Biomolecular Functions of Micronutrients Toward Abiotic Stress Tolerance in Plants

  • Shyam N. Pandey


Many of the world’s cultivated areas are facing various abiotic stresses such as drought, salinity, temperature extremes, and nutrient abnormalities. For the maintenance of crop productivity, improvement of the micronutrient status in plants under abiotic stress is very important. In most cases of abiotic stress, plants experience either poor or excessive availability of micronutrients, which alters their biochemical composition and minimizes growth and yield. Micronutrient availability greatly affects the ability of plants to adapt to unfavorable conditions. Essential micronutrients, such as zinc (Zn), copper (Cu), manganese (Mn), boron (B), iron (Fe), molybdenum (Mo), chloride (Cl), nickel (Ni), and cobalt (Co), have direct roles in plant metabolism. Most of these nutrients have two or more oxidation states, and therefore participate in oxidation–reduction reactions through electron transport. These elements form metalloenzymes, function as catalysts, and are vital in osmoregulation and protection against abiotic stress in plants. Micronutrients protect plants by functioning as constituents and activators of several enzymes in their defense system [such as catalase, ascarbate peroxidase, superoxide dismutase (Zn-SOD, Cu-Zn SOD, Fe-SOD, Mn-SOD)] that are involved in the detoxification of highly reactive oxygen species (ROS) produced during abiotic stress. In the present study, the role of micronutrients in the growth and metabolism of plants, as well as their support to the plants for protection, adaptation, and tolerance against abiotic stress through supporting biochemical activities, is emphasized.


Micronutrients Abiotic stress Biochemical constituents Reactive oxygen species 



The author expresses his gratitude to the late Professor C.P. Sharma, Former Head of the Department and In Charge of the ICAR Project, Department of Botany, University of Lucknow, for his invaluable suggestions and fruitful discussions during his study on plant nutrition and stress physiology. He also acknowledges the help of Ms. Isha Verma during finalizing the article.


  1. Agarwala SC, Bisht SS, Sharma CP (1991) Variable boron supply and sugarbeet metabolism. Proc Natl Acad Sci (India) 61:109–114Google Scholar
  2. Ahmed S, Evans HJ (1960) Cobalt. Soil Sci 90(3):205–210Google Scholar
  3. Alaya MB, Palmgren MG (2001) Inventory of the superfamily of P-type ion pumps in Arabidopsis. Plant Physiol 126:696–706CrossRefGoogle Scholar
  4. Alscher RG (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53(372):1331–1341PubMedCrossRefPubMedCentralGoogle Scholar
  5. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress and signal transduction. Annu Rev Plant Biol 55:373–400PubMedCrossRefPubMedCentralGoogle Scholar
  6. Asad A, Blamey FPC, Edwards DG (2003) Effects of boron foliar applications on vegetative and reproductive growth of sunflower. Ann Bot 92:565–570PubMedPubMedCentralCrossRefGoogle Scholar
  7. Asada K (1997) The role of ascorbate peroxidase and monodehydroascorbate reductase in hydrogen peroxide scavenging in plants. In: Candalios JGS (ed) Oxidation states and the molecular biology of antioxidant defenses. Cold Sring Harbor Laboratory Press, New York, pp 715–735Google Scholar
  8. Assuncão AGL, Costa Martins PDA, De Folter S, Voijs R, Schat H, Aarts MGM (2001) Elevated expression of metal transporter genes in three accessions of the metal hyperaccumulater Thalspi caerulescens. Plant Cell Environ 24:217–226CrossRefGoogle Scholar
  9. Ayala MB, Gorge JL, Lachica M, Sandmann G (1992) Changes in carotenoids and fatty acids in photosystem II of Cudeficient pea plants. Physiol Plant 84(1):1–5CrossRefGoogle Scholar
  10. Baron M, Arellano B, Lopez GJ (1995) Copper and photosystem II. A controversial relationship. Physiol Plant 94:174–180CrossRefGoogle Scholar
  11. Beak D, Cha JY, Kang S, Park B, Lee HJ, Hong H (2015) The Arabidopsis a zinc finger domain protein ARS1 is essential for seed germination and ROS homeostasis in response to ABA and oxidative stress. Front Plant Sci 6:963Google Scholar
  12. Becana M, Moran JF, Iturbe-Ormaetxe I (1998) Iron-dependent oxygen free radical generation in plants subjected to environmental stress: toxicity and antioxidant protection. Plant Soil 201(1):137–147Google Scholar
  13. Berg JM, Shi Y (1996) The galvanization of biology: a growing appreciation for the role of zinc. Science 271:1081–1085PubMedCrossRefPubMedCentralGoogle Scholar
  14. Bisht SS, Nautiyal BD, Sharma CP (2002) Zinc nutrition dependent changes in tomato (Lycopersicon esculentum) metabolism. J Plant Biol 29:159–163Google Scholar
  15. Brown PH, Bellaloui N, Hu H, Dandekar A (1999) Transgenically enhanced sorbitol synthesis facilitates phloem boron transport and increases tolerance of tobacco to boron deficiency. Plant Physiol 119:17–20PubMedPubMedCentralCrossRefGoogle Scholar
  16. Brown PH, Bellauli N, Wimmer MA, Bassil ES, Ruiz J, Hu H, Pfeffer H, Dannel F, Römheld V (2002) Boron in plant biology. Plant Biol 4:205–223CrossRefGoogle Scholar
  17. Bughio N, Yamaguchi H, Nishizawa NK, Nakanishi H, Mori S (2002) Cloning in iron regulated metal transporter from rice. J Exp Bot 53:1677–1682PubMedCrossRefPubMedCentralGoogle Scholar
  18. Burnell JN (1988) The biochemistry of manganese in plants. In: Hannam RJ, Uren NC (eds) Manganese in soil and plants (Graham RD). Kluwer Academic, Dordrecht, pp 125–137CrossRefGoogle Scholar
  19. Cakmak I, Marschner H (1988) Zinc-dependent changes in ESR signals, NADPH-oxidase and plasma membrane permeability in cotton roots. Physiol Plant 73:182–186CrossRefGoogle Scholar
  20. Cakmak I, Kurtz H, Marschner H (1995) Short-term effects of boron, germanium and high light intensity on membrane permeability in boron-deficient leaves of sunflower. Physiol Plant 95:11–18CrossRefGoogle Scholar
  21. Cakmak I (2000) Tansley review no. 111. New Phytol 146(2):185–205CrossRefGoogle Scholar
  22. Camacho-Christobal JJ, Gonzalez-Fontes A (1993) Boron deficiency causes drastic decrease in nitrate reductase activity and increases the content of carbohydrates in leaves from tobacco plants. Planta 209:528–536CrossRefGoogle Scholar
  23. Cao H, Huang P, Zhang I, Shi Y, Sun D, Yan Y (2016) Characterization of 47 Cys2–His2 zinc finger proteins required for the development and pathogenicity of the rice blast fungus Magnaporthe oryzae. New Phytol 211:1035–1051PubMedCrossRefPubMedCentralGoogle Scholar
  24. Cara FA, Sănchez E, Ruiz JM, Romero L (2002) Isophenol oxidation responsible for the short term effects of boron deficiency on plasma membrane permeability and fuction in squash roots? Plant Physiol Biochem 40:853–858CrossRefGoogle Scholar
  25. Chapple C (1998) Molecular genetic analysis of plant cytochrome P450-dependent monooxygenase. Annu Rev Plant Physiol Plant Mol Biol 49:311–343PubMedCrossRefPubMedCentralGoogle Scholar
  26. Chen Z-H, Walker RP, Acheson RM, Leegood RC (2002) Phasphophenol pyuvate carboxykinase assayed at physiological concentrations of metal ions has a high affinity for CO2. Plant Physiol 128:160–164PubMedPubMedCentralCrossRefGoogle Scholar
  27. Cowles JR, Evans HJ, Russel S (1969) B12 co-enzyme dependent ribonucleotide reductase in Rhizobium species and the effect of cobalt deficiency on the activity of enzyme. J Bacteriol 97:1460PubMedPubMedCentralGoogle Scholar
  28. Curic C, Alonso JM, Le Jean M, Ecker JR, Briat JF (2000) Involvement of NRAMPI from Arabidopsis thaliana in iron transport. Biochem J 347:749–755CrossRefGoogle Scholar
  29. D’Orso F, De Leonardis AM, Salvi S, Gadaleta A, Ruberti I, Cattivelli L (2015) Conservation of AtTZF1, AtTZF2, and AtTZF3 homolog gene regulation by salt stress in evolutionarily distant plant species. Front Plant Sci 6:394–402PubMedPubMedCentralGoogle Scholar
  30. Dannel F, Pfeffer H, Romheld V (2000) Characterization of root boron pools, boron uptake and boron translocation in sunflower using stable isotopes 10B and 11B. Aust J Plant Physiol 27:397–405Google Scholar
  31. Dilworth MJ, Robson AD, Chatel DL (1979) Cobalt and nitrogen fixation in Lupinus angustifolius L. II. Nodule formation and function. New Phytol 83:63–79CrossRefGoogle Scholar
  32. Ditch S, Paull TT (2012) The ATM protein kinase and cellular redox signaling: beyond the DNA damage response. Trend Biochem Sci 37:15–22PubMedCrossRefPubMedCentralGoogle Scholar
  33. Dixit D, Srivastava NK, Sharma S (2002) Boron deficiency induced changes in translocation of 14CO2-photosynthate into primary metabolites in relation to essential oil and curcumin accumulation in tumeric (Curcuma longa L.). Photosynthetica 40:109–113CrossRefGoogle Scholar
  34. Dordas C, Brown PH (2000) Permeability of boric acid across lipid bilayers and factors affecting it. J Membr Biol 175:95–105PubMedCrossRefPubMedCentralGoogle Scholar
  35. Eckhardt U, Margues AM, Buckhout TJ (2001) Two iron regulated cation transporters from tomato complement metal uptake deficient yeast mutants. Plant Mol Biol 45:437–448PubMedCrossRefPubMedCentralGoogle Scholar
  36. Eide D, Broderius M, Feit J, Guerinot ML (1996) A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc Natl Acad Sci U S A 93:5624–5628PubMedPubMedCentralCrossRefGoogle Scholar
  37. EL-Shintinawy F (1991) Structural and functional damage caused by boron deficiency in sunflower leaves. Photosynthetica 36:565–572CrossRefGoogle Scholar
  38. Felle HH (1994) The H+/Cl- symporter in root-hair cells of Sinapis alba (An electrophysiological study using ion-selective microelectrodes). Plant Physiol 106(3):1131–1136PubMedPubMedCentralCrossRefGoogle Scholar
  39. Feussner I, Waternack C (2002) The lipoxygenase pathway. Annu Rev Plant Biol 53:273–297CrossRefGoogle Scholar
  40. Flowers TJ (1988) Chloride as a nutrient and as an osmoticum. In: Tinker B, Läuchli A (eds) Advances in plant nutrition. Praeger, New York, pp 55–78Google Scholar
  41. Gerendas J, Sattelmacher B (1997) Significance of Ni supply for growth, urease activity and the contents of urea, amino acids and mineral nutrients of urea grown plants. Plant Soil 190:153–162CrossRefGoogle Scholar
  42. Gerendas J, Polacco JC, Freyermuth SK, Sattelmacher B (1999) Significance of nickel for plant growth and metabolism. J Plant Nutr Soil Sci 162:241–256CrossRefGoogle Scholar
  43. Gibbs J, Greenway H (2003) Mechanism of anoxia tolerance in plants. I. Growth, survival and anaerobic catabolism. Funct Plant Biol 30:1–47CrossRefGoogle Scholar
  44. Gorham J (1995) Betains in higher plants: biosynthesis and role in stress metabolism. In: Wallsgrove RM (ed) Amino acids and their derivatives in higher plants. Cambridge University Press, Cambridge, pp 171–203Google Scholar
  45. Grotz N, Fox T, Connolly E, Park W, Guerinot ML, Eide D (1998) Identification of a family of zinc transporter genes from Arabidopsis that respond to zinc deficiency. Proc Natl Acad Sci U S A 95:7220–7224PubMedPubMedCentralCrossRefGoogle Scholar
  46. Guerinot ML (2000) The ZIP family of metal transporters. Biochem Biophys Acta 1465:190–198PubMedCrossRefPubMedCentralGoogle Scholar
  47. Henriques FS (2001) Loss of blade photosnthetic area and of chloroplasts’ photochemical capacity account for reduced CO2 assimilation rates in zinc-deficient sugar beet leaves. J Plant Physiol 158(7):915–919CrossRefGoogle Scholar
  48. Henstein SM, Felle HH (2002) CO2-triggered chloride release from guard cells in intact fava bean leaves. Kinetics of the onset of stomatal closure. Plant Physiol 130:940–950CrossRefGoogle Scholar
  49. Herrmann KM, Weaver LM (1999) The shikimate pathway. Annu Rev Plant Physiol Plant Mol Biol 50:473–503PubMedCrossRefPubMedCentralGoogle Scholar
  50. Heuwinkel H, Kirkby EA, Le Bot J, Marschner H (1992) Phosphorus deficiency enhances molybdenum uptake by tomato plants. J Plant Nutr 15:549–568CrossRefGoogle Scholar
  51. Hewitt EJ, Bond G (1966) The cobalt requirement of non-legume root nodule plants. J Exp Bot 17:480–491CrossRefGoogle Scholar
  52. Hille R (1996) The mononuclear molybdenum enzymes. Chem Rev 96:2757–2816PubMedCrossRefPubMedCentralGoogle Scholar
  53. Hoganson CW, Bobcock GT (1997) A metalloradical mechanism for the generation of oxygen from water in photosynthesis. Science 277:1953–1956PubMedCrossRefPubMedCentralGoogle Scholar
  54. Hu H, Penn SG, Lebrilla CB, Brown PH (1997) Isolation and characterization of soluble boron complexes in higher plants. Plant Physiol 113:649–655PubMedPubMedCentralCrossRefGoogle Scholar
  55. Huber DM, Graham RD (1999) The role of nutrition in crop resistance and tolerance to diseases. In: Rengel Z (ed) Mineral nutrition of crops: fundamental mechanisms and implications. Haworth Press, New York, pp 169–204Google Scholar
  56. Huffman DL, O’Halloran TV (2001) Function, structure and mechanism of intracellular trafficking protiens. Annu Rev Biochem 70:677–701PubMedCrossRefPubMedCentralGoogle Scholar
  57. Jaleel CA, Riadh K, Gopi R, Manivannan P (2009) Antioxidant defense responses: physiological plasticity in higher plants under abiotic constraints. Acta Physiol Plant 31:427–436CrossRefGoogle Scholar
  58. Johnson DC, Dean DR, Smith AD, Johnson MK (2005) Structure, Function, and formation of biological iron-sulfur clusters. Annu Rev Biochem 74(1):247–281PubMedCrossRefPubMedCentralGoogle Scholar
  59. Johnson GV, Mayeux PA, Evans HJ (1996) A cobalt reqiurement for symbiotic growth of Azolla filiculoides in the absence of combined nitrogen. Plant Physiol 41:852–855CrossRefGoogle Scholar
  60. Jordan A, Reichard P (1998) Ribonucleotide reductases. Annu Rev Biochem 67:71–98PubMedCrossRefPubMedCentralGoogle Scholar
  61. Kaiser WH, Weiner H, Kandlbinder A, Tsai C-B, Roctul P, Sonoda M, Planchet E (2002) Modulation of nitrate reductase: some new insights. An unusual case and a potentially important side reaction. J Exp Bot 53:875–882PubMedCrossRefPubMedCentralGoogle Scholar
  62. Kannaujia PK, Pandey SN (2013) Effect of zinc-stresses in alluvial soil on growth and yield of wheat. J Biol Chem Res 30:892–900Google Scholar
  63. Kastori R, Plesnicar M, Pankoic D, Sakae Z (1995) Photosynthesis, chlorophyll fluorescence and soluble carbohydrates in sunflower leaves as affected by boron deficiency. J Plant Nutr 18:1751–1763CrossRefGoogle Scholar
  64. Kobayashi M, Mutosh T, Matoh T (2004) Boron nutrition of cultured tobacco BY-2 cells. IV. Genes induced under low boron supply. J Exp Bot 55:1441–1443PubMedPubMedCentralCrossRefGoogle Scholar
  65. Koshiba T, Saito H, Ono N, Yamarnoto N, Sato M (1996) Purification and properties of flavin-and molybdenum containing aldehyde oxidase from coleoptile of maize. Plant Biol 110:781–789Google Scholar
  66. Lindsay CO, Rodrigues L, Pasternak CA (1989) Protection of cells against membrane damage by haemolytic agents: divalent cations and protons act at the extracellular side of the plasma membrane. Biophys Acta 983:56–64CrossRefGoogle Scholar
  67. Llamas A, Kalakontskii KL, Fernandez E (2000) Molybdenum cofactor amounts in Chlamydomonas reinhardtii depend on the Nit 5 gene function related to molybdate transport. Plant Cell Environ 23:1247–1255CrossRefGoogle Scholar
  68. Lohaus G, Hussmann PK, Pennewiss K, Schneider H, Zhu JJ, Sattlemacher B (2000) Solute balance of a maize (Zea mays) source leaf as affected by salt treatment with special emphasis on phloem retranslocation and ion leaching. J Exp Bot 51:1721–1732PubMedCrossRefPubMedCentralGoogle Scholar
  69. Loneragen JF (1981) Distribution and movement of copper in plants. In: Loneragan JF, Robson AD, Graham RD (eds) Copper in soils and plants. Academic Press, London, pp 165–188Google Scholar
  70. Loomis WD, Durst RW (1991) Boron and cell walls. Curr Top Plant Biochem Physiol 10:149–178Google Scholar
  71. Lorenzen I, Aberle T, Plieth C (2004) Salt stress induced chloride flux: a study using transgenic Arabidopsis expressing a fluorescent anion probe. Plant J 38:538–544CrossRefGoogle Scholar
  72. Ma D, Sun D, Wang C, Ding H, Qin H, Hou J, Huang X, Xie Y, Guo T (2017) Physiological responses and yield of wheat plants in zinc-mediated alleviation of drought stress. Front Plant Sci 8:860. CrossRefPubMedPubMedCentralGoogle Scholar
  73. Maksymiec W (1997) Effect of copper on cellular processes in higher plants. Photosynthesis 34:321–342CrossRefGoogle Scholar
  74. Marschner H (1995) Mineral nutrition of higher plants. Academic Press, LondonGoogle Scholar
  75. Mehdy MC (1994) Active oxygen species in plant defense against pathogen. Plant Physiol 105:467–472PubMedPubMedCentralCrossRefGoogle Scholar
  76. Mendel RR, Hansch R (2002) Molybdoenzymes and molybdenum cofactor in plants. J Exp Bot 53:1689–1698PubMedCrossRefPubMedCentralGoogle Scholar
  77. Miyake C, Cao W-H, Asada K (1993) Purification and molecular properties of the thylakoid-bound ascorbate peroxidase in spinach chloroplasts. Plant Cell Physiol 34:881–889Google Scholar
  78. Moreau S, Thomson RM, Kaiser BN, Trevaskis B, Guerinot ML, Udvardi MK, Puppo A, Day DA (2002) Gm ZIP1 encodes a symbiosis-specific zinc transporter in soyabean. J Biol Chem 277:4738–4746PubMedCrossRefPubMedCentralGoogle Scholar
  79. Moya JL, Primo-Millo E, Talon M (1999) Morphological factors determining salt tolerance in citrus seedlings: the shoot to root ratio modulates passive root uptake of chloride ions and their accumulation in leaves. Plant Cell Environ 22:1425CrossRefGoogle Scholar
  80. Nautiyal N, Chatterjee C (1999) Role of copper in improving the seed quality of sunflower (Helianthus annuus). Indian J Agric Sci 69:210–213Google Scholar
  81. Nautiyal N, Chatterjee C, Sharma CP (1999) Copper stress affects grain filling in rice. Common Soil Sci Plant Anal 30:1625–1632CrossRefGoogle Scholar
  82. O’halloran TV, Culotta VC (2000) Metallo-chaperones, an intracellular shuttle service for metals ions. J Biol Chem 275:25057–25060PubMedCrossRefPubMedCentralGoogle Scholar
  83. O’Neill MA, Eberhard S, Albersheim P, Darvell AG (2001) Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsis growth. Science 294:846–849PubMedCrossRefPubMedCentralGoogle Scholar
  84. O’Neill MA, Ishii T, Albushein P, Darvill AG (2004) Rhamnogalacturonan II: structure and function of a borate cross-linked cell wall pectic polysaccharide. Annu Rev Plant Biol 55:109–139PubMedCrossRefPubMedCentralGoogle Scholar
  85. Ono T, Onone Y (1991) A possible role of redox active histidine in the photoligation of manganese into photosynthetic O2 evolving enzyme. Biochemistry 30:6183–6188PubMedCrossRefPubMedCentralGoogle Scholar
  86. Orozco-Cardenas ML (2001) Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell Online 13(1):179–191CrossRefGoogle Scholar
  87. Pandey SN (2006) Accumulation of heavy metals (Cd, Cr, Cu, Ni and Zn) in Raphanus sativus L. and Spinacia oleracea L. plants irrigated with industrial effluent. J Environ Biol 27:381–384PubMedPubMedCentralGoogle Scholar
  88. Pandey SN (2014) Effect of soil sodicity on growth, biochemical constituents and zinc content in wheat plants. J Biol Chem Res 31:317–324Google Scholar
  89. Pandey SN, Verma P (2010) Effects on growth, nodulation and some physiological attributes of legumes with cobalt supply. J Eco-Friendly Agric 5:21–24Google Scholar
  90. Pandey N, Pathak GC, Singh AK, Sharma CP (2002) Enzymic changes in response to zinc nutrition. J Plant Physiol 151:1151–1153CrossRefGoogle Scholar
  91. Pandey SN, Naaz S, Ansari SR (2009) Growth, biomass and petroleum convertible hydrocarbons yield of Grindelia camporum planted on an alluvial soil (Entisol) of North India and its response to sulfur fertilization. Biomass Bioenergy 33:454–458CrossRefGoogle Scholar
  92. Pfeffer H, Dannel F, Romheld V (1999) Are there two mechanisms for boron uptake in sunflower. J Plant Physiol 155:34–40CrossRefGoogle Scholar
  93. Prescott AG, John P (1996) Dioxygenases: molecular structure and role in plant metabolism. Annu Rev Plant Mol Biol 47:245–271CrossRefGoogle Scholar
  94. Ravichandran V, Pathmanabhan G (2004) Studies of nodulation and ethanol producing enzymes in copper under flood stress regime. J Plant Biol 33:75–80Google Scholar
  95. Rabotti G, Zocchi G (1994) Plasma membrane bound H+-ATPase and reductase activities in Fe-deficient cucumber roots. Physiol Plant 90:779–785CrossRefGoogle Scholar
  96. Rockel P, Strube F, Rockel A, Wildt J, Kaiser WM (2002) Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and invitro. J Exp Bot 53:103–110PubMedCrossRefPubMedCentralGoogle Scholar
  97. Romao MJ, Archer M, Maura JJG, Le Gall J, Engh R, Schveider M, Holf P, Huber R (1995) Crystal structure of the xanthione oxidase-related aldehyde oxido-reductase from D. gigas. Science 270:1170–1176PubMedCrossRefPubMedCentralGoogle Scholar
  98. Romero P, Botia P, Keller M (2017) Hydraulics and gas exchange recover more rapidaly from severe drought stress in small pot-grown grapevines than in field grown plants. J Plant Physiol 216:58–73PubMedCrossRefPubMedCentralGoogle Scholar
  99. Sancenon V, Puigs S, Mira H, Thiele DJ, Peoarrubi L (2003) Identification of a copper transporter family in Arabidopsis thaliana. Plant Mol Biol 51:577–587PubMedCrossRefPubMedCentralGoogle Scholar
  100. Schomburg FM, Bizzell CM, Lee DJ, Zeevaort JAD, Amasino RM (2002) Over expression of a novel class of gibberellin 2-oxidases decreases gibberellin levels and creates dwarf plants. Plant Cell 15:151–163CrossRefGoogle Scholar
  101. Sharma CP (2006) Plant micronutrients. Science Publishers, EnfieldCrossRefGoogle Scholar
  102. Shrotri CK, Tewari MN, Rathore VS (1978) Morphological and ultrastructural abnormalities in zinc deficient maize chloroplasts. Plant Biochem J 5:89–96Google Scholar
  103. Sigel A, Sigel H (2002) Molybdenum and tungsten. Their roles in biological processes. Metal ions in biological systems. Marcel Dekker, New YorkGoogle Scholar
  104. Singh K, Pandey SN, Mishra A (2015) Preference of heavy metals accumulation, tolerance limit and biochemical responses of Eichhornia crassipes (Mart.) exposed to industrial waste water. Int J Curr Res 7:11818–11822Google Scholar
  105. Skerrett M, Tyerman SD (1994) A channel that allows inwardly directed fluxes of anions in protoplast derived from wheat roots. Planta 192:295–305CrossRefGoogle Scholar
  106. Slooten L, Capiau K, Van Camp W, Van Montagn M, Sybesma C, Inze D (1995) Factors affecting the enhancement of oxidative stress tolerance in transgenic tobacco over expressing manganese superoxide dismutase in the chloroplasts. Plant Physiol 107:735–750CrossRefGoogle Scholar
  107. Stiefel EI (1996) Molybdenum bolsters the bioinorganic brigade. Science 272(5268):1599–1600PubMedCrossRefPubMedCentralGoogle Scholar
  108. Storey R (1995) Salt tolerance, ion relations and the effect of root medium on the response of citrus to salinity. Aust J Plant Physiol 22:101–114CrossRefGoogle Scholar
  109. Sun T-P, Gubler F (2004) Molecular mechanism of gibberellin signalling in plants. Annu Rev Plant Biol 55:197–224PubMedCrossRefPubMedCentralGoogle Scholar
  110. Taylor IB (1991) Genetics of ABA synthesis. In: Davis WJ, Jones HG (eds) Abscisic acid, physiology and biochemistry. Bios Publishers, Oxford, pp 23–37Google Scholar
  111. Thomine S, Lelievre F, Debarbieux E, Schroeder JL, Barbier-Brygoo H (2003) At NRAMP 3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency. Plant J 34:685–695PubMedCrossRefPubMedCentralGoogle Scholar
  112. Upadhyay A, Tripathi S, Pandey SN (2013) Effects of soil sodicity on growth, nutrients uptake and biochemical responses of Ammi majus L. Res J Soil Biol 4:69–80CrossRefGoogle Scholar
  113. Van der Zaal BJ, Neuteboom LW, Pinas JE, Charonnens AN, Schat H, Verkeij JAC, Hooykaas PJJ (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 119:1047–1055PubMedPubMedCentralCrossRefGoogle Scholar
  114. Verma AK, Singh RB, Pandey SN (2014) Bioaccumulation of heavy metals (Zn, Cu, Fe, Cd, Ni and Cr) and biochemical responses of wild plants near express highway (NH 25) in Unnao district, Uttar Pradesh state (India). J Biol Chem Res 31:777–787Google Scholar
  115. Vert G, Grotz N, Dedaldechamp F, Gaymard F, Guerinot ML, Briat J-F, Curie C (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14:1223–1233PubMedPubMedCentralCrossRefGoogle Scholar
  116. Waters BM, Blevins DG, Eide DJ (2002) Characterization of FRON1, a pea ferric chelate reductase involved in root iron acquisition. Plant Physiol 129:85–94PubMedPubMedCentralCrossRefGoogle Scholar
  117. White MC, Deeker AM, Chaney RI (1981) Metal complexation in xylem fluid. I. Chemical composition of tomato and soyabean root exudate. Plant Physiol 67:301–310PubMedPubMedCentralCrossRefGoogle Scholar
  118. White PJ, Broadley MR (2001) Chloride in soils and its uptake and movement within the plant: a review. Ann Bot 88(6):967–988CrossRefGoogle Scholar
  119. Wu G, Wilen RW, Robertson AJ, Gusta LV (1999) Isolation, chromosomal localization and differential expression of mitochondrial manganese superoxide dismutase and chloroplastic copper/zinc superoxide disutase genes in wheat. Plant Physiol 120:513–520PubMedPubMedCentralCrossRefGoogle Scholar
  120. Wu Z, Liang F, Hony B, Yaung JC, Sussman MR, Harper JF, Sze H (2002) An endoplasmic reticulum-bound Ca+/Mn2+ pump, ECA1, supports plant growth and confers tolerance to Mn2+stress. Plant Physiol 130:128–137PubMedPubMedCentralCrossRefGoogle Scholar
  121. Xu G, Magen H, Tarchitzky J, Kafkafi U (2000) Advance in chloride nutrition. Adv Agron 66:96–150Google Scholar
  122. Yu Q, Hlavacka A, Matoh T, Volkmann D, Menzel D, Goldbach HE, Baluska F (2003) Short term boron deprivation inhibits endocytosis of wall pectins in meristematic cells of maize and wheat root apics. Plant Physiol 130:415–421CrossRefGoogle Scholar

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© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Shyam N. Pandey
    • 1
  1. 1.Department of BotanyUniversity of LucknowLucknowIndia

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