An Integrated Transcriptomic, Proteomic, and Metabolomic Approach to Unravel the Molecular Mechanisms of Metal Stress Tolerance in Plants

  • Parul Parihar
  • Samiksha Singh
  • Rachana Singh
  • G. Rajasheker
  • P. Rathnagiri
  • Rakesh K. Srivastava
  • Vijay Pratap Singh
  • Penna Suprasanna
  • Sheo Mohan Prasad
  • P. B. Kavi Kishor


Industrialization coupled with modern agricultural practices is resulting in heavy metal contamination of both our terrestrial and aquatic systems very rapidly. Metal stress induces a number of morphological, physiological, and genetic defects and thus limits plant growth and productivity. Further, metal stress causes nutritional and water stresses besides oxidative damage in plants. But, plants have evolved diverse intricate mechanisms in order to cope with heavy metal toxicities. Undoubtedly, phytochelatins, metallothione in proteins, and several transcription factors play pivotal roles during metal detoxification and in plant survival under such metal toxicities. Recent advances in transcriptomic, proteomic, and metabolomic approaches have facilitated us to dissect out the complex mechanisms of metal accumulation/tolerance in different plants and their effective management. This book chapter summarizes transcriptomic, proteomic, and metabolomic changes associated with metal stress and how such an understanding can help in generating crop plants that are resilient to metal stress.


Metal stress Phytochelatins Metallothioneins Transcriptomics Proteomics Metabolomics 



PBK is grateful to the CSIR, New Delhi, for providing Emeritus Scientist Fellowship.

Conflict of Interest

Authors declare that they do not have any conflict of interests regarding the publication of this paper.


  1. Ahsan N, Lee DG, Kim KH, Alam I, Lee SH, Lee KW, Lee H, Lee BH (2010) Analysis of arsenic stress-induced differentially expressed proteins in rice leaves by two-dimensional gel electrophoresis coupled with mass spectrometry. Chemosphere 78:224–231PubMedCrossRefGoogle Scholar
  2. Ahsan N, Nakamura T, Komatsu S (2012) Differential responses of microsomal proteins and metabolites in two contrasting cadmium (Cd)-accumulating soybean cultivars under Cd stress. Amino Acids 42:317–327PubMedCrossRefGoogle Scholar
  3. Akashi K, Nishimura N, Ishida Y, Yokota A (2004) Potent hydroxyl radical-scavenging activity of drought-induced type-2 metallothionein in wild watermelon. Biochem Bioph Res Commun 323:72–78CrossRefGoogle Scholar
  4. Al Mahmud J, Hasanuzzaman M, Nahar K, Rahman A, Hossain MS, Fujita M (2017) Maleic acid assisted improvement of metal chelation and antioxidant metabolism confers chromium tolerance in Brassica juncea L. Ecotoxicol Environ Saf 144:216–226PubMedCrossRefGoogle Scholar
  5. Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals- concepts and applications. Chemosphere 91:869–881PubMedCrossRefGoogle Scholar
  6. Alves M, Moes S, Jenö P, Pinheiro C, Passarinho J, Ricardo CP (2011) The analysis of Lupinusalbus root proteome revealed cytoskeleton altered features due to long-term boron deficiency. J Proteome 74:1351–1363CrossRefGoogle Scholar
  7. Anjum NA, Gill SS, Duarte AC, Pereira E, Ahmad I (2013) Silver nanoparticles in soil plant systems. J Nanopart Res 15:1–26. Scholar
  8. Anjum NA, Hasanuzzaman M, Hossain MA, Thangavel P, Roychoudhury A, Gill SS, Rodrigo MAM, Adam V, Fujita M, Kizek R, Duarte AC, Pereira E, Ahmad I (2015) Jacks of metal/metalloid chelation trade in plants-an overview. Front Plant Sci 6:192. Scholar
  9. Arenhart RA, Lima JC, Pedron M, Carvalho FE, Silveira JA, Rosa SB, Caverzan A, Andrade CM, Schünemann M, Margis R, Margis-Pinheiro M (2013) Involvement of ASR genes in aluminium tolerance mechanisms in rice. Plant Cell Environ 36:52–67PubMedCrossRefGoogle Scholar
  10. Baker AJM, McGrath SP, Reeves RD, Smith JAC (2000) Metal hyperaccumulator plants: a review of the ecology and physiology of a biological resource for phytoremediation of metal polluted soils. In: Terry N, Banuelos G (eds) Phytoremediation of contaminated soil and water. Michael Lewis publishers, Boca Raton, pp 85–107Google Scholar
  11. Barcelo J, Poschenrieder C (1990) Plant water relations as affected by heavy metal stress: a review. J Plant Nutr 13:1–37. Scholar
  12. Bernhard WR, Kagi JH (1987) Purification and characterization of a typical cadmium-binding polypeptides from Zea mays. Experientia Suppl 52:309–315PubMedCrossRefGoogle Scholar
  13. Bona E, Marsano M, Massa M, Cattaneo C, Cesaro P, Argese E, Toppi LS, Cavaletto M, Berta G (2011) Proteomic analysis as a tool for investigating arsenic stress in Pterisvittata roots colonized or not by arbuscular mycorrhizal symbiosis. J Proteome 74:1338–1350CrossRefGoogle Scholar
  14. Burkhead JL, Reynolds KA, Abdel-Ghany SE, Cohu CM, Pilon M (2009) Copper homeostasis. New Phytol 182:799–816. Scholar
  15. Carvajal M, Cooke DT, Clarkson DT (1996) Responses of wheat plants to nutrient deprivation may involve the regulation of water-channel function. Planta 199:372–381CrossRefGoogle Scholar
  16. Casterline JL, Barnett NM (1982) Cadmium-binding components in soybean plants. Plant Physiol 69:1004–1007PubMedPubMedCentralCrossRefGoogle Scholar
  17. Castrillo G, Sánchez-Bermejo E, de Lorenzo L, Crevillén P, Fraile-Escanciano A, Tc M, Mouriz A, Catarecha P, Sobrino-Plata J, Olsson S, Leo Del Puerto Y, Mateos I, Rojo E, Hernández LE, Jarillo JA, Piñeiro M, Paz-Ares J, Leyva A (2013) WRKY6 Transcription factor restricts arsenate uptake and transposon activation in Arabidopsis. Plant Cell 25:2944–2957PubMedPubMedCentralCrossRefGoogle Scholar
  18. Chen Z, Pan Y, Wang S, Ding Y, Yang W, Zhu C (2012) Overexpression of a protein disulfideisomerase-like protein from Methanothermobacter thermoautotrophicum enhances mercury tolerance in transgenic rice. Plant Sci 197:10–20PubMedCrossRefGoogle Scholar
  19. Chen Y, Zhi J, Zhang H, Li J, Zhao Q, Xu J (2017) Transcriptome analysis of Phytolaccaamericana L. in response to cadmium stress. PLoS One 12(9):e0184681PubMedPubMedCentralCrossRefGoogle Scholar
  20. Chia MA, Lombardi AT, Melão MGG, Parrish C (2015) Combined nitrogen limitation and cadmium stress stimulate total carbohydrates, lipids, protein and amino acid accumulation in Chlorella vulgaris (Trebouxiophyceae). Aquat Toxicol 160:87–95PubMedCrossRefGoogle Scholar
  21. Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719PubMedCrossRefGoogle Scholar
  22. Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182PubMedCrossRefGoogle Scholar
  23. Collin VC, Eymery F, Genty B, Rey P, Havaux M (2008) Vitamin E is essential for the tolerance of Arabidopsis thaliana to metal induced oxidative stress. Plant Cell Environ 31:244–8257PubMedGoogle Scholar
  24. Cuypers A, Smeets K, Vangronsveld J (2009) Heavy metal stress in plants. In: Hirt H (ed) Plant stress biology: from genomics to systems biology. Wiley-VCH Verlag, Weinheim, pp 161–178CrossRefGoogle Scholar
  25. Dago A, Gonzalez I, Arino C, Diaz-Cruz JM, Esteban M (2014) Chemometrics applied to the analysis of induced phytochelatins in Hordeum vulgare plants stressed with various toxic non-essential metals and metalloids. Talanta 118:201–209. Scholar
  26. DalCorso G, Farinati S, Maistri S, Furini A (2008) How plants cope with cadmium: staking all on metabolism and gene expression. J Integr Plant Biol 50:1268–1280PubMedCrossRefGoogle Scholar
  27. DalCorso G, Fasani E, Furini A (2013) Recent advances in the analysis of metal hyperaccumulation and hypertolerance in plants using proteomics. Front Plant Sci 4:280PubMedPubMedCentralCrossRefGoogle Scholar
  28. Dalvi AA, Bhalerao SA (2013) Response of plants towards heavy metal toxicity: an overview of avoidance, tolerance and uptake mechanism. Annals of Plant Sciences 2:362–368Google Scholar
  29. Duan GL, Hu Y, Lui WJ, Kneer R, Zhao FJ, Zhu YG (2011) Evidence for a role of phytochelatins in regulating arsenic accumulation in rice grains. Environ Exp Bot 71:416–421. Scholar
  30. Elbaz B, Shoshani-Knaani N, David-Assael O, Mizrachy-Dagri T, Mizrahi K, Saul H, Brook E, Berezin I, Shaul O (2006) High expression in leaves of the zinc hyperaccumulator Arabidopsis halleri of AhMHX, a homolog of an Arabidopsis thaliana vacuolar metal/proton exchanger. Plant Cell Environ 29:1179–1190PubMedCrossRefGoogle Scholar
  31. Enger MD, Tesmer JG, Travis GL, Barham SS (1986) Clonal variation of cadmium response in human-tumor cell-lines. Am J Phys 250:C256–C263CrossRefGoogle Scholar
  32. Feleafel MN, Mirdad ZM (2013) Hazard and effects of pollution by lead on vegetable crops. J Agric Environ Ethic 26:547–567. Scholar
  33. Freisinger E (2011) Structural features specific to plant metallothioneins. J Biol Inorg Chem 16:1035–1045. Scholar
  34. Führs H, Behrens C, Gallien S, Heintz D, Van Dorsselaer A, Braun HP, Horst WJ (2010) Physiological and proteomic characterization of manganese sensitivity and tolerance in rice (Oryza sativa) in comparison with barley (Hordeumvulgare). Ann Bot 105:1129–1140PubMedPubMedCentralCrossRefGoogle Scholar
  35. Fukao Y, Ferjani A, Tomioka R, Nagasaki N, Kurata R, Nishimori Y, Fujiwara M, Maeshima M (2011) iTRAQ analysis reveals mechanisms of growth defects due to excess zinc in Arabidopsis. Plant Physiol 155:1893–1907PubMedPubMedCentralCrossRefGoogle Scholar
  36. Gabbrielli R, Pandolfini T, Espen L, Palandri MR (1999) Growth, peroxidase activity and cytological modifications in Pisum sativum seedlings exposed to Ni2+ toxicity. J Plant Physiol 155:639–645. Scholar
  37. Gallego SM, Pena LB, Barcia RA, Azpilicueta CE, Iannone MF, Rosales EP, Zawoznik MS, Groppa MD, Benavides MP (2012) Unravelling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms. Environ Exp Bot 83:33–46. Scholar
  38. Gao J, Sun L, Yang X, Liu JX (2013) Transcriptomic analysis of cadmium stress response in the heavy metal hyperaccumulator Sedum alfrediiHance. PLoS One 8:e64643PubMedPubMedCentralCrossRefGoogle Scholar
  39. Gao J, Luo M, Zhu Y, He Y, Wang Q, Zhang C (2015) Transcriptome sequencing and differential gene expression analysis in Viola yedoensis Makino (Fam. Violaceae) responsive to cadmium (Cd) pollution. Biochem Biophys Res Commun 459:60–65PubMedCrossRefPubMedCentralGoogle Scholar
  40. Gautam N, Verma PK, Verma S, Tripathi RD, Trivedi PK, Adhikari B (2012) Genome-wide identification of rice class I metallothionein gene: tissue expression patterns and induction in response to heavy metal stress. Funct Integr Genomics 12:635–647. Scholar
  41. Gekeler W, Grill E, Winnacker EL, Zenk MH (1989) Survey of the plant kingdom for the ability to bind heavy metals through phytochelatins. Z Naturforsch 44:361–369CrossRefGoogle Scholar
  42. Gothberg A, Greger M, Holm K, Bengtsson BE (2004) Influence of nutrient levels on uptake and effects of mercury, cadmium, and lead in water spinach. J Environ Qual 33:1247–1255. Scholar
  43. Grill E, Gekeler W, Winnacker E-L, Zenk MH (1986) Homo-phytochelatins are heavy metal-binding peptides of homo-glutathione containing Fabales. FEBS Lett 205:47–50CrossRefGoogle Scholar
  44. Grill E, Loffler S, Winnacker EL, Zenk MH (1989) Phytochelatins, the heavy-metal-binding peptides of plants, are synthesized from glutathione by a specific gamma-glutamyl cysteine dipeptidyltranspeptidase (phytochelatin synthase). Proc Natl Acad Sci U S A 86:6838–6842PubMedPubMedCentralCrossRefGoogle Scholar
  45. Guerinot ML (2000) The ZIP family of metal transporters. Biochim Biophys Acta 1465:190–198. Scholar
  46. Guo WJ, Bundithya W, Goldsbrough PB (2003) Characterization of the Arabidopsis metallothionein gene family: tissue-specific expression and induction during senescence and in response to copper. New Phytol 159:369–381. Scholar
  47. Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11. Scholar
  48. Han FX, Sridhar BBM, Monts DL, Su Y (2004) Phytoavailability and toxicity of trivalent and hexavalent chromium to Brassica juncea. New Phytol 162:489–499. Scholar
  49. Han X, Yin H, Song X, Zhang Y, Liu M, Sang J, jiang J, Li J, Zhuo R (2016) Integration of small RNAs, degradome and transcriptome sequencing in hyperaccumulator Sedum alfredii uncovers a complex regulatory network and provides insights into cadmium phytoremediation. Plant Biotechnol J 14:1470–1483PubMedPubMedCentralCrossRefGoogle Scholar
  50. Hassinen VH, Tervahauta AI, Schat H, Kärenlampi SO (2011) Plant metallothioneins-metal chelators with ROS scavenging activity? Plant Biol 13:225–232. Scholar
  51. Herbette S, Taconnat L, Hugouvieux V, Piette L, Magniette ML, Cuine S, Auroy P, Richaud P, Forestier C, Bourguignon J, Renou JP, Vavasseur A, Leonhardt N (2006) Genome-wide transcriptome profiling of the early cadmium response of Arabidopsis roots and shoots. Biochimie 88:1751–1765PubMedCrossRefGoogle Scholar
  52. Higashimoto M, Isoyama N, Ishibashi S, Inoue M, Takiguchi M, Suzuki S, Ohnishi Y, Sato M (2009) Tissue-dependent preventive effect of metallothionein against DNA damage in dyslipidemic mice under repeated stresses of fasting or restraint. Life Sci 84:569–575PubMedCrossRefGoogle Scholar
  53. Hossain Z, Komatsu S (2012) Contribution of proteomic studies towards understanding plant heavy metal stress response. Front Plant Sci 3:310PubMedGoogle Scholar
  54. Hossain MA, Piyatida P, Jaime A, da Silva T, Fujita M (2012a) Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J Bot. Scholar
  55. Hossain Z, Hajika M, Komatsu S (2012b) Comparative proteome analysis of high and low cadmium accumulating soybeans under cadmium stress. Amino Acids 43:2393–2416PubMedCrossRefGoogle Scholar
  56. Jin S, Cheng Y, Guan Q, Liu D, Takano T, Liu S (2006). A metallothionein-like protein of rice (rgMT) functions in E. coli and its gene expression is induced by abiotic stresses. Biotechnol Lett 28:1749–1753PubMedCrossRefGoogle Scholar
  57. John R, Ahmad P, Gadgil K, Sharma S (2009) Heavy metal toxicity: effect on plant growth, biochemical parameters and metal accumulation by Brassica juncea L. Int J Plant Prod 3:65–76Google Scholar
  58. Karin M, Cathala G, Nguyenhuu MC (1983) Expression and regulation of a human metallothionein gene carried on an autonomously replicating shuttle vector. Proc Natl Acad Sci U S A 80:4040–4044PubMedPubMedCentralCrossRefGoogle Scholar
  59. Khan MIR, Khan NA (2014) Ethylene reverses photosynthetic inhibition by nickel and zinc in mustard through changes in PS II activity, photosynthetic nitrogen use efficiency, and antioxidant metabolism. Protoplasma 251:1007–1019PubMedCrossRefGoogle Scholar
  60. Kieffer P, Dommes J, Hoffmann L, Hausman JF, Renaut J (2008) Quantitative changes in protein expression of cadmium exposed poplar plants. Proteomics 8:2514–2430PubMedCrossRefGoogle Scholar
  61. Kieffer P, Planchon S, Oufir M, Ziebel J, Dommes J, Hoffmann L (2009) Combining proteomics and metabolite analyses to unravel cadmium stress- response in poplar leaves. J Proteome Res 8:400–417PubMedCrossRefGoogle Scholar
  62. Klapheck S, Chrost B, Starke J, Zimmermann H (1992) γ-Glutamylcysteinylserine: a new homologue of glutathione in plants of the family Poaceae. Bot Acta 105:174–179CrossRefGoogle Scholar
  63. Kondo N, lsobe M, Imai K, Goto T (1985) Synthesis of metallothionein-like peptides cadystin A and B occurring in a fission yeast, and their isomers. Agric Biol Chem 49:71–83Google Scholar
  64. Lasat MM (2002) Phytoextraction of toxic metals: a review of biological mechanisms. J Environ Qual 31:109–120PubMedCrossRefGoogle Scholar
  65. Laureysens I, Blust R, De Temmerman L, Lemmens C, Ceulemans R (2004) Clonal variation in heavy metal accumulation and biomass production in a poplar coppice culture: I. Seasonal variation in leaf, wood and bark concentrations. Environ Pollut 131:485–494PubMedCrossRefGoogle Scholar
  66. Lee K, Bae DW, Kim SH, Han HJ, Liu X, Park HC, Lim CO, Lee SY, Chung WS (2010) Comparative proteomic analysis of the short-term responses of rice roots and leaves to cadmium. J Plant Physiol 167:161–168PubMedCrossRefGoogle Scholar
  67. Leopold I, Gunther D, Schmidt J, Neumann D (1999) Phytochelatins and heavy metal tolerance. Phytochemistry 50:1323–1328CrossRefGoogle Scholar
  68. Lingua G, Bona E, Todeschini V, Cattaneo C, Marsano F, Berta G, Cavaletto M (2012) Effects of heavy metal and arbuscularmycorrhiza on the leaf proteome of a selected Poplar clone: a time course analysis. PLoS One 7:e38662PubMedPubMedCentralCrossRefGoogle Scholar
  69. Liu X, Wu H, Ji C, Wei L, Zhao J, Yu J (2013) An integrated proteomic and metabolomic study on the chronic effects of mercury in Suaeda salsa under an environmentally relevant salinity. PLoS One 8:e64041PubMedPubMedCentralCrossRefGoogle Scholar
  70. Liu W, Xu L, Wang Y, Shen H, Zhu X, Zhang K, Chen Y, Yu R, Limera C, Liu L (2015a) Transcriptome-wide analysis of chromium-stress responsive microRNAs to explore miRNA8 mediated regulatory networks in radish (Raphanus sativus L.). Sci Rep 5:14024Google Scholar
  71. Liu T, Zhu S, Tang Q, Tang S (2015b) Genome-wide transcriptomic profiling of ramie (Boehmeria nivea L. Gaud) in response to cadmium stress. Gene 558:131–137PubMedCrossRefGoogle Scholar
  72. Llamas A, Ullrich CI, Sanz A (2000) Cd2+effects on transmembrane electrical potential difference, respiration and membrane permeability of rice (Oryza sativa L.) roots. Plant Soil 219:21–28. Scholar
  73. Llamas A, Ullrich CI, Sanz A (2008) Ni2+ toxicity in rice: effect on membrane functionality and plant water content. Plant Physiol Biochem 46:905–910. Scholar
  74. Loebus J, Leitenmaier B, Meissner D, Braha B, Krauss GJ, Dobritzsch D, Freisinger E (2013) The major function of a metallothionein from the aquatic fungus Heliscus lugdunensis is cadmium detoxification. J Inorg Biochem 127:253–260PubMedCrossRefGoogle Scholar
  75. Lux A, Martinka M, Vaculık M, White PJ (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62:21–37. Scholar
  76. Lv Y, Deng X, Quan L, Xia Y, Shen Z (2013) Metallothioneins BcMT1 and BcMT2 from Brassica campestris enhance tolerance to cadmium and copper and decrease production of reactive oxygen species in Arabidopsis thaliana. Plant Soil 367:507–519CrossRefGoogle Scholar
  77. Maestri E, Marmiroli M, Visioli G, Marmiroli N (2010) Metal tolerance and hyperaccumulation: costs and trade-offs between traits and environment. Environ Exp Bot 68:1–13. Scholar
  78. Maggio A, Joly RJ (1995) Effects of mercuric chloride on the hydraulic conductivity of tomato root systems (evidence for a channel-mediated water pathway). Plant Physiol 109:331–335PubMedPubMedCentralCrossRefGoogle Scholar
  79. Malar S, Vikram SS, Favas PJC, Perumal V (2014) Lead heavy metal toxicity induced changes on growth and antioxidative enzymes level in water hyacinths [Eichhorniacrassipes (Mart.)]. Bot Stud 55:54PubMedPubMedCentralCrossRefGoogle Scholar
  80. Manara A (2012) Plant responses to heavy metal toxicity. In: Furini A (ed) Plants and heavy metals, Springer briefs in molecular science. Springer, Dordrecht, pp 27–53CrossRefGoogle Scholar
  81. Margoshes M, Valle BL (1957) A cadmium protein from equine kidney cortex. J Am Chem Soc 79:4813–4814CrossRefGoogle Scholar
  82. Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, London, pp 405–435CrossRefGoogle Scholar
  83. Mehes-Smith M, Nkongolo K, Cholewa E (2013) Coping mechanisms of plants to metal contaminated soil. In: Steven S (ed) Environmental change and sustainability, InTech Open, London, UK.
  84. Mehra RK, Winge DR (1988) Cu(I) binding to the Saccharomyces pombe γ-glutamylpeptides varying in chain lengths. Arch Biochem Biophys 265:381–389PubMedCrossRefGoogle Scholar
  85. Mendoza-Cózatl DG, Butko E, Springer F, Torpey JW, Komives EA, Kehr J, Schroeder JI (2008) Identification of high levels of phytochelatins, glutathione and cadmium in the phloem sap of Brassica napus. A role for thiol peptides in the long-distance transport of cadmium and the effect of cadmium on iron translocation. Plant J 54:249–259PubMedPubMedCentralCrossRefGoogle Scholar
  86. Meuwly P, Thibault P, Rauser WE (1993) γ-Glutamylcysteinyl glutamic acid; a new homologue of glutathione in maize seedlings exposed to cadmium. FEBS Lett 336:472–476PubMedCrossRefGoogle Scholar
  87. Meuwly P, Thibault P, Schwan AL, Rauser WE (1995) Three families of thiol peptides are induced by cadmium in maize. Plant J 7:391–400PubMedCrossRefGoogle Scholar
  88. Mir G, Domènech J, Huguet G, Guo WJ, Goldsbrough P, Atrian S, Molinas M (2004) A plant type 2 metallothionein (MT) from cork tissue responds to oxidative stress. J Exp Bot 55:2483–2493PubMedCrossRefGoogle Scholar
  89. Montargès-Pelletier E, Chardot V, Echevarria G, Michot LJ, Bauer A, Morel JL (2008) Identification of nickel chelators in three hyperaccumulating plants: an X-ray spectroscopic study. Phytochemistry 69:1695–1709PubMedCrossRefGoogle Scholar
  90. Morelli E, Scarano G (2001) Synthesis and stability of phytochelatins induced by cadmium and lead in the marine diatom Phaeodactylum tricornutum. Mar Environ Res 52:383–395. Scholar
  91. Nadgorska-Socha A, Kafel A, Kandziora-Ciupa M, Gospodarek J, Zawisza-Raszka A (2013) Accumulation of heavy metals and antioxidant responses in Viciafaba plants grown on monometallic contaminated soil. Environ Sci Pollut Res 20:1124–1134CrossRefGoogle Scholar
  92. Nahar K, Hasanuzzaman M, Alam MM, Rahmana A, Suzuki T, Fujita M (2016) Polyamine and nitric oxide crosstalk: antagonistic effects on cadmium toxicity in mung bean plants through up-regulating the metal detoxification, antioxidant defense and methylglyoxal detoxification systems. Ecotoxicol Environ Saf 126:245–255PubMedCrossRefPubMedCentralGoogle Scholar
  93. Nakashima K, Ito Y, Yamaguchi-Shinozaki K (2009) Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol 149:88–95PubMedPubMedCentralCrossRefGoogle Scholar
  94. Nath S, Panda P, Mishra S, Dey M, Choudhury S, Sahoo L, Panda SK (2014) Arsenic stress in rice: redox consequences and regulation by iron. Plant Physiol Biochem 80:203–210PubMedCrossRefGoogle Scholar
  95. Nazar R, Iqbal N, Masood A, Iqbal M, Khan R, Syeed S, Khan NA (2012) Cadmium toxicity in plants and role of mineral nutrients in its alleviation. Am J Plant Sci 3:1476–1489. Scholar
  96. Oono Y, Yazawa T, Kawahara Y, Kanamori H, Kobayashi F, Sasaki H, Mori S, Wu Z, Handa H, Itoh T, Matsumoto T (2014) Genome-wide transcriptome analysis reveals that cadmium stress signaling controls the expression of genes in drought stress signal pathways in rice. PLoS One 9:e96946PubMedPubMedCentralCrossRefGoogle Scholar
  97. Oono Y, Yazawa T, Kanamori H, Sasaki H, Mori S, Handa H, Matsumoto T (2016) Genome-wide transcriptome analysis of cadmium stress in rice. BioMed Res Int 2016:9739505PubMedPubMedCentralCrossRefGoogle Scholar
  98. Opdenakker K, Remans T, Keunen E, Vangronsveld J, Cuypers A (2012) Exposure of Arabidopsis thaliana to Cd or Cu excess leads to oxidative stress mediated alterations in MAP Kinase transcript levels. Environ Exp Bot 83:53–61CrossRefGoogle Scholar
  99. Pandey S, Rai R, Rai LC (2012) Proteomics combines morphological, physiological and biochemical attributes to unravel the survival strategy of Anabaena sp. PCC7120 under arsenic stress. J Proteome 75:921–937CrossRefGoogle Scholar
  100. Patra M, Bhowmik N, Bandopadhyay B, Sharma A (2004) Comparison of mercury, lead and arsenic with respect to genotoxic effects on plant systems and the development of genetic tolerance. Environ Exp Bot 52:199–223CrossRefGoogle Scholar
  101. Perfus-Barbeoch L, Leonhardt N, Vavasseur A, Forestier C (2002) Heavy metal toxicity: cadmium permeates through calcium channels and disturbs the plant water status. Plant J 32:539–548. Scholar
  102. Peroza EA, Schmucki R, Guntert P, Freisinger E, Zerbe O (2009) The β-domain of wheat metallothionein: a metal binding domain with a distinctive structure. J Mol Biol 387:207–218PubMedCrossRefGoogle Scholar
  103. Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? and what makes them so interesting? Plant Sci 180:169–181PubMedCrossRefGoogle Scholar
  104. Rauser WE (1999) Structure and function of metal chelators produced by plants. The case for organic acids, amino acids, phytin and metallothioneins. Cell Biochem Biophys 31:19–48PubMedCrossRefGoogle Scholar
  105. Rezvani M, Zaefarian F, Miransari M, Nematzadeh GA (2012) Uptake and translocation of cadmium and nutrients by Aeluropus littoralis. Arch Agron Soil Sci 58:1413–1425. Scholar
  106. Ritter A, Ubertini M, Romac S, Gaillard F, Delage L, Mann A, Cock JM, Tonon T, Correa JA, Potin P (2010) Copper stress proteomics highlights local adaptation of two strains of the model brown alga Ectocarpussiliculosus. Proteomics 10:2074–2088PubMedCrossRefGoogle Scholar
  107. Robinson NJ, Urwin PE, Robinson PJ, Jackson PJ (1994) Gene expression in relation to metal toxicity and tolerance. In: Basra AS (ed) Stress-induced gene expression in plants. Harwood Academic Publisher, UK, pp 209–248Google Scholar
  108. Rodriguez-Celma J, Rellan-Alvarez R, Abadia A, Abadia J, Lopez- Millan AF (2010) Changes induced by two levels of cadmium toxicity in the 2-DE protein profile of tomato roots. J Proteome 73:1694–1706CrossRefGoogle Scholar
  109. Roosens NH, Bernard C, Leplae R, Verbruggen N (2004) Evidence for copper homeostasis function of metallothionein (MT3) in the hyperaccumulator Thlaspi caerulescens. FEBS Lett 577:9–16. Scholar
  110. Roosens NH, Leplae R, Bernard C, Verbruggen N (2005) Variations in plant metallothioneins: the heavy metal hyper accumulator Thlaspi caerulescens as a study case. Planta 222:716–729. Scholar
  111. Rucinska-Sobkowiak R (2016) Water relations in plants subjected to heavy metal stresses. Acta Physiol Plant 38:257. Scholar
  112. Rucinska-Sobkowiak R, Nowaczyk G, Krzesłowska M, Rabeda I, Jurga S (2013) Water status and water diffusion transport in lupine roots exposed to lead. Environ Exp Bot 87:100–109. Scholar
  113. Ruttkay-Nedecky B, Nejd L, Gumulec J, Zitka O, Masarik M, Eckschlager T, Stiborova M, Adam V, Kizek R (2013) The role of metallothionein in oxidative stress. Int J Mol Sci 14:6044–6066. Scholar
  114. Salt DE, Rauser WE (1995) Mg-ATP dependent transport of phytochelatins across the tonoplast of oat roots. Plant Physiol 107:1293–1301PubMedPubMedCentralCrossRefGoogle Scholar
  115. Samson SLA, Gedamu L (1997) Molecular Analyses of Metallothionein Gene Regulation. Progress in Nucleic Acid Research and Molecular Biology 59:257–288Google Scholar
  116. Schneider T, Schellenberg M, Meyer S, Keller F, Gehrig P, Riedel K, Lee Y, Eberl L, Martinoia E (2009) Quantitative detection of changes in the leaf-mesophyll tonoplast proteome in dependency of a cadmium exposure of barley (Hordeumvulgare L.) plants. Proteomics 9:2668–2677PubMedCrossRefGoogle Scholar
  117. Semane B, Dupae J, Cuypers A, Noben JP, Tuomainen M, Tervahauta A, Sirpa K, Frank Van B, Karen S, Jaco V (2010) Leaf proteome responses of Arabidopsisthaliana exposed to mild cadmium stress. J Plant Physiol 167:247–254PubMedCrossRefGoogle Scholar
  118. Seth CS, Chaturvedi PK, Misra V (2008) The role of phytochelatins and antioxidants in tolerance to Cd accumulation in Brassica juncea L. Ecotoxicol Env Saf 71:76–85CrossRefGoogle Scholar
  119. Seth C, Remans T, Keunen E, Jozefczak M, Gielen H, Opdenakker K, Weyens N, Vangronsveld J, Cuypers A (2012) Phytoextraction of toxic metals: a central role for glutathione. Plant Cell Environ 35:334–346. Scholar
  120. Shameer K, Ambika S, Varghese SM, Karaba N, Udayakumar M, Sowdhamini R (2009) STIFDB – Arabidopsis stress-responsive transcription factor data base. Int J Plant Genomics 2009:583429PubMedPubMedCentralCrossRefGoogle Scholar
  121. Sharma I (2012) Arsenic induced oxidative stress in plants. Biologia 67:447–453. Scholar
  122. Sharma SS, Dietz KJ (2009) The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci 14:43–50PubMedCrossRefGoogle Scholar
  123. Sharmin SA, Alam I, Kim KH, Kim YG, Kim PJ, Bahk JD, Lee BH (2012) Chromium-induced physiological and proteomic alterations in roots of Miscanthussinensis. Plant Sci 187:113–126PubMedCrossRefGoogle Scholar
  124. Shen ZG, Zhao FJ, McGrath SP (1997) Uptake and transport of zinc in the hyperaccumulator Thlaspi caerulescens and the non-hyperaccumulator Thlaspi ochroleucum. Plant Cell Environ 20:898–906CrossRefGoogle Scholar
  125. Shiu SH, Shih MC, Li WH (2005) Transcription factor families have much higher expansion rates in plants than in animals. Plant Physiol 139:18–26PubMedPubMedCentralCrossRefGoogle Scholar
  126. Shukla D, Kesari R, Tiwari M, Dwivedi S, Tripathi RD, Nath P, Trivedi PK (2013) Expression of Ceratophyllum demersum phytochelatin synthase, CdPCS1, in Escherchia coli and Arabidopsis enhances heavy metal(loid)s accumulation. Protoplasma 250:1263–1272. Scholar
  127. Silva P, Matos M (2016) Assessment of the impact of aluminum on germination, early growth and free proline content in Lactuca sativa L. Ecotoxicol Environ Saf 131:151–156PubMedCrossRefGoogle Scholar
  128. Singh S, Parihar P, Singh R, Singh VP, Prasad SM (2015) Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. Front Plant Sci 6:1143PubMedGoogle Scholar
  129. Siripornadulsil S, Traina S, Verma DPS, Sayre RT (2002) Molecular mechanisms of proline-mediated tolerance to toxic heavy metal in transgenic microalgae. Plant Cell 14:2837–2847PubMedPubMedCentralCrossRefGoogle Scholar
  130. Sobrino-Plata J, Ortega-Villasante C, Flores-Cáceres ML, Escobar C, Del Campo FF, Hernández LE (2009) Differential alterations of antioxidant defenses as bioindicators of mercury and cadmium toxicity in alfalfa. Chemosphere 77:946–954. Scholar
  131. Sobrino-Plata J, Meyssen D, Cuypers A, Escobar C, Hernández LE (2014) Glutathione is a key antioxidant metabolite to cope with mercury and cadmium stress. Plant Soil 377:369–381CrossRefGoogle Scholar
  132. Solanki R, Dhankhar R (2011) Biochemical changes and adaptive strategies of plants under heavy metal stress. Biologia 66:195–204. Scholar
  133. Song WY, Mendoza-Cozatl DG, Lee Y, Schroeder JI, Ahn SN, Lee H, Wicker T, Martinoia E (2014) Phytochelatin-metal(loid) transport into vacuoles shows different substrate preferences in barley and Arabidopsis. Plant Cell Environ 37:1192–1201. Scholar
  134. Srivalli S, Khanna-Chopra R (2008) Delayed wheat flag leaf senescence due to the removal of spikelets is associated with increased activities of leaf antioxidant enzymes, reduced glutathione/oxidized glutathione ratio and oxidative damage to mitochondrial proteins. Plant Physiol Biochem 47:663–670. Scholar
  135. Subashchandrabose SR, Wang L, Venkateswarlu K, Naidu R, Megharaj M (2017) Interactive effects of PAHs and heavy metal mixtures on oxidative stress in Chlorella sp. MM3 as determined by artificial neural network and genetic algorithm. Algal Res 21:203–212CrossRefGoogle Scholar
  136. Sun JY, Shen ZG (2007) Effects of Cd stress on photosynthetic characteristics and nutrient uptake of cabbages with different Cd-tolerance. Chin J Appl Ecol 18:2605–2610Google Scholar
  137. Sytar O, Kumar A, Latowski D, Kuczynska P, Strzałka K, Prasad MNV (2013) Heavy metal-induced oxidative damage, defense reactions, and detoxifcation mechanisms in plants. Acta Physiol Plant 385:985–999CrossRefGoogle Scholar
  138. Takahashi H, Kawakatsu T, Wakasa Y, Hayashi S, Takaiwa F (2012) A rice transmembrane bZIP transcription factor, OsbZIP39, regulates the endoplasmic reticulum stress response. Plant Cell Physiol 53:144–153PubMedCrossRefGoogle Scholar
  139. Thangavel P, Long S, Minocha R (2007) Changes in phytochelatins and their biosynthetic intermediates in red spruce (Picea rubens Sarg.) cell suspension cultures under cadmium and zinc stress. Plant Cell Tissue Org Cult 88:201–216. Scholar
  140. Toppi LS, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130CrossRefGoogle Scholar
  141. Usman K, Mienda BS, Idris S, Idris ZL (2015) Type-4 plant metallothioneins (MT4): an overview of Hordeum vulgare. Int J Tech Res Appl 3:269–271Google Scholar
  142. Vaculık M, Konlechner C, Langer I, Adlassnig W, Puschenreiter M, Lux A, Hauser MT (2012) Root anatomy and element distribution vary between two Salix caprea isolates with different Cd accumulation capacities. Environ Pollut 163:117–126. Scholar
  143. Vannini C, Marsoni M, Domingo G, Antognoni F, Biondi S, Bracale M (2009) Proteomic analysis of chromate-induced modifications in Pseudokirchneriellasubcapitata. Chemosphere 76:1372–1379PubMedCrossRefGoogle Scholar
  144. Vasak M, Hasler DW (2000) Metallothioneins: new functional and structural insights. Curr Opin Chem Biol 4:177–183PubMedCrossRefGoogle Scholar
  145. Verbruggen N, Hermans C, Schat H (2009) Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 181:759–776. Scholar
  146. Viehweger K (2014) How plants cope with heavy metals. Bot Stud 55:1–12CrossRefGoogle Scholar
  147. Walliwalagedara C, van Keulen H, Willard B, Wei R (2012) Differential proteome analysis of Chlamydomonasreinhardtii response to arsenic exposure. Am J Plant Sci 3:764–772CrossRefGoogle Scholar
  148. Wang HC, Wu JS, Chia JC, Yang CC, Wu YJ, Juang RH (2009) Phytochelatin synthase is regulated by protein phosphorylation at a threonine residue near its catalytic site. J Agric Food Chem 57:7348–7355. Scholar
  149. Wang Y, Hu H, Zhu LY, Li XX (2012) Response to nickel in the proteome of the metal accumulator plant Brassica juncea. J Plant Interact 7:230–237CrossRefGoogle Scholar
  150. Wang R, Gao F, Guo BG, Huang JC, Wang L, Zhou YJ (2013) Short-term chromium-stress-induced alterations in the maize leaf proteome. Int J Mol Sci 14:11125–11144PubMedPubMedCentralCrossRefGoogle Scholar
  151. Wang Y, Xu L, Shen H, Wang J, Liu W, Zhu X, Wang R, Sun X, Liu L (2015) Metabolomic analysis with GC-MS to reveal potential metabolites and biological pathways involved in Pb and Cd stress response of radish roots. Sci Rep 5:18296PubMedPubMedCentralCrossRefGoogle Scholar
  152. Witters N, Van Slycken S, Meers E, Adriaensen K, Meiresonne L, Tack FMG, Vangronsveld J, Thewys T (2009) Short-rotation coppice of willow for phytoremediation of a metal-contaminated agricultural area: a sustainability assessment. Bioenergy Res 2:144–152CrossRefGoogle Scholar
  153. Wray GA, Hahn MW, Abouheif E, Balhoff JP, Pizer M, Rockman MV, Romano LA (2003) The evolution of transcriptional regulation in eukaryotes. Mol Biol Evol 20:1377–1419PubMedCrossRefGoogle Scholar
  154. Wu H, Chen C, Du J, Liu H, Cui Y, Zhang Y, He Y, Wang Y, Chu C, Feng Z, Li J, Ling HQ (2012) Co-overexpression FIT with AtbHLH38 or AtbHLH39 in Arabidopsis-enhanced cadmium tolerance via increased cadmium sequestration in roots and improved iron homeostasis of shoots. Plant Physiol 158:790–800. Scholar
  155. Wu CS, Chen DY, Chang CF, Li MJ, Hung KY, Chen LJ, Chen PW (2014) The promoter and the 50-untranslated region of rice metallothionein OsMT2b gene are capable of directing high-level gene expression in germinated rice embryos. Plant Cell Rep 33:793–806PubMedCrossRefGoogle Scholar
  156. Xu J, Zhu Y, Ge Q, Li Y, Sun J, Zhang Y, Liu X (2012) Comparative physiological responses of Solanumnigrum and Solanumtorvum to cadmium stress. New Phytol 196:125–138PubMedCrossRefGoogle Scholar
  157. Xu L, Wang Y, Liu W, Wang J, Zhu X, Zhang K, Yu R, Wang R, Xie Y, Zhang W, Gong Y, Liu L (2015) De novo sequencing of root transcriptome reveals complex cadmium-responsive regulatory networks in radish (Raphanussativus L.). Plant Sci 236:313–323PubMedCrossRefGoogle Scholar
  158. Yoshihara T, Hodoshima H, Miyano Y, Shoji K, Shimada H, Goto F (2006) Cadmium inducible Fe deficiency responses observed from macro and molecular views in tobacco plants. Plant Cell Rep 25:365–373. Scholar
  159. Yu L-J, Luo Y-F, Liao B, Xie L-J, Chen L, Xiao S, Li JT, Hu S, Shu W-S (2012) Comparative transcriptome analysis of transporters, phytohormone and lipid metabolism pathways in response to arsenic stress in rice (Oryzasativa). New Phytol 195:97–112PubMedCrossRefGoogle Scholar
  160. Yu R, Li D, Du X, Xia S, Liu C, Shi G (2017) Comparative transcriptome analysis reveals key cadmium transport-related genes in roots of two pakchoi (Brassica rapa L. ssp. chinensis) cultivars. BMC Genomics 18:587PubMedPubMedCentralCrossRefGoogle Scholar
  161. Yusuf M, Fariduddin Q, Ahmad A (2012) 24-Epibrassinolide modulates growth, nodulation, antioxidant system, and osmolyte in tolerant and sensitive varieties of Vignaradiata under different levels of nickel: a shotgun approach. Plant Physiol Biochem 57:143–153PubMedCrossRefGoogle Scholar
  162. Zenk MH (1996) Heavy metal detoxification in higher plants- a review. Gene 179:21–30PubMedPubMedCentralCrossRefGoogle Scholar
  163. Zhang H, Lian C, Shen Z (2009) Proteomic identification of small, copper-responsive proteins in germinating embryos of Oryzasativa. Ann Bot 103:923–930PubMedPubMedCentralCrossRefGoogle Scholar
  164. Zhao L, Sun YL, Cui SX, Chen M, Yang HM, Liu HM, Chai TY, Huang F (2011) Cd induced changes in leaf proteome of the hyperaccumulator plant Phytolaccaamericana. Chemosphere 85:56–66PubMedCrossRefGoogle Scholar
  165. Zhou B, Yao W, Wang S, Wang X, Jiang T (2014) The metallothionein gene, TaMT3, from Tamarix androssowii confers Cd2+ tolerance in tobacco. Int J Mol Sci 15:10398–10409PubMedPubMedCentralCrossRefGoogle Scholar
  166. Zimeri AM, Dhankher OP, McCaig B, Meagher RB (2005) The plant MT1 metallothioneins are stabilized by binding cadmiums and are required for cadmium tolerance and accumulation. Plant Mol Biol 58:839–855. Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Parul Parihar
    • 1
  • Samiksha Singh
    • 1
  • Rachana Singh
    • 1
  • G. Rajasheker
    • 2
  • P. Rathnagiri
    • 3
  • Rakesh K. Srivastava
    • 4
  • Vijay Pratap Singh
    • 5
  • Penna Suprasanna
    • 6
  • Sheo Mohan Prasad
    • 1
  • P. B. Kavi Kishor
    • 2
  1. 1.Ranjan Plant Physiology and Biochemistry Laboratory, Department of BotanyUniversity of AllahabadAllahabadIndia
  2. 2.Department of GeneticsOsmania UniversityHyderabadIndia
  3. 3.Genomix Molecular Diagnostics Pvt. Ltd.Kukatpally, HyderabadIndia
  4. 4.International Crops Research Institute for the Semi-Arid Tropics (ICRISAT)Patancheru, HyderabadIndia
  5. 5.Govt. R.P.S. Post Graduate CollegeBaikunthpurIndia
  6. 6.Nuclear Agriculture & Biotechnology DivisionBhabha Atomic Research CentreTrombay, MumbaiIndia

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