa of the Andalusian Autonomic Governement (ref. P06-CVI-02263) for financial support to part of the work reported here. Karim Benabdellah was supported by an I3P contract from the Spanish Council for Scientific Research (CSIC).

References

  1. Argüello J, Eren E, González-Guerrero M (2007) The structure and function of heavy metal transport P1B-ATPases. Biometals 20:233–248PubMedCrossRefGoogle Scholar
  2. Ashford AE (2002) Tubular vacuoles in arbuscular mycorrhizas. New Phytol 154:545–547CrossRefGoogle Scholar
  3. Bacik JP, Hazes B (2006) Crystal structures of a poxviral glutaredoxin in the oxidized and reduced states show redox-correlated structural changes. J Mol Biol 365:1545–1558PubMedCrossRefGoogle Scholar
  4. Bago B, Vierheilig H, Piché Y, Azcón-Aguilar C (1996) Nitrate depletion and pH changes induced by the extraradical mycelium of the arbuscular mycorrhizal fungus Glomus intraradices. grown in monoxenic culture New Phytol 133:273–280CrossRefGoogle Scholar
  5. Bago B, Cano C, Azcón-Aguilar C, Samson J, Coughlan AP, Piché Y (2004) Differential morphogenesis of the extraradical mycelium of an arbuscular mycorrhizal fungus grown monoxenically on spatially heterogeneous culture media. Mycologia 96:452–462PubMedCrossRefGoogle Scholar
  6. Bellion M, Courbot M, Jacob C, Blaudez D, Chalot M (2006) Extracellular and cellular mechanisms sustaining metal tolerance in ectomycorrhizal fungi. FEMS Microbiol Lett 254:173–181PubMedCrossRefGoogle Scholar
  7. Bellion M, Courbot M, Jacob C, Guinet F, Blaudez D, Chalot M (2007) Metal induction of a Paxillus involutus. metallothionein and its heterologous expression in Hebeloma cylindrosporum New Phytol 174:151–158PubMedCrossRefGoogle Scholar
  8. Benabdellah K, Merlos M, Azcón-Aguilar C, Ferrol N (2008). GintGRX1, the first characterized glomeromycotan glutaredoxin, is a multifunctional enzyme that responds to oxidative stress. Fungal Genet Biol. doi:10.1016/j.fgb.2008.09.019Google Scholar
  9. Blaudez D, Botton B, Chalot M (2000) Cadmium uptake and subcellular compartmentation in the ectomycorrhizal fungus Paxillus involutus. Microbiology 146:1109–1117PubMedGoogle Scholar
  10. Burleigh S, Kristensen B, Bechmann IE (2003) A plasma membrane zinc transporter from Medicago truncatula. is up-regulated in roots by Zn fertilization, yet down-regulated by arbuscular mycorrhizal colonization Plant Mol Biol 52:1077–1088PubMedCrossRefGoogle Scholar
  11. Canovas D, Vooijs R, Schat H, De Lorenzo V (2004) The role of thiol species in the hypertolerance of Aspergillus. sp P37 to arsenic J Biol Chem 279:51234–51240PubMedCrossRefGoogle Scholar
  12. Chen B, Li X, Tao H, Christie P, Wong M (2003) The role of arbuscular mycorrhiza in zinc uptake by red clover growing in a calcareous soil spiked with various quantities of zinc. Chemosphere 50:839–846PubMedCrossRefGoogle Scholar
  13. Chern EC, Tsai DW, Ogunseitan OA (2007) Deposition of glomalin-related soil protein and sequestered toxic metals into watersheds. Environ Sci Technol 41:3566–3572PubMedCrossRefGoogle Scholar
  14. Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: Roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182PubMedCrossRefGoogle Scholar
  15. Cooper KM, Tinker PB (1978) Translocation and transfer of nutrients in vesicular arbuscular mycorrhizas II. Uptake and translocation of phosphorus, zinc and sulphur. New Phytol 81:43–52Google Scholar
  16. Courbot M, Diez L, Ruotolo R, Chalot M, Leroy P (2004) Cadmium-responsive thiols in the ectomycorrhizal fungus Paxillus involutus. Appl Environ Microbiol 70:7413–7417PubMedCrossRefGoogle Scholar
  17. Darrah PR, Tlalka M, Ashford AE, Watkinson SC, Fricker MD (2006) The vacuole system is a significant intracellular pathway for longitudinal solute transport in basidiomycete fungi. Eukaryot Cell 5:1111–1125PubMedCrossRefGoogle Scholar
  18. del Val C, Barea JM, Azcón-Aguilar C (1999a) Diversity of arbuscular mycorrhizal fungus populations in heavy-metal-contaminated soils. Appl Environ Microbiol 65:718–723Google Scholar
  19. del Val C, Barea JM, Azcón-Aguilar C (1999b) Assessing the tolerance to heavy metals of arbuscular mycorrhizal fungi isolated from sewage sludge-contaminated soils. Appl Soil Ecol 11:261–269CrossRefGoogle Scholar
  20. Díaz G, Azcón-Aguilar C, Honrubia M (1996) Influence of arbuscular mycorrhizae on heavy metals (Zn and Pb) uptake and growth of Lygeum spartum. and Anthillis cytisoides Plant Soil 180:241–249CrossRefGoogle Scholar
  21. Eide DJ (2004) The ABC of solute carriers. The SLC39 family of metal ion transporters. Eur J Physiol 447:796–800CrossRefGoogle Scholar
  22. Entry JA, Watrud LS, Reeves M (1999) Accumulation of 137Cs and 90Sr from contaminated soil by three grass species inoculated with mycorrhizal fungi. Environ Pollut 104:449–457CrossRefGoogle Scholar
  23. Faraco V, Sannia G, Giardina P (2003) Metal-responsive elements in Pleurotus ostratus. laccase gene promoters Microbiology 149:2155–2162PubMedCrossRefGoogle Scholar
  24. Fogarty RV, Tobin JM (1996) Fungal melanins and their interactions with metals. Enzyme Microb Technol 19:311–317PubMedCrossRefGoogle Scholar
  25. Fomina M, Ritz K, Gadd GM (2000) Negative fungal chemotropism to toxic metals. FEMS Microbiol Lett 193:207–211PubMedCrossRefGoogle Scholar
  26. Fraústro da Silva JJR, Williams RJP (2001) The biological chemistry of the elements, 2nd edn. Oxford University Press, New YorkGoogle Scholar
  27. González-Chávez MC, Carrillo-González R, Wright SF, Nichols KA (2004) The role of glomalin, a protein produced by arbuscular mycorrhizal fungi, in sequestering potentially toxic elements. Environ Pollut 130:317–323PubMedCrossRefGoogle Scholar
  28. González-Guerrero M, Azcón-Aguilar C, Mooney M, Valderas A, MacDiarmid CW, Eide DJ, Ferrol N (2005) Characterization of a Glomus intraradices. gene encoding a putative Zn transporter of the cation diffusion facilitator family Fungal Genet Biol 42:130–140PubMedCrossRefGoogle Scholar
  29. González-Guerrero M, Cano C, Azcón-Aguilar C, Ferrol N (2007) GintMT1 encodes a functional metallothionein in Glomus intraradices. that responds to oxidative stress Mycorrhiza 17:327–335PubMedCrossRefGoogle Scholar
  30. González-Guerrero M, Melville LH, Ferrol N, Lott JNA, Azcón-Aguilar C, Peterson RL (2008) Ultrastructural localization of heavy metals in the extraradical mycelium and spores of the arbuscular mycorrhizal fungus Glomus intraradices. Can J Microbiol 54:103–110PubMedCrossRefGoogle Scholar
  31. Green F, Clausen CA (2003) Copper tolerance of brown-rot fungi: time course of oxalic acid production. Int Biodeterior Biodegrad 51:145–149CrossRefGoogle Scholar
  32. Guerinot ML (2000) The ZIP family of metal transporters. Biochim Biophys Acta 1465:190–198PubMedCrossRefGoogle Scholar
  33. Halliwell B, Gutteridge JMC (1989) Free radicals in biology and medicine. Clanderon Press, Oxford, UKGoogle Scholar
  34. Hamer DH (1986) Metallothionein. Ann Rev Biochem 55:913–951PubMedCrossRefGoogle Scholar
  35. Harrison M, Dewbre G, Liu J (2002) A phosphate transporter from Medicago truncatula. involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi Plant Cell 14:2413–2429PubMedCrossRefGoogle Scholar
  36. Haselwandter K, Dobernigg B, Beck W, Jung G, Cansier A, Winkelmann G (1992) Isolation and identification of hydroxamate siderophores of ericoid mycorrhizal fungi. Biometals 5:51–56CrossRefGoogle Scholar
  37. Hawkins HJ, Johansen A, George E (2000) Uptake and transport of organic and inorganic nitrogen by arbuscular mycorrhizal fungi. Plant Soil 226:275–285CrossRefGoogle Scholar
  38. Hildebrandt U, Regvar M, Bothe H (2007) Arbuscular mycorrhiza and heavy metal tolerance. Phytochemistry 68:139–146PubMedCrossRefGoogle Scholar
  39. Hodgson JF (1963) Chemistry of the micronutrient elements in soils. Adv Agron 15:119–159CrossRefGoogle Scholar
  40. Holmgren A, Johansson C, Berndt C, Lönn ME, Hudemann C, Lillig CH (2005) Thiol redox control via thioredoxin and glutaredoxin systems. Biochem Soc Trans 33:1375–1377PubMedCrossRefGoogle Scholar
  41. Howe R, Evans RL, Ketteridge SW (1997) Copper-binding proteins in ectomycorrhizal fungi. New Phytol 135:123–131CrossRefGoogle Scholar
  42. Jacquot E, van Tuinen D, Gianinazzi S, Gianinazzi-Pearson V (2000) Monitoring species of arbuscular mycorrhizal fungi in planta and in soil by nested PCR: Application to the study of the impact of sewage sludge. Plant Soil 226:179–188CrossRefGoogle Scholar
  43. Javot H, Pumplin N, Harrison MJ (2007) Phosphate in the arbuscular mycorrhizal symbiosis: Transport properties and regulatory roles. Plant Cell Environ 30:310–322PubMedCrossRefGoogle Scholar
  44. Joner EJ, Briones R, Leyval C (2000) Metal-binding capacity of arbuscular mycorrhizal mycelium. Plant Soil 226:227–234CrossRefGoogle Scholar
  45. Karandashov V, Bucher M (2005) Symbiotic phosphate transport in arbuscular mycorrhizas. Trends Plant Sci 10:22–29PubMedCrossRefGoogle Scholar
  46. Khan AG (2005) Role of soil microbes in the rhizospheres of plants growing on trace metal contaminated soils in phytoremediation. J Trace Elem Med Biol 18:355–364PubMedCrossRefGoogle Scholar
  47. Kim D, Gustin JL, Lahner B, Persans MW, Baek D, Yun DJ, Salt DE (2004) The plant CDF family member TgMTP1 from the Ni/Zn hyperaccumulator Thlaspi goesingense. acts to enhance efflux of Zn at the plasma membrane when expressed in Saccharomyces cerevisiae Plant J 39:237–251PubMedCrossRefGoogle Scholar
  48. Kolukisaoglu HU, Bovet L, Klein M, Eggmann T, Geisler M, Wanke D, Martinoia E, Schulz B (2002) Family business: the multidrug-resistance related protein (MRP) ABC transporter genes in Arabidopsis thaliana. Planta 216:107–119PubMedCrossRefGoogle Scholar
  49. Kruh GD, Belinsky MG (2003) The MRP family of drug efflux pumps. Oncogene 22:7537–7552PubMedCrossRefGoogle Scholar
  50. Lahner B, Gong J, Mahmoudian M, Smith E, Abid K, Rogers E, Guerinot M, Harper J, Ward J, McIntyre L, Schoroeder J, Salt D (2003) Genomic scale profiling of nutrient and trace elements in Arabidopsis thaliana. Nat Biotechnol 21:1215–1221PubMedCrossRefGoogle Scholar
  51. Lanfranco L, Balsamo R, Martino E, Perotto S, Bonfante P (2002a) Zinc ions alter morphology and chitin deposition in an ericoid fungus. Eur J Histochem 46:341–350Google Scholar
  52. Lanfranco L, Bolchi A, Ros E, Ottonello S, Bonfante P (2002b) Differential expression of a metallothionein gene during the presymbiotic versus the symbiotic phase of an arbuscular mycorrhizal fungus. Plant Physiol 130:58–67CrossRefGoogle Scholar
  53. Lanfranco L, Balsamo R, Martino P, Bonfante P, Perotto S (2004) Zinc ions differentially affect chitin synthase gene expression in an ericoid mycorrhizal fungus. Plant Biosyst 138:271–277CrossRefGoogle Scholar
  54. Lanfranco L, Novero M, Bonfante P (2005) The mycorrhizal fungus Gigaspora margarita. possesses a CuZn superoxide dismutase that is up-regulated during symbiosis with legume host Plant Physiol 137:1319–1330PubMedCrossRefGoogle Scholar
  55. Leyval C, Joner EJ, del Val C, Haselwandter K (2002) Potential of arbuscular mycorrhizal fungi for bioremediation. Gianinazzi S, Schüepp H, Barea JM, Haselwandter K Mycorrhizal technology in agriculture. Birkhäuser Verlag, Basel 175–186CrossRefGoogle Scholar
  56. MacDiarmid CW, Milanick MA, Eide D (2002) Biochemical properties of vacuolar zinc transport systems of Saccharomyces cerevisiae. J Biol Chem 277:39187–39194PubMedCrossRefGoogle Scholar
  57. MacDiarmid C, Milanick M, Eide D (2003) Induction of the ZRC1. metal tolerance gene in zinc-limited yeast confers resistance to zinc shock J Biol Chem 278:15065–15072PubMedCrossRefGoogle Scholar
  58. Malcová R, Rydlová J, Vosátka M (2003) Metal-free cultivation of Glomus. sp BEG 140 isolated from Mn-contaminated soil reduces tolerance to Mn. Mycorrhiza 13:151–157Google Scholar
  59. Maldonado-Mendoza IE, Dewbre GR, Harrison MJ (2001) A phosphate transporter gene from the extra-radical mycelium of an arbuscular mycorrhizal fungus Glomus intraradices. is regulated in response to phosphate in the environment Mol Plant Microbe Interact 14:1140–1148PubMedCrossRefGoogle Scholar
  60. Maret W (2000) The function of zinc metallothionein: a link between cellular zinc and redox state. J Nutr 130:1455S-–1458SPubMedGoogle Scholar
  61. Maret W (2003) Cellular zinc and redox states converge in the metallothionein/thionein pair. J Nutr 133:1460S-–1462PubMedGoogle Scholar
  62. Marin E, Leonhardt N, Vavasseur A, Forestier C (1998) Cloning of AtMRP1, an Arabidopsis thaliana. cDNA encoding a homologue of the mammalian multidrug resistance-associated protein Biochim Biophys Acta 1369:7–13PubMedCrossRefGoogle Scholar
  63. Marschner H, Römheld V (1994) Strategies of plants for acquisition of iron. Plant Soil 165:261–274CrossRefGoogle Scholar
  64. Mosse B (1957) Growth and chemical composition of mycorrhizal and non-mycorrhizal apples. Nature 179:349–362CrossRefGoogle Scholar
  65. O’Halloran TV, Culotta VC (2000) Metallochaperones, an intracellular shuttle service for metal ions. J Biol Chem 275:25057–25060PubMedCrossRefGoogle Scholar
  66. Ortiz DF, Ruscitti T, McCue KF, Ow DW (1995) Transport of metal-binding peptides by HMT1, a fission yeast ABC-type vacuolar membrane protein. J Biol Chem 270:4721–4728PubMedCrossRefGoogle Scholar
  67. Outten C, O’Halloran T (2001) Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science 292:2488–2492PubMedCrossRefGoogle Scholar
  68. Ouziad F, Hildebrandt U, Schmelzer E, Bothe H (2005) Differential gene expressions in arbuscular mycorrhizal-colonized tomato grown under heavy metal stress. J Plant Physiol 162:634–649PubMedCrossRefGoogle Scholar
  69. Palmieri F, Giardina P, Bianco C, Fontanella B, Sannia G (2000) Copper induction of laccase isoenzymes in the ligninolytic fungus Pleurotus ostreatus. Appl Environ Microbiol 66:920–924PubMedCrossRefGoogle Scholar
  70. Palmiter RD (1998) The elusive function of metallothioneins. Proc Natl Acad Sci USA 85:8428–8430CrossRefGoogle Scholar
  71. Pawlowska TE, Charvat I (2004) Heavy-metal stress and development patterns of arbuscular mycorrhizal fungi. Appl Environ Microbiol 70:6643–6649PubMedCrossRefGoogle Scholar
  72. Puig S, Thiele DJ (2002) Molecular mechanisms of copper uptake and distribution. Curr Opin Chem Biol 6:171–180PubMedCrossRefGoogle Scholar
  73. Repetto O, Bestel-Corre G, Dumas-Gaudot E, Berta G, Gianinazzi-Pearson V, Gianinazzi S (2003) Targeted proteomics to identify cadmium-induced protein modifications in Glomus mosseae. -inoculated pea roots New Phytol 157:555–567CrossRefGoogle Scholar
  74. Repetto O, Massa N, Gianinazzi-Pearson V, Dumas-Gaudot E, Berta G (2007) Cadmium effects on populations of root nuclei in two pea genotypes inoculated or not with the arbuscular mycorrhizal fungus Glomus mosseae. Mycorrhiza 17:111–120PubMedCrossRefGoogle Scholar
  75. Rivera-Becerril F, Calantzis C, Turnau K, Caussanel JP, Belimov AA, Gianinazzi S, Strasser RJ, Gianinazzi-Pearson V (2002) Cadmium accumulation and buffering of cadmium-induced stress by arbuscular mycorrhiza in three Pisum sativum. L genotypes. J Exp Bot 53:1177–1185CrossRefGoogle Scholar
  76. Rivera-Becerril F, van Tuinen D, Martin-Laurent F, Metwally A, Dietz K, Gianinazzi S, Gianinazzi-Pearson V (2005) Molecular changes in Pisum sativum. L roots during arbuscular mycorrhiza buffering of cadmium stress. Mycorrhiza 16:51–60Google Scholar
  77. Ruel MT, Bouis HE (1998) Plant breeding: A long-term strategy for the control of zinc deficiency in vulnerable populations. Am J Clin Nutr 68:488S-–494SPubMedGoogle Scholar
  78. Rufyikiri G, Thiry Y, Wang L, Delvaux B, Declerck S (2002) Uranium uptake and translocation by the arbuscular mycorrhizal fungus Glomus intraradices. under root-organ culture conditions New Phytol 156:275–281CrossRefGoogle Scholar
  79. Rufyikiri G, Thiry Y, Declerck S (2003) Contribution of hyphae and roots to uranium uptake and translocation by arbuscular mycorrhizal carrot roots under root-organ culture conditions. New Phytol 158:391–399CrossRefGoogle Scholar
  80. Rufyikiri G, Declerck S, Thiry Y (2004) Comparison of 232. U and 33P uptake and translocation by the arbuscular mycorrhizal fungus Glomus intraradices in root organ culture conditions Mycorrhiza 14:203–207PubMedCrossRefGoogle Scholar
  81. Segerer AH, Burggraf S, Fiala G, Huber G, Huber R, Pley U, Stetter KO (1993) Life in hot springs and hydrothermal vents. Orig Life Evol Biosph 23:77–90PubMedCrossRefGoogle Scholar
  82. Sheehan D, Meade G, Foley VM, Dowd CA (2001) Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. Biochem J 360:1–16PubMedCrossRefGoogle Scholar
  83. Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, LondonGoogle Scholar
  84. Stommel M, Mann P, Franken P (2001) EST-library construction using spore RNA of the arbuscular mycorrhizal fungus Gigaspora rosea. Mycorrhiza 10:281–285CrossRefGoogle Scholar
  85. Strandberg GW, Shumate SE, Parrott JR, Jr (1981) Microbial cells as biosorbents for heavy metals: accumulation of uranium by Saccharomyces cerevisiae. and Pseudomonas aeruginosa Appl Environ Microbiol 41:237–245PubMedGoogle Scholar
  86. Szaniszlo PJ, Powell PE, Reid CPP, Cline GR (1981) Production of hydroxamate siderophores iron chelators by ectomycorrhizal fungi. Mycologia 73:1158–1174CrossRefGoogle Scholar
  87. Titiz O, Tambasco-Studart M, Warzych E, Apel K, Amrhein N, Laloi C, Fitzpatrick TB (2006) PDX1 is essential for vitamin B6 biosynthesis, development and stress tolerance in Arabidopsis. Plant J 48:933–946PubMedCrossRefGoogle Scholar
  88. Tuszynska S, Davies D, Turnau K, Ashford AE (2006) Changes in vacuolar and mitochondrial motility and tubularity in response to zinc in a Paxillus involutus. isolate from a zinc-rich soil Fungal Genet Biol 43:155–163PubMedCrossRefGoogle Scholar
  89. Vasak M, Hasler DW (2000) Metallothioneins: new functional and structural insights. Curr Opin Chem Biol 4:177–183PubMedCrossRefGoogle Scholar
  90. Waschke A, Sich M, Tamasloukht M, Fischer K, Mann P, Franken P (2006) Identification of heavy metal-induced genes encoding glutathione S-transferase in the arbuscular mycorrhizal fungus Glomus intraradices. Mycorrhiza 17:1–10PubMedCrossRefGoogle Scholar
  91. Weiersbye IM, Straker CJ, Przybylowicz WJ (1999) Micro-PIXE mapping of elemental distribution in arbuscular mycorrhizal roots of the grass Cynodon dactylon. , from gold and uranium mine tailings Nucl Inst Methods Phys Res 158:335–343CrossRefGoogle Scholar
  92. Weissenhorn I, Leyval C, Belgy G, Berthelin J (1995) Arbuscular mycorrhizal contribution to heavy metal uptake by maize (Zea mays. ) in pot cultures with contaminated soil Mycorrhiza 5:245–251Google Scholar
  93. Wünschmann J, Beck A, Meyer L, Letzel T, Grill E, Lendzian KJ (2007) Phytochelatins are synthesized by two vacuolar serine carboxypeptidases in Saccharomyces cerevisiae. FEBS Lett 581:1681–1687PubMedCrossRefGoogle Scholar
  94. Zhao H, Eide D (1996) The yeast ZRT1. gene encodes the zinc transporter protein of a high-affinity uptake system induced by zinc limitation Proc Natl Acad Sci USA 93:2454–2458PubMedCrossRefGoogle Scholar
  95. Zhao H, Butler E, Rodgers J, Spizzo T, Duesterhoeft S, Eide D (1998) Regulation of zinc homeostasis in yeast by binding of the ZAP1 transcriptional activator to zinc-responsive promoter elements. J Biol Chem 273:28713–28720PubMedCrossRefGoogle Scholar
  96. Zhu YL, Pilon-Smits EA, Tarun AS, Weber SU, Jouanin L, Terry N (1999) Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing gamma-glutamylcysteine synthetase. Plant Physiol 121:1169–1178PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2009

Authors and Affiliations

  • Manuel González-Guerrero
    • 1
  • Karim Benabdellah
    • 2
  • Nuria Ferrol
    • 2
  • Concepción Azcón-Aguilar
    • 2
    Email author
  1. 1.Department of Chemistry and BiochemistryWorcester Polytechnic InstituteWorcester MAUSA
  2. 2.Departamento de Microbiología del Suelo y Sistemas SimbióticosEstación Experimental del ZaidínSpain

Personalised recommendations