Skip to main content
SpringerLink
Log in

Evaluating the Importance of Proline in Cadmium Tolerance and Its Interaction with Phytohormones

  • Chapter
Osmolytes and Plants Acclimation to Changing Environment: Emerging Omics Technologies

Abstract

Cadmium (Cd) stress is one of the most challenging environmental problems that adversely affects growth and development of plants. Plants adopt various strategies to overcome the adverse effects of Cd stress. Among these, recently phytohormones and osmolytes have been involved in overcoming the adverse effects of Cd stress. Proline is an important osmolyte that maintains cellular homeostasis through osmotic regulation and regulates physiological processes under Cd stress. The role of phytohormones under Cd stress is critical in modulating physiological responses that eventually leads to adaptation of plants to an unfavorable environment. The individual role of both proline and phytohormones has been extensively studied, but a comprehensive study on the interaction of phytohormones with proline under Cd is lacking. The present study focuses on enhancing our understanding on the mechanism of Cd tolerance via proline and phytohormones with emphasis on phytohormones’ interaction with proline under Cd stress.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abdelhamid MT, Rady M, Osman A, Abdalla MA (2013) Exogenous application of proline alleviates salt-induced oxidative stress in Phaseolus vulgaris L. plants. J Hort Sci Biotechnol 88:439–446

    CAS  Google Scholar 

  • Ahammed GJ, Choudhary SP, Chen S, Xia X et al (2013) Role of brassinosteroids in alleviation of phenanthrene-cadmium co contamination-induced N photosynthetic inhibition and oxidative stress in tomato. J Exp Bot 64:199–213

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ahmad P, Sarwat M, Bhat NA, Wani MR, Kazi AG, Tran LSP (2015) Alleviation of cadmium toxicity in Brassica juncea L. (Czern. & Coss.) by calcium application involves various physiological and biochemical strategies. PLoS One 10, e0114571

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ali E, Modzeka A, Hussain N, Shamsi IH, Jiang L (2015) The alleviation of cadmium toxicity in oilseed rape (Brassica napus) by the application of salicylic acid. Plant Growth Regul 75:641–655

    Article  CAS  Google Scholar 

  • Al-Whaibi MH, Siddiqui MH, Basalah MO (2012) Salicylic acid and calcium induced protection of wheat against salinity. Protoplasma 249:769–778

    Article  CAS  PubMed  Google Scholar 

  • Aly AA (2012) Application of DNA [RAPD] and ultrastructure to detect the effect of cadmium stress in Egyptian clover and Sudan grass plantlets. J Stress Physiol Biochem 8:241–257

    Google Scholar 

  • Amuthavalli P, Anbu D, Sivasankaramoorthy S (2012) Effect of calcium chloride on growth and biochemical constituents of cotton (Gossypium hirsutum L.) under salt stress. Int J Res Bot 2:9–12

    Google Scholar 

  • Anjum NA, Gill SS, Umar S, Ahmad I, Duarte AC, Pereira E (2012) Improving growth and productivity of Oleiferous Brassicas under changing environment: significance of nitrogen and sulphur nutrition, and underlying mechanisms. Sci World J 2012:657808

    Article  CAS  Google Scholar 

  • Anjum NA, Aref IM, Duarte AC, Pereira E, Ahmad I, Iqbal M (2014) Glutathione and proline can coordinately make plants withstand the joint attack of metal(loid) and salinity stresses. Front Plant Sci 5:Article 662 | 1–4

    Google Scholar 

  • Antosiewicz DM, Hennig J (2004) Overexpression of LCT1 in tobacco enhances the protective action of calcium against cadmium toxicity. Environ Poll 129:237–245

    Article  CAS  Google Scholar 

  • Anuradha A, Rao SSR (2007) The effect of brassinosteroids on radish (Raphanus sativus L.) seedlings growing under cadmium stress. plant. Soil Environ 53:465–472

    CAS  Google Scholar 

  • Asgher M, Khan MIR, Iqbal N, Masood A, Khan NA (2013) Cadmium tolerance in mustard cultivars: dependence on proline accumulation and nitrogen assimilation. J Funct Environ Bot 3:30–42

    Article  Google Scholar 

  • Asgher M, Khan NA, Khan MIR, Fatma M, Masood A (2014) Ethylene production is associated with alleviation of cadmium-induced oxidative stress by sulfur in mustard types differing in ethylene sensitivity. Ecotoxicol Environ Saf 106:54–61

    Article  CAS  PubMed  Google Scholar 

  • Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216

    Article  CAS  Google Scholar 

  • Aspinall D, Paleg LG (1981) Proline accumulation: biochemical aspects. In: Paleg LG, Aspinall D (eds) The physiology and biochemistry of drought resistance in plants. Academic, Sydney, pp 243–259

    Google Scholar 

  • Badr-uz-Zaman, Salim M, Asghar R (2010) Role of Ca2+ on growth of Brassica campestris L. and B. juncea (L.) Czern & Coss under Na+ stress. J Integ Plant Biol 52:549–555

    Article  CAS  Google Scholar 

  • Bahmani R, Bihamta MR, Habibi D, Forozesh P, Ahmadvand S (2012) The effect of cadmium stress on growth, SOD activity, proline and ABA content in bean seedlings (Phaseolus vulgaris L.). The 1st international and the 4th National Congress on Recycling of Organic Waste in Agriculture 26–27 April 2012 in Isfahan, Iran

    Google Scholar 

  • Bai XY, Dong YJ, Xu LL, Kong J, Liu S (2015) Effects of exogenous nitric oxide on physiological characteristics of perennial ryegrass under cadmium and copper stress. Russ J Plant Physiol 62:237–245

    Article  CAS  Google Scholar 

  • Bajguz A (2000) Effect of brassinosteroids on nucleic acids and protein content in cultured cells of Chlorella vulgaris. Plant Physiol Biochem 38:209–215

    Article  CAS  Google Scholar 

  • Balestrasse KB, Gallego SM, Benavides MP, Tomaro ML (2005) Polyamines and proline are affected by cadmium stress in nodules and roots of soybean plants. Plant Soil 270:343–353

    Article  CAS  Google Scholar 

  • Bartha B, Kolbert Z, Erdei L (2005) Nitric oxide production induced by heavy metals in Brassica juncea L. Czern. and Pisum sativum L. Acta Biol Szeged 49:9–12

    Google Scholar 

  • Basalah MO, Ali HM, Al-Whaibi MH, Siddiqui MH, Sakran AM, Al Sahl AA (2013) Nitric oxide and salicylic acid mitigate cadmium stress in wheat seedlings. J Pure Appl Microbiol 7:139–148

    CAS  Google Scholar 

  • Battal P, Turker M, Tileklioglu B (2003) Effects of different mineral nutrients on abscisic acid in maize (Zea mays). Ann Bot Fenn 40:301–308

    CAS  Google Scholar 

  • Bender KW, Dobney S, Ogunrinde A, Chiasson D, Mullen RT, Teresinski HJ, Singh P, Munro K, Smith SP, Snedden WA (2014) The calmodulin-like protein CML43 functions as a salicylic-acid-inducible root-specific Ca2+ sensor in Arabidopsis. Biochem J 457:127–136

    Article  CAS  PubMed  Google Scholar 

  • Besson-Bard A, Pugin A, Wendehenne D (2008) New insights into nitric oxide signaling in plants. Annu Rev Plant Biol 59:21–39

    Article  CAS  PubMed  Google Scholar 

  • Besson-Bard A, Gravot A, Richaud P, Auroy P, Duc C, Gaymard F, Taconnat L, Renou JP, Pugin A, Wendehenne D (2009) Nitric oxide contributes to cadmium toxicity in Arabidopsis by promoting cadmium accumulation in roots and by up-regulating genes related to iron uptake. Plant Physiol 149:1302–1315

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bohnert HJ, Nelson DE, Jensen RG (1995) Adaption to environmental stress. Plant Cell 7:1099–1111

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bouchereau A, Aziz A, Larher F, Martin-Tanguy J (1999) Polyamines and environmental challenges: recent development. Plant Sci 140:103–125

    Article  CAS  Google Scholar 

  • Braam J (1992) Regulated expression of the calmodulin-related TCH genes in cultured Arabidopsis cells: induction by calcium and heat shock. Proc Natl Acad Sci 89:3213–3216

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Çanakci S, Dursun B (2013) Amelioration of Cd toxicity by pretreatment of salicylic acid in Cicer arietinum L. seedlings. J Environ Biol 34:1089–1094

    PubMed  Google Scholar 

  • Cao S, Chen Z, Liu G, Jiang L, Yuan H, Ren G, Bian X, Jian H, Ma X (2009) The Arabidopsis ethylene-insensitive 2 gene is required for lead resistance. Plant Physiol Biochem 47:308–312

    Article  CAS  PubMed  Google Scholar 

  • Cao MJ, Wang Z, Zhao Q, Mao JL, Speiser A, Wirtz M, Hell R, Zhu JK, Xiang CB (2014) Sulfate availability affects ABA levels and germination response to ABA and salt stress in Arabidopsis thaliana. Plant J 77:604–615

    Article  CAS  PubMed  Google Scholar 

  • Celik I, Tuluce Y, Isik I (2007) Evaluation of toxicity of abscisic acid and gibberellic acid in rats: 50 days drinking water study. J Enzym Inhib Med Chem 22:219–226

    Article  CAS  Google Scholar 

  • Chaffei C, Pageau K, Suzuki A, Gouia H, Brulfert J, Ghorbal MH, Daubresse CM (2004) Cadmium toxicity induced changes in nitrogen management in Lycopersicon esculentum leading to a metabolic safeguard through an amino acid storage strategy. Plant Cell Physiol 45:1681–1693

    Article  CAS  PubMed  Google Scholar 

  • Chao YY, Chen CY, Huang WD, Ching CH (2010) Salicylic acid mediated hydrogen peroxide accumulation and protection against Cd toxicity in rice leaves. Plant Soil 329:327–337

    Article  CAS  Google Scholar 

  • Chen C, Dickman MB (2005) Proline suppresses apoptosis in the fungal pathogen Colletotrichum trifolii. Proc Natl Acad Sci USA 102:3459–3464

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chen CT, Chen LM, Lin CC, Kao HC (2001) Regulation of proline accumulation in detached rice leaves exposed to excess copper. Plant Sci 160:283–290

    Article  CAS  PubMed  Google Scholar 

  • Chmielowska-Bąak J, Lefèvre I, Lutts S, Deckert J (2013) Short term signaling responses in roots of young soybean seedlings exposed to cadmium stress. J Plant Physiol 170:1585–1594

    Article  CAS  Google Scholar 

  • Choudhary M, Jetley UK, Khan MA, Zutshi S, Fatma T (2007) Effect of heavy metal stress on proline, malondialdehyde, and superoxide dismutase activity in the cyanobacterium Spirulina platensis S5. Ecotox Environ Safet 66:204–209

    Article  CAS  Google Scholar 

  • Clemens S, Antosiewicz DM, Ward JM, Schachtman DP, Schroeder JI (1998) The plant cDNA LCT1 mediates the uptake of calcium and cadmium in yeast. Proc Natl Acad Sci U S A 95:12043

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Considine MJ, Foyer CH (2014) Redox regulation of plant development. Antioxid Redox Signal 21:1305–1326

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dalio RJD, Pinheiro HP, Sodek L, Haddad CRB (2013) 24-epibrassinolide restores nitrogen metabolism of pigeon pea under saline stress. Bot Stud 54:9

    Article  CAS  Google Scholar 

  • De Grauwe L, Dugardeyn J, Van Der Straeten D (2008) Novel mechanisms of ethylene-gibberellin crosstalk revealed by the gai eto2-1 double mutant. Plant Signal Behav 3:1113–1115

    Article  PubMed Central  PubMed  Google Scholar 

  • De Michele R, Vurro E, Rigo C, Costa A, Elviri L, di Valentin M, Careri M, Zottini M, di Toppi LS, Schiavo FL (2009) Nitric oxide is involved in cadmium-induced programmed cell death in Arabidopsis suspension cultures. Plant Physiol 150:217–228

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Demiral T, Türkan I (2004) Does exogenous glycinebetaine affect antioxidative system of rice seedlings under NaCl treatment? J Plant Physiol 161:1089–1100

    Article  CAS  PubMed  Google Scholar 

  • Du S, Zhang Y, Lin XY, Wang Y, Tang CX (2008) Regulation of nitrate reductase by nitric oxide in Chinese cabbage pakchoi (Brassica chinensis L.). Plant Cell Environ 31:195–204

    CAS  PubMed  Google Scholar 

  • Dugardeyn J, Vandenbussche F, Van Der Straeten D (2008) To grow or not to grow: what can we learn on ethylene-gibberellin cross-talk by in silico gene expression analysis? J Exp Bot 59:1–16

    Article  CAS  PubMed  Google Scholar 

  • El-Enany AE, Issa AA (2001) Proline alleviates heavy metal stress in Scenedesmus armatus. Foliar Microbiol 46:227–230

    Article  CAS  Google Scholar 

  • El-Hamid A, Nabrawy MF, Amera A, Gaber AA, Amal MK (2003) Control the physiological stress resulted from Cd and Pb foliage application on sugar beet plant by using foliar spray with certain growth regulators. J Agric Sci 28:3571–3602

    Google Scholar 

  • Fan HF, Du CX, Guo SR (2012) Effect of nitric oxide on proline metabolism in cucumber seedlings under salinity stress. J Am Soc Hort Sci 137:127–133

    CAS  Google Scholar 

  • Fan SK, Fang XZ, Guan MY, Ye YQ, Lin XY, Du ST, Jin CW (2014) Exogenous abscisic acid application decreases cadmium accumulation in Arabidopsis plants, which is associated with the inhibition of IRT1-mediated cadmium uptake. Front Plant Sci 5:Article 721 | 1

    Google Scholar 

  • Fediuc E, Lips SH, Erdei L (2005) O-Acetylserine (thiol) lyase activity in Phragmites and Typha plants under cadmium and NaCl stress conditions and the involvement of ABA in the stress response. J Plant Physiol 162:865–872

    Article  CAS  PubMed  Google Scholar 

  • Filippou P, Antoniou C, Fotopoulos V (2013) The nitric oxide donor sodium nitroprusside regulates polyamine and proline metabolism in leaves of Medicago truncatula plants. Free Rad Biol Med 56:172–183

    Article  CAS  PubMed  Google Scholar 

  • Finkemeier I, Kluge C, Metwally A, Georgi M, Grotjohann N, Dietz KJ (2003) Alterations in Cd-induced gene expression under nitrogen deficiency in Hordeum vulgare. Plant Cell Environ 26:821–833

    Article  CAS  PubMed  Google Scholar 

  • Fismes J, Vong PC, Guckert A, Frossard E (2000) Influence of sulfur on apparent N-use efficiency, yield and quality of oilseed rape (Brassica napus L.) grown on a calcareous soil. Eur J Agron 12:127–141

    Article  CAS  Google Scholar 

  • Foy CD (1998) Plant adaptation to acid, aluminum-toxic soils. Comm Soil Sci Plant Anal 19:959–987

    Article  Google Scholar 

  • Fuchs Y, Lieberman M (1968) Effects of kinetin, IAA and gibberellin on ethylene production and their interactions in growth of seedlings. Plant Physiol 43:2029–2036

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Garcia-Mata C, Gay R, Sokolovski S, Hills A, Lamattina L, Blatt MR (2003) Nitric oxide regulated K+ and Cl− channels in guard cells through a subset of abscisic acid-evoked signaling pathways. Proc Natl Acad Sci U S A 100:11116–11121

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Garg SK (2013) Role and hormonal regulation of nitrate reductase activity in higher plants: a review. Plant Sci Feed 3:13–20

    Google Scholar 

  • Gavelienė V, Pakalniškytė L, Novickienė L (2014) Regulation of proline and ethylene levels in rape seedlings for freezing tolerance. Cent Eur J Biol 9:1099–1107

    Google Scholar 

  • Ghorbanli M, Hadade-Kaveh SH, Sepehr MF (1999) Effects of cadmium and gibberellin on growth and photosynthesis of Glycin max L. Photosynthetica 37:627–631

    Article  CAS  Google Scholar 

  • Gilroy S, Jones RL (1992) Gibberellic acid and abscisic acid coordinately regulated cytoplasmic calcium and secretory activity in barley aleurone protoplasts. Proc Natl Acad Sci 89:3591–3595

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gojon A, Gaymard F (2010) Keeping nitrate in the roots: an unexpected requirement for cadmium tolerance in plants. J Mol Cell Biol 2:299–301

    Article  CAS  PubMed  Google Scholar 

  • Gómez-Jiménez MC, Matilla AJ, Garrido D (1998) Isolation and characterization of a cDNA encoding an ACC oxidase from Cicer arietinum and its expression during embryogenesis and seed germination. Aust J Plant Physiol 25:765–773

    Article  Google Scholar 

  • Grabov A, Blatt MR (1998) Membrane voltage initiates Ca2+ waves and potentiates Ca2+ increases with abscisic acid in stomatal guard cells. Proc Natl Acad Sci U S A 95:4778–4783

    Google Scholar 

  • Gratão PL, Monteiro CC, Carvalho RF, Tezotto T, Piotto FA, Peres LEP, Azevedo RA (2012) Biochemical dissection of diageotropica and never ripe tomato mutants to Cd-stressful conditions. Plant Physiol Biochem 56:79–96

    Article  PubMed  CAS  Google Scholar 

  • Groppa D, Rosales EP, Iannone MF, Benavides MP (2008) Nitric oxide, polyamines and Cd-induced phytotoxicity in wheat roots. Phytochemistry 69:2609–2615

    Article  CAS  PubMed  Google Scholar 

  • Guo X, Ma YY, Liu ZH, Liu BH (2008) Effects of exterior abscisic acid on calcium distribution of mesophyll cells and calcium concentration of guard cells in maize seedlings. Agric Sci China 7:438–446

    Article  CAS  Google Scholar 

  • Guo B, Liang Y, Zhu Y (2009) Does salicylic acid regulate antioxidant defense system cell death, cadmium uptake and partitioning to acquire cadmium tolerance in rice? J Plant Physiol 166:20–31

    Article  CAS  PubMed  Google Scholar 

  • Guo H, Zhu N, Deyholos MK, Liu J, Zhang X, Dong J (2015) Calcium mobilization in salicylic acid-induced Salvia miltiorrhiza cell cultures and its effect on the accumulation of rosmarinic acid. Appl Biochem Biotechnol 175:2689–2702

    Article  CAS  PubMed  Google Scholar 

  • Hare PD, Cress WA, Van Staden J (1999) Proline synthesis and degradation: a model system for elucidating stress-related signal transduction. J Exp Bot 50:413–434

    CAS  Google Scholar 

  • Hasan SA, Fariduddin Q, Ali B, Hayat S, Ahmad A (2009) Cadmium: toxicity and tolerance in plants. J Environ Biol 30:165–174

    CAS  PubMed  Google Scholar 

  • Hassan MJ, Wang F, Ali S, Zhang GP (2005) Toxic effect of cadmium on rice as affected by nitrogen fertilizer form. Plant Soil 277:359–365

    Article  CAS  Google Scholar 

  • Hayat S, Hasan SA, Hayat Q, Ahmad A (2010) Brassinosteroids protect Lycopersicon esculentum from cadmium toxicity applied as shotgun approach. Protoplasma 239:3–14

    Article  CAS  PubMed  Google Scholar 

  • Hayat Q, Hayat S, Alyemenia MN, Ahmad A (2012) Salicylic acid mediated changes in growth, photosynthesis, nitrogen metabolism and antioxidant defense system in Cicer arietinum L. Plant Soil Environ 58:417–423

    CAS  Google Scholar 

  • Hayat S, Hayat Q, Alyemenia MN, Ahmad A (2013) Proline enhances antioxidative enzyme activity, photosynthesis and yield of Cicer arietinum L. exposed to cadmium stress. Acta Bot Croat 72:323–335

    CAS  Google Scholar 

  • Hayat S, Hayat Q, Alyemenia MN, Ahmad A (2014) Salicylic acid enhances the efficiency of nitrogen fixation and assimilation in Cicer arietinum plants grown under cadmium stress. J Plant Interac 9:35–42

    Article  CAS  Google Scholar 

  • He J, Ren Y, Chen X, Chen H (2014) Protective roles of nitric oxide on seed germination and seedling growth of rice (Oryza sativa L.) under cadmium stress. Ecotoxicol Environ Saf 108:114–119

    Article  CAS  PubMed  Google Scholar 

  • Hollenbach B, Schreiber L, Hartung W, Dietz KJ (1997) Cadmium tends to stimulate expression of lipid transfer protein (ltp) in barley: implications for the involvement of LTP in wax assembly. Planta 203:9–19

    Article  CAS  PubMed  Google Scholar 

  • Hoque MA, Banu MN, Okuma E, Amako K, Nakamura Y, Shimoishi Y, Murata Y (2007) Exogenous proline and glycinebetaine increase NaCl-induced ascorbate glutathione cycle enzyme activities, and proline improves salt tolerance more than glycinebetaine in tobacco Bright Yellow-2 suspension-cultured cells. J Plant Physiol 164:1457–1468

    Article  CAS  PubMed  Google Scholar 

  • Hsu YT, Kao CH (2003) Accumulation of ammonium ion in cadmium tolerant and sensitive cultivars of Oryza sativa. Plant Growth Regul 39:271–276

    Article  CAS  Google Scholar 

  • Hsu YT, Kao CH (2004) Cadmium toxicity is reduced by nitric oxide in rice leaves. Plant Growth Regul 42:227–238

    Article  CAS  Google Scholar 

  • Iakimova ET, Woltering EJ, Kapchina-Toteva VM, Frans JM, Harren C, Simona MC (2008) Cadmium toxicity in cultured tomato cells – role of ethylene, proteases and oxidative stress in cell death signaling. Cell Biol Int 32:1521–1529

    Article  CAS  PubMed  Google Scholar 

  • Iqbal N, Nazar R, Syeed S, Masood A, Khan NA (2011) Exogenously-sourced ethylene increases stomatal conductance, photosynthesis, and growth under optimal and deficient nitrogen fertilization in mustard. J Exp Bot 62:4955–4963

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Iqbal N, Khan NA, Nazar R, Silva JA (2012) Ethylene-stimulated photosynthesis results from increased nitrogen and sulfur assimilation in mustard types that differ in photosynthetic capacity. Environ Exp Bot 78:84–90

    Article  CAS  Google Scholar 

  • Iqbal N, Trivellini A, Masood A, Ferrante A, Khan NA (2013) Current understanding on ethylene signaling in plants: the influence of nutrient availability. Plant Physiol Biochem 73:128–138

    Article  CAS  PubMed  Google Scholar 

  • Iqbal N, Umar S, Khan NA, Khan MIR (2014) A new perspective of phytohormones in salinity tolerance: regulation of proline metabolism. Environ Exp Bot 100:34–42

    Article  CAS  Google Scholar 

  • Iqbal N, Umar S, Khan NA (2015) Nitrogen availability regulates proline and ethylene production and alleviates salinity stress in mustard (Brassica juncea). J Plant Physiol 178:84–91

    Article  CAS  PubMed  Google Scholar 

  • Islam MM, Hoque MA, Okuma E, Banu MNA, Shimoishi Y, Nakamura Y, Murata Y (2009) Exogenous proline and glycinebetaine increase antioxidant activities and confer tolerance to cadmium stress in cultured tobacco cells. J Plant Physiol 166:1587–1596

    Article  CAS  PubMed  Google Scholar 

  • Ismail MA (2008) Involvement of Ca2+ in alleviation of Cd2+ Toxicity in Common Bean (Phaseolas vulgaris L.) plants. Asian J Biol Sci 1:26–32

    Article  CAS  Google Scholar 

  • Jager H, Grill D (1975) Einfluss von SO2 und HF auf Aminosauren der Fichte (Picea abies [L.j Karsten). Eur J For Pathol 5:279–286

    Article  Google Scholar 

  • Jager H, Pahlich E (1972) Einfluss von SO2 auf den Aminosaur estoffwechsel von Erbsenkeimlingen. Oecologia (Berl) 9:135–140

    Article  Google Scholar 

  • Janeczko A, Kocielniak J, Pilipowicz M (2005) Protection of winter rape photosystem 2 by 24-epibrassinolide under cadmium stress. Photosynthetica 43:293–298

    Article  CAS  Google Scholar 

  • Jang SW, Hamayun M, Sohn EY, Shin DH, Kim KU, Lee BH, Lee IJ (2008) Effect of elevated nitrogen levels on endogenous gibberellin and jasmonic acid contents of three rice (Oryza sativa L.) cultivars. J Soil Sci Plant Nutr 171:181–186

    Article  CAS  Google Scholar 

  • Jáuregui-Zùñiga D, Ferrer MA, Calderón AA, Muñoz R, Moreno A (2005) Heavy metal stress reduces the deposition of calcium oxalate crystals in leaves of Phaseolus vulgaris. J Plant Physiol 162:1183–1187

    Article  PubMed  CAS  Google Scholar 

  • Jiang Y, Huang B (2001) Effect of calcium on antioxidant activities and water relations associated with heat tolerance in two cool season grasses. J Exp Bot 355:341–349

    Article  Google Scholar 

  • Jing-hong H, Yang Y, Qing-mao S, Chun-juan D, Zhi-gang Z (2012) Effect of exogenous salicylic acid on nitrogen assimilation of cucumber seedling under drought stress. Acta Hort Sinice 39:81–90

    Google Scholar 

  • Kalinich JF, Mandava NB, Todhunter JA (1985) Relationship of nucleic acid metabolism to brassinolide induced responses in beans. J Plant Physiol 120:207–214

    Article  CAS  Google Scholar 

  • Kapoor D, Bhardwaj R (2014) Physiological mechanisms of Brassica Juncea L. plants exposed to cadmium metal stress. Indian J Appl Res 4:8

    Google Scholar 

  • Kapoor D, Rattan A, Gautam V, Kapoor N, Bharadwaj R (2014) 24-Epibrassinolide mediated photosynthetic pigments and antioxidative defense systems of radish seedling under cadmium and mercury stress. J Stress Physiol Biochem 10:110–121

    Google Scholar 

  • Khan NA, Mobin M, Samiullah (2005) The influence of gibberellic acid and sulfur fertilization rate on growth and S-use efficiency of mustard (Brassica juncea). Plant Soil 270:269–274

    Article  CAS  Google Scholar 

  • Khan MN, Siddiqui MH, Mohammad F, Naeem M, Khan MMA (2010) Calcium chloride and gibberellic acid protect linseed (Linum usitatissimum L.) from NaCl stress by inducing antioxidative defence system and osmoprotectant accumulation. Acta Physiol Plant 32:121–132

    Article  CAS  Google Scholar 

  • Khan MIR, Iqbal N, Masood A, Per TS, Khan NA (2013) Salicylic acid alleviates adverse effects of heat stress on photosynthesis through changes in proline production and ethylene formation. Plant Signal Behav 8, e26374

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Khan MIR, Nazir F, Asgher M, Per TS, Khan NA (2014) Selenium and sulfur influence ethylene formation and alleviate cadmium-induced oxidative stress by improving proline and glutathione production in wheat. J Plant Physiol 173:9–18

    Article  CAS  Google Scholar 

  • Khatai L, Goessler W, Lorencova H, Zangger K (2004) Modulation of nitric oxide-mediated metal release from metallothionein by the redox state of glutathione in vitro. Eur J Biochem 271:2408–2416

    Article  CAS  PubMed  Google Scholar 

  • Kiba T, Kudo T, Kojima M, Sakakibara H (2011) Hormonal control of nitrogen acquisition: roles of auxin, abscisic acid, and cytokinin. J Exp Bot 62:1399–1409

    Article  CAS  PubMed  Google Scholar 

  • Kim H, Fujiwara T, Hayashi H, Chino M (1997) Effects of exogenous ABA application on sulfate and OAS concentrations, and on composition of seed storage proteins in in vitro cultured soybean immature cotyledons (conference paper). Soil Sci Plant Nutr 43:1119–1123

    CAS  Google Scholar 

  • Kim Y, Yang YY, Lee Y (2002) Pb and Cd uptake in rice toots. Physiol Plant 116:368–372

    Article  CAS  Google Scholar 

  • Koç E, Üstün AS, Çelik N (2013) Effect of exogenously applied salicylic acid on cadmium chloride-induced oxidative stress and nitrogen metabolism in tomato (Lycopersicon esculentum L.). Turk J Biol 37:361–369

    Google Scholar 

  • Koprivova A, North KA, Kopriva S (2008) Complex signaling network in regulation of adenosine 5′- phosphosulfate reductase by salt stress in Arabidopsis roots. Plant Physiol 146:1408–1420

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Krantev A, Yordanova R, Janda T, Szalai G, Popova L (2008) Treatment with salicylic acid decreases the effect of cadmium on photosynthesis in maize plants. J Plant Physiol 165:920–931

    Article  CAS  PubMed  Google Scholar 

  • Kumari A, Sheokand S, Swaraj K (2010) Nitric oxide induced alleviation of toxic effects of short term and long term Cd stress on growth, oxidative metabolism and Cd accumulation in chickpea. Braz J Plant Physiol 22:271–284

    Article  Google Scholar 

  • Kurtyka R, Małkowski E, Kita A, Karcz W (2008) Effect of calcium and cadmium on growth and accumulation of cadmium, calcium, potassium and sodium in maize seedlings. Polish J Environ Stud 17:51–56

    CAS  Google Scholar 

  • Kuthanova A, Gemperlova´ L, Zelenkova S, Eder J, Machácková I, Opatrny Z, Cvikrova M (2004) Cytological changes and alterations in polyamine contents induced by cadmium in tobacco BY-2 cells. Plant Physiol Biochem 42:149–156

    Article  CAS  PubMed  Google Scholar 

  • Kwak SH, Lee SH (1997) The requirements for Ca2+, protein phosphorylation, and dephosphorylation for ethylene signal transduction in Pisum sativum L. Plant Cell Physiol 38:1142–1149

    Article  CAS  PubMed  Google Scholar 

  • Lamotte O, Gould K, Lecourieux D, Sequeira-Legrand A, Lebrun-Garcia A, Durner J, Pugin A, Wendehenne D (2004) Analysis of nitric oxide signaling functions in tobacco cells challenged by the elicitor cryptogein. Plant Physiol 135:516–529

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Laspina NV, Groppa MD, Tomaro ML, Benavides MP (2005) Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Sci 169:323–330

    Article  CAS  Google Scholar 

  • Lee BR, Jin YL, Avice JC, Cliquet JB, Ourry A, Kim TH (2009) Increased proline loading to phloem and its effects on nitrogen uptake and assimilation in water stressed white clover (Trifolium repens). New Phytol 182:654–663

    Article  CAS  PubMed  Google Scholar 

  • Lin T, Zhu X, Zhang F, Wan X (2011) The detoxification effect of cadmium stress in Populus yunnanensis. Res J Bot 4:13–19

    Google Scholar 

  • Lopez-Carrion AI, Castellano R, Rosales MA, Ruiz JM, Romero L (2008) Role of nitric oxide under saline stress: implications on proline metabolism. Plant Biol 52:587–591

    Article  CAS  Google Scholar 

  • Lu J, Ertl JR, Chen C (1992) Transcriptional regulation of nitrate reductase mRNA levels by cytokinin abscisic acid interactions in etiolated barley leaves. Plant Physiol 98:1255–1260

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lux A, Martinka M, Vaculik M, White PJ (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62:21–37

    Article  CAS  PubMed  Google Scholar 

  • Ma W, Xu W, Xu H, Chen Y, He Z, Ma M (2010) Nitric oxide modulates cadmium influx during cadmium-induced programmed cell death in tobacco BY-2 cells. Planta 232:325–335

    Article  CAS  PubMed  Google Scholar 

  • MacRobbie EAC (1992) Calcium and ABA-induced stomatal closure. Philos Trans R Soc B 338:5–18

    Article  CAS  Google Scholar 

  • Maggio A, Barbieri G, Raimondi G, Pascale SD (2010) Contrasting effects of GA3 treatments on tomato plants exposed to increasing salinity. J Plant Growth Regul 29:63–72

    Article  CAS  Google Scholar 

  • Mahmood T, Kapuganti J, Gupta WMK (2009) Cadmium stress stimulates nitric oxide production by wheat roots. Pak J Bot 41:1285–1290

    CAS  Google Scholar 

  • Mai Y, Lin S, Zeng X, Ran R (1989) Effect of brassinolide on nitrate reductase activity in rice seedlings. Plant Physiol Commun 2:50–52

    Google Scholar 

  • Makela P, Munns R, Colmer TD, Peltonen-Sainio P (2003) Growth of tomato and an ABA-deficient mutant (sitiens) under saline conditions. Physiol Plant 117:58–63

    Article  CAS  Google Scholar 

  • Manaa A, Gharbi E, Mimouni H, Wasti S, Aschi-Smiti S, Lutts S, Ben Ahmed H (2014) Simultaneous application of salicylic acid and calcium improves salt tolerance in two contrasting tomato (Solanum lycopersicum) cultivars. South Afr J Bot 95:32–39

    Article  CAS  Google Scholar 

  • Marefat E, Shabani L, Amooaghaie R (2012) Interaction effect of cadmium and salicylic acid on proline and antioxidant enzyme activity in soybean. Malaysian Appl Biol 41:25–30

    Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, San Diego

    Google Scholar 

  • Masood A, Khan NA (2013) Ethylene and gibberellic acid interplay in regulation of photosynthetic capacity inhibition by cadmium. J Plant Biochem Physiol 1:3

    Google Scholar 

  • Masood A, Iqbal N, Khan NA (2012) Role of ethylene in alleviation of cadmium-induced photosynthetic capacity inhibition by sulphur in mustard. Plant Cell Environ 35:524–533

    Article  CAS  PubMed  Google Scholar 

  • McAinsh MR, Brownlee C, Hetherington AM (1997) Calcium ions as second messengers in guard cell signal transduction. Physiol Plant 100:16–29

    Article  CAS  Google Scholar 

  • Meher HC, Gajbhiye VT, Singh G (2011) Salicylic acid-induced glutathione status in tomato crop and resistance to root-knot nematode, Meloidogyne incognita (Kofoid & White). Chitwood J Xenobiotics 1, e5

    Article  CAS  Google Scholar 

  • Mehta SK, Gaur JP (1999) Heavy-metal-induced proline accumulation and its role in ameliorating metal toxicity in Chlorella vulgaris. New Phytol 143:253–259

    Article  CAS  Google Scholar 

  • Mendoza-Cózatl DG, Jobe TO, Hauser F, Schroeder JI (2011) Long-distance transport, vacuolar sequestration, tolerance, and transcriptional responses induced by cadmium and arsenic. Curr Opin Plant Biol 14:554–562

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Meng H, Hua S, Shamsi IH, Jilani G, Li Y et al (2009) Cadmium-induced stress on the seed germination and seedling growth of Brassica napus L., and its alleviation through exogenous plant growth regulators. Plant Growth Regul 58:47–59

    Article  CAS  Google Scholar 

  • Metwally A, Safronova VI, Belimov AA, Dietz KJ (2005) Genotypic variation of the response to cadmium toxicity in Pisum sativum L. J Exp Bot 56:167–178

    CAS  PubMed  Google Scholar 

  • Misra N, Gupta AK (2006) Interactive effects of sodium and calcium on proline metabolism in salt tolerant green gram cultivar. J Plant Physiol 1:1–12

    Article  CAS  Google Scholar 

  • Misra N, Saxena P (2009) Effect of salicylic acid on proline metabolism in lentil grown under salinity stress. Plant Sci 177:181–189

    Article  CAS  Google Scholar 

  • Moat AG, Foster JW, Spector MP (2003) Biosynthesis and metabolism of amino acids. In: Moat AG, Foster JW, Spector MP (eds) Microbial physiology. Wiley, New York, pp 503–544

    Google Scholar 

  • Molinari HBC, Marur CJ, Daros E, de Campos MKF, de Carvalho JFRP, Filho JCB (2007) Evaluation of the stress-inducible production of praline in transgenic sugarcane (Saccharum spp.): osmotic adjustment, chlorophyll fluorescence and oxidative stress. Physiol Plant 130:218–229

    Article  CAS  Google Scholar 

  • Moradkhani S, Nejad RAK, Dilmaghani K, Chaparzadeh N (2013) Salicylic acid decreases Cd toxicity in sunflower plants. Ann Biol Res 4:135–141

    CAS  Google Scholar 

  • Mori IC, Schroeder JI (2004) Reactive oxygen species activation of plant Ca2+ channels. A signaling mechanism in polar growth, hormone transduction, stress signaling and hypothetically mechanotransduction. Plant Physiol 135:702–708

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Moussa HR, El-Gamal SM (2010) Role of salicylic acid in regulation of cadmium toxicity in wheat (Triticum aestivum L.). J Plant Nutr 33(10):1460–1471

    Article  CAS  Google Scholar 

  • Murata Y, Pei ZM, Mori IC, Schroeder J (2001) Abscisic acid activation of plasma membrane Ca2+ channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell 13:2513–2523

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nazar R, Iqbal N, Syeed S, Khan NA (2011) Salicylic acid alleviates decreases in photo-synthesis under salt stress by enhancing nitrogen and sulfur assimilation and antioxidant metabolism differentially in two mungbean cultivars. J Plant Physiol 168:807–815

    Article  CAS  PubMed  Google Scholar 

  • Nazar R, Iqbal N, Masood A, Khan MIR, Khan NA (2012) Cadmium toxicity in plants and role of mineral nutrients in its alleviation. J Plant Sci 3:1476–1489

    Article  CAS  Google Scholar 

  • Nazar R, Khan MIR, Iqbal N, Masood A, Khan NA (2014) Involvement of ethylene in reversal of salt-inhibited photosynthesis by sulphur in mustard. Physiol Plant 152:331–344

    Article  CAS  PubMed  Google Scholar 

  • Nazar R, Umar S, Khan NA, Sareer O (2015) Salicylic acid supplementation improves photosynthesis and growth in mustard through changes in proline accumulation and ethylene formation under drought stress. S Afr J Bot 98:84–94

    Article  CAS  Google Scholar 

  • Nedjimi B, Daoud Y (2009) Cadmium accumulation in Atriplex halimus subsp. schweinfurthii and its influence on growth, proline, root hydraulic conductivity and nutrient uptake. Flora-Mor Dist Func Ecol Plant 204:316–324

    Article  Google Scholar 

  • Neill SJ, Desikan R, Hancock JT (2003) Nitric oxide signaling in plants. New Phytol 159:11–35

    Article  CAS  Google Scholar 

  • Nelson MT (1986) Interactions of divalent cations with single calcium channels from rat brain synaptosomes. J Gen Physiol 87:201–222

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nies DH (1999) Microbial heavy-metal resistance. Appl Microbiol Biotechnol 51:730–750

    Article  CAS  PubMed  Google Scholar 

  • Nikiforova VJ, Daub CO, Hesse H, Willmitzer L, Hoefgen R (2005) Integrative gene-metabolite network with implemented causality deciphers informational fluxes of sulphur stress response. J Exp Bot 56:1887–1896

    Article  CAS  PubMed  Google Scholar 

  • Oh M-H, Kim HS, Wu X, Clouse SD, Zielinski RE, Huber SC (2012) Calcium/calmodulin inhibition of the Arabidopsis BRASSINOSTEROID-INSENSITIVE 1 receptor kinase provides a possible link between calcium and brassinosteroid signaling. Biochem J 443:515–523

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Okuma E, Murakami Y, Shimoishi Y, Tada M, Murata Y (2004) Effects of exogenous application of proline and betaine on the growth of tobacco cultured cells under saline conditions. Soil Sci Plant Nutr 50:1301–1305

    Article  CAS  Google Scholar 

  • Ouariti O, Boussama N, Zarrouk M, Cherif A, Ghorbal MH (1997) Cadmium- and copper-induced changes in tomato membrane lipids. Phytochemistry 45:1343–1350

    Article  CAS  PubMed  Google Scholar 

  • Oulhajd A, Kuschk P, Humback K (2006) Heavy metal stress and leaf senescence induce the barley gene HvC2d1 encoding a calcium-dependent novel C2 domain-like protein. New Phytol 170:261–273

    Article  Google Scholar 

  • Pal UR, Gossett DR, Sims JL, Legett JE (1976) Molybdenum and sulfur nutrition effects on nitrate reductase in barley tobacco. Can J Bot 54:2014–2022

    Article  CAS  Google Scholar 

  • Paleg LG, Doughlas TJ, Vandaal A, Keech DB (1981) Proline and betaine protect enzymes against heat inactivation. Aust J Plant Physiol 8:107–114

    CAS  Google Scholar 

  • Panda P, Nath S, Chanu TT, Sharma GD, Panda SK (2011) Cadmium stress-induced oxidative stress and role of nitric oxide in rice (Oryza sativa L.). Acta Physiol Plant 33:1737–1747

    Article  CAS  Google Scholar 

  • Pandey S (2001) Response of nitrate assimilation to putrescine and glutamine supply in subabul (Leucaena leucocephala) cotyledons. Indian J Agric Sci 71:341–343

    CAS  Google Scholar 

  • Pankovic D, Plesnicar M, Arsenijeevic-Maksimovic I, Petrovic N, Sakac Z, Kastori R (2000) Effects of nitrogen nutrition on photosynthesis in Cd-treated sunflower plants. Ann Bot 86:841–847

    Article  CAS  Google Scholar 

  • Parmar P, Kumari N, Sharma V (2013) Structural and functional alterations in photosynthetic apparatus of plants under cadmium stress. Bot Stud 54:45

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Picazo I, Ros R, Moya JL (2007) Heavy metal hormone interactions in rice plants: effect on growth, net photosynthesis and carbohydrate distribution. J Plant Growth Regul 14:61–67

    Google Scholar 

  • Popova LP, Maslenkova LT, Yordanova RY, Ivanova AP, Krantev AP, Szalai G, Janda T (2009) Exogenous treatment with salicylic acid attenuates cadmium toxicity in pea seedlings. Plant Physiol Biochem 47:224–231

    Article  CAS  PubMed  Google Scholar 

  • Potters G, Pasternak TP, Guisez Y, Palme KJ, Jansen MA (2007) Stress-induced morphogenic responses: growing out of trouble? Trends Plant Sci 12:98–105

    Article  CAS  PubMed  Google Scholar 

  • Pustovoitova TN, Bavrina TV, Zhdanova NE (2000) Drought tolerance of transgenic tobacco plants carrying the iaaM and iaaH genes of auxin biosynthesis. Russ J Plant Physiol 47:380e385

    Google Scholar 

  • Qiao X, Wang P, Shi G, Yang H (2015) Zinc conferred cadmium tolerance in Lemna minor L. via modulating polyamines and proline metabolism. Plant Growth Regul. doi:10.1007/s10725-015-0027-0

    Google Scholar 

  • Radic S, Babic M, Skobic D, Roje V, Pevalek-Kozlina B (2010) Ecotoxicological effects of aluminum and zinc on growth and antioxidants in Lemna minor L. Ecotoxicol Environ Saf 73:336–342

    Article  CAS  PubMed  Google Scholar 

  • Rady MM (2011) Effect of 24-epibrassinolide on growth, yield, antioxidant system and cadmium content of bean (Phaseolus vulgaris L.) plants under salinity and cadmium stress. Sci Hortic 129:232–237

    Article  CAS  Google Scholar 

  • Rais L, Masood A, Inam A, Khan NA (2013) Sulfur and nitrogen co-ordinately improve photosynthetic efficiency, growth and proline accumulation in two cultivars of mustard under salt stress. J Plant Biochem Physiol 1:1

    Google Scholar 

  • Raz V, Fluhr R (1992) Calcium requirement for ethylene-dependent responses. Plant Cell 4:1123–1130

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 20:600–608

    Article  CAS  Google Scholar 

  • Rodríguez-Serrano M, Romero-Puertas MC, Pazmiño DM, Testillano PS, Risueño MC, del Río LA, Sandalio LM (2009) Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiol 150:229–243

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Rubio M, Escrig I, Martinez-Cortina C, Lopez-Benet F, Sanz A (1994) Cadmium and nickel accumulation in rice plants. Effects on mineral nutrition and possible interactions of abscisic and gibberellic acids. Plant Growth Regul 14:151–157

    Article  CAS  Google Scholar 

  • Sakakibara H (2003) Nitrate-specific and cytokinin-mediated nitrogen signaling pathways in plants. J Plant Res 116:253–257

    Article  CAS  PubMed  Google Scholar 

  • Sánchez E, Ávila-Quezada G, Gardea AA, Ruiz JM, Romero L (2007) Biosynthesis of proline in fruits of green bean plants: deficiency versus toxicity of nitrogen. Int J Exp Bot 76:143–152

    Google Scholar 

  • Sandalio LM, Dalurzo HC, Gómez M, Romero-Puertas MC, del Río LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2126

    CAS  PubMed  Google Scholar 

  • Sankla M, Huber W (1975) Effect of salt and abscisic acid on in vivo activity of nitrate reductase in seedlings of Phaseolus aconitifolius. Z Pflanzenphysiol 76:467–470

    Article  Google Scholar 

  • Schwartz A (1985) Role of calcium and EGTA on stomatal movements in Commelina communis. Plant Physiol 79:1003–1005

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Seki M, Umezawa T, Urano K (2007) Regulatory metabolic networks in drought stress responses. Curr Opin Plant Biol 10:296–302

    Article  CAS  PubMed  Google Scholar 

  • Schroeder JI, Hagiwara S (1990) Repetitive increases in cytosolic Ca2+ of guard cells by abscisic acid activation of nonselective Ca2+ permeable channels. Proc Natl Acad Sci U S A 87:9305–9309

    Google Scholar 

  • Shah K, Dubey RS (1998) Effect of cadmium on proline accumulation and ribonuclease activity in rice seedlings: role of proline as a possible enzyme protectant. Biol Plant 40:121–130

    Article  Google Scholar 

  • Shah SH, Wainwright SJ, Merrett MJ (1990) The interaction of sodium and calcium chlorides and light on growth, potassium nutrition and proline accumulation in callus culture of Medicago sativa L. New Phytol 116:37–45

    Article  CAS  Google Scholar 

  • Shah SH, Tobita S, Shono M (2001) Supplemental calcium regulates proline accumulation in NaCl-stressed suspension culture of Oryza sativa L. at the level of mRNA translation. Pak J Biol Sci 4:707–710

    Article  Google Scholar 

  • Sharma S, Dietz K (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 57:711–726

    Article  CAS  PubMed  Google Scholar 

  • Sharma SS, Schat H, Vooijs R (1998) In vitro alleviation of heavy metal induced enzyme inhibition by proline. Phytochemistry 46:1531–1535

    Article  Google Scholar 

  • Shi GR, Cai QS, Liu QQ, Wu L (2009) Salicylic acid-mediated alleviation of cadmium toxicity in hemp plants in relation to cadmium uptake, photosynthesis and antioxidant enzymes. Acta Physiol Plant 31:969–977

    Article  CAS  Google Scholar 

  • Siddiqui MH, Khan MN, Mohammad F, Khan MMA (2008) Role of nitrogen and gibberellins (GA3) in the regulation of enzyme activities and in osmoprotectant accumulation in Brassica juncea L. under salt stress. J Agron Crop Sci 194:214–224

    Article  CAS  Google Scholar 

  • Siddiqui MH, Al-Whaibi MH, Basalah MO (2011) Interactive effect of calcium and gibberellin on nickel tolerance in relation to antioxidant systems in Triticum aestivum L. Protoplasma 248:503–511

    Article  CAS  PubMed  Google Scholar 

  • Signora L, De Smet I, Foyer CH, Zhang H (2001) ABA plays a central role in mediating the regulatory effects of nitrate on root branching in Arabidopsis. Plant J 28:655–662

    Article  CAS  PubMed  Google Scholar 

  • Simaei M, Khavarinejad RA, Saadatmand S, Bernard F, Fahimi H (2011) Interactive effects of salicylic acid and nitric oxide on soybean plants under NaCl salinity. Russ J Plant Physiol 58:783–790

    Article  CAS  Google Scholar 

  • Singh PK, Chaturvedi VK (2012) Effects of salicylic acid on seedling growth and nitrogen use efficiency in cucumber (Cucumis sativus L.). Plant Biosyst 146:302–308

    Article  Google Scholar 

  • Singh I, Shah K (2015) Evidences for suppression of cadmium induced oxidative stress in presence of sulphosalicylic acid in rice seedlings. Plant Growth Regul 76:12p

    Google Scholar 

  • Singla B, Chugh A, Khurana JP, Khurana P (2006) An early auxin-responsive Aux/IAA gene from wheat (Triticum aestivum) is induced by epibrassinolide and differentially regulated by light and calcium. J Exp Bot 57:4059–4070

    Article  CAS  PubMed  Google Scholar 

  • Siripornadulsil S, Traina S, Verma DP, Sayre RT (2002) Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae. Plant Cell 14:2837–2847

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Stroiński A, giżewska K, zielezińska M (2013) Abscisic acid is required in transduction of cadmium signal to potato roots. Biol Plant 57:121–127

    Article  CAS  Google Scholar 

  • 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 18:2605–2610

    CAS  Google Scholar 

  • Sun Q, Yec ZH, Wang XR, Wong MH (2007) Cadmium hyperaccumulation leads to an increase of glutathione rather than phytochelatins in the cadmium hyperaccumulator Sedum alfredii. J Plant Physiol 164:1489–1498

    Article  CAS  PubMed  Google Scholar 

  • Suzuki N (2005) Alleviation by calcium of cadmium-induced root growth inhibition in Arabidopsis seedlings. Plant Biotechnol 22:19–25

    Article  CAS  Google Scholar 

  • Talanova VV, Titov AF, Boeva NP (2000) Effect of increasing concentrations of lead and cadmium on cucumber seedlings. Biol Plant 43:441–444

    Article  CAS  Google Scholar 

  • Tarighaleslami M, Zarghami R, Boojar MMA, Oveysi M (2012) Effects of drought stress and different nitrogen levels on morphological traits of proline in leaf and protein of corn seed (Zea mays L.). Am-Eurasian J Agric Environ Sci 12:49–56

    Google Scholar 

  • Terrile MC, Tonon CV, Iglesias MJ, Lamattina L, Casalongue CA (2010) Extracellular ATP and nitric oxide signaling pathways regulate redox-dependent responses associated to root hair growth in etiolated Arabidopsis seedlings. Plant Signal Behav 5:698–701

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Upreti KK, Murti GSR (2004) Effects of brassinosteroids on growth, nodulation, phytohormone content and nitrogenase activity in French bean under water stress. Biol Plant 48:407–411

    Article  CAS  Google Scholar 

  • Verma K, Mehta SK, Shekhawat GS (2013) Nitric oxide (NO) counteracts cadmium induced cytotoxic processes mediated by reactive oxygen species (ROS) in Brassica juncea: cross-talk between ROS, NO and antioxidant responses. BioMetals 26:255–269

    Article  CAS  PubMed  Google Scholar 

  • Villiers F, Jourdain A, Bastien O, Leonhardt N et al (2012) Evidence for functional interaction between brassinosteroids and cadmium response in Arabidopsis thaliana. J Exp Bot 63:1185–1200

    Article  CAS  PubMed  Google Scholar 

  • Wang QC, Song H (2009) Calcium protects Trifolium repens L. seedlings against cadmium stress. Plant Cell Rep 28:1341–1349

    Article  CAS  PubMed  Google Scholar 

  • Wang LJ, Chen SJ, Kong WF, Li SH, Archbold DD (2006) Salicylic acid pretreatment alleviates chilling injury and affects the antioxidant system and heat shock proteins of peaches during cold storage. Postharvest Biol Technol 41:244–225

    Article  CAS  Google Scholar 

  • Wang Q, Liang X, Dong Y, Xu L, Zhang X, Kong J, Liu S (2013) Effects of exogenous salicylic acid and nitric oxide on physiological characteristics of perennial ryegrass under cadmium stress. J Plant Growth Regul 32:721–731

    Article  CAS  Google Scholar 

  • Wen X-P, Ban Y, Inoue H, Matsuda N, Kita M et al (2011) Antisense inhibition of a spermidine synthase gene highlights the role of polyamines for stress alleviation in pear shoots subjected to salinity and cadmium. Environ Exp Bot 72:157–166

    Article  CAS  Google Scholar 

  • Wu JT, Chang SJ, Chou TL (1995) Intracellular proline accumulation in some algae exposed to copper and cadmium. Bot Bull Acad Sinica 36:89–93

    CAS  Google Scholar 

  • Xie HL, Jiang RF, Zhang FS, McGrath SP, Zhao FJ (2009) Effect of nitrogen form on the rhizosphere dynamics and uptake of cadmium and zinc by the hyperaccumulator Thlaspi caerulescens. Plant and Soil 318:205–215

    Article  CAS  Google Scholar 

  • Xiong J, Fu G, Tao L, Zhu C (2010) Roles of nitric oxide in alleviating heavy metal toxicity in plants. Arch Biochem Biophys 497:13–20

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Yin HX, Li X (2009) Protective effects of proline against cadmium toxicity in micropropagated hyperaccumulator, Solanum nigrum L. Plant Cell Rep 28:325–333

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Wang W, Yin H, Liu X, Sun H, Mi Q (2010) Exogenous nitric oxide improves antioxidative capacity and reduces auxin degradation in roots of Medicago truncatula seedlings under cadmium stress. Plant Soil 326:321–330

    Article  CAS  Google Scholar 

  • Xu X, Shi G, Ding C, Xu Y, Zhao J, Yang H, Pan Q (2011) Regulation of exogenous spermidine on the reactive oxygen species level and polyamine metabolism in Alternanthera philoxeroides (Mart.) Griseb under copper stress. Plant Growth Regul 63:251–258

    Article  CAS  Google Scholar 

  • Xu C, Li X, Zhang L (2013a) The effect of calcium chloride on growth, photosynthesis, and antioxidant responses of Zoysia japonica under drought conditions. PLoS One 8, e68214

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xu L, Dong Y, Fan Z, Kong J, Liu S, Bai S (2013b) Effects of the application of exogenous NO at different growth stage on the physiological characteristics of peanut grown in Cd-contaminated soil. J Plant Interact 9:285–296

    Article  CAS  Google Scholar 

  • Yadav S, Hayat S, Wani AS, Irfan M, Ahmad A (2012) Homobrassinolide and 24-epibrassinolide on nitrate reductase activity, proline content, and antioxidative enzymes of tomato. Intl J Veg Sci 18:161–170

    Article  Google Scholar 

  • Yamagami K, Nishimura S, Sorimachi M (1998) Cd2+ and Co2+ at micromolar concentrations mobilize Ca2+ via the generation of 1,4,5-triphosphate in bovine chromaffin cells. Brain Res 798:316–319

    Article  CAS  PubMed  Google Scholar 

  • Yang C-S, Tzou B-C, Liu YP, Tsai M-J, Shye SQ, Tzeng S-F (2008) Inhibition of cadmium induced oxidative injury in rat primary astrocytes by the addition of antioxidants and the reduction of intracellular calcium. J Cell Biochem 103:825–834

    Article  CAS  PubMed  Google Scholar 

  • Ye J-L, Mao W-P, Wu A-L, Zhang N-N, Zhang C, Yu Y-J, Zhou L, Wei C-L (2007) Cadmium-induced apoptosis in human normal liver L-02 cells by acting on mitochondria and regulating Ca2+ signals. Environ Toxicol Phar 24:45–54

    Article  CAS  Google Scholar 

  • Yendrek CR, Lee YC, Morris V, Liang Y, Pislariu CI, Burkart G, Meckfessel MH, Salehin M, Kessler H, Wessler H, Lloyd M, Lutton H, Teillet A, Sherrier DJ, Journet EP, Harris JM, Dickstein R (2010) A putative transporter is essential for integrating nutrient and hormone signaling with lateral root growth and nodule development in Medicago truncatula. Plant J 62:100–112

    Article  CAS  PubMed  Google Scholar 

  • Yilmaz R, Sakcali S, Yarci C, Aksoy A, Ozturk M (2006) Use of Aesculus hippocastanum L. as a biomonitor of heavy metal pollution. Pak J Bot 38:1519–1527

    Google Scholar 

  • Yoo JH, Park CY, Kim JC, Heo WD, Cheong MS, Park HC, Kim MC, Moon BC, Choi MS, Kang YH, Lee JH, Kim HS, Lee SM, Yoon HW, Lim CO, Yun DJ, Lee SY, Chung WS, Cho MJ (2005) Direct interaction of a divergent CaM isoform and the transcription factor, MYB2, enhances salt tolerance in Arabidopsis. J Biol Chem 280:3697–3706

    Article  CAS  PubMed  Google Scholar 

  • Youm JW, Jeon JH, Choi D, Yi SY, Joung H, Kim HS (2008) Ectopic expression of pepper CaPF1 in potato enhances multiple stresses tolerance and delays initiation of in vitro tuberization. Planta 228:701–708

    Article  CAS  PubMed  Google Scholar 

  • Yuan L, Yuan Y, Du J, Sun J, Guo S (2012) Effects of 24-epibrassinolide on nitrogen metabolism in cucumber seedlings under Ca(NO3)2 stress. Plant Physiol Biochem 61:29–35

    Article  CAS  PubMed  Google Scholar 

  • Yusuf M, Fariduddin Q, Ahmad I, Ahmad A (2014) Brassinosteroid-mediated evaluation of antioxidant system and nitrogen metabolism in two contrasting cultivars of Vigna radiata under different levels of nickel. Physiol Mol Biol Plant 20:449–460

    Article  CAS  Google Scholar 

  • Zafar S, Nasri M, Moghadam HRT, Zahedi H (2014) Effect of zinc and sulfur foliar applications on physiological characteristics of sunflower (Helianthus annuus L.) under water deficit stress. Int J Biosci 5:87–96

    CAS  Google Scholar 

  • Zakery-Asl MA, Bolandnazara S, Oustanb S (2014) Effect of salinity and nitrogen on growth, sodium, potassium accumulation, and osmotic adjustment of halophyte Suaedaa egyptiaca (Hasselq.). Zoh Arch Agron Soil Sci 60:785–792

    Article  CAS  Google Scholar 

  • Zawoznik MS, Groppa MD, Tomaro ML, Benavides MP (2007) Endogenous salicylic acid potentiates cadmium-induced oxidative stress in Arabidopsis thaliana. Plant Sci 173:190–197

    Article  CAS  Google Scholar 

  • Zengin FK, Munzuroglu O (2005) Effects of some heavy metals on content of chlorophyll, proline and some antioxidant chemicals in bean (Phaseolus vulgaris L.) seedlings. Acta Biol Cracov Bot 47:157–164

    Google Scholar 

  • Zhang WN, Chen WL (2011) Role of salicylic acid in alleviating photochemical damage and autophagic cell death induction of cadmium stress in Arabidopsis thaliana. Photochem Photobiol Sci 10:947–955

    Article  CAS  PubMed  Google Scholar 

  • Zhang LP, Mehta SK, Liu ZP, Yang ZM (2008) Copper induced proline synthesis is associated with nitric oxide generation in Chlamydomonas reinhardtii. Plant Cell Physiol 49:411–419

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Li F, Li D, Zhang H, Huang R (2010) Expression of ethylene response factor JERF1 in rice improves tolerance to drought. Planta 232:765e774

    Google Scholar 

  • Zhang Y, Xu S, Yang S, Chen Y (2015) Salicylic acid alleviates cadmium-induced inhibition of growth and photosynthesis through upregulating antioxidant defense system in two melon cultivars (Cucumis melo L.). Protoplasma 252:911–924

    Article  CAS  PubMed  Google Scholar 

  • Zhao Y, Qi Z, Berkowitz GA (2013) Teaching an old hormone new tricks: cytosolic Ca2+ elevation involvement in plant brassinosteroid signal transduction cascades. Plant Physiol 163:555–565

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhenyan HE, Jiangchuan LI, Zhang H, Ma MI (2005) different effects of calcium and lanthanum on the expression of phytochelatin synthase gene and cadmium absorption in Lactuca sativa. Plant Sci 168:309–318

    Article  CAS  Google Scholar 

  • Zhou ZS, Guo K, Elbaz AA, Yang ZM (2009) Salicylic acid alleviates mercury toxicity by preventing oxidative stress in roots of Medicago sativa. Environ Exp Bot 65:27–34

    Article  CAS  Google Scholar 

  • Zhu E, Liu D, Li JG, Li TQ, Yang XE, He ZL, Stoffella PJ (2011) Effect of nitrogen fertilizer on growth and cadmium accumulation in Sedum alfredii Hance. J P Nutr 34:115–126

    Article  CAS  Google Scholar 

  • Zhu XF, Jiang T, Wang ZW, Lei GJ, Shi YZ, Li GX, Zheng SJ (2012) Gibberellic acid alleviates cadmium toxicity by reducing nitric oxide accumulation and expression of IRT1 in Arabidopsis thaliana. J Hazard Mat 239–240:302–307

    Article  CAS  Google Scholar 

Download references

Acknowledgment

The first and the second author are thankful to the University Grants Commission, New Delhi, for D. S. Kothari Postdoctoral Fellowship (File No. F.4-2/2006 (BSR)/13-848/2013(BSR) and File No. F.4-2/2006(BSR)/13-711/2012(BSR)).

Author information

Authors and Affiliations

  1. Department of Botany, Jamia Hamdard University, New Delhi, 110062, Delhi, India

    Noushina Iqbal & Rahat Nazar

  2. Department of Botany, Faculty of Science, Jamia Hamdard University, New Delhi, 110062, India

    Shahid Umar

Authors
  1. Noushina Iqbal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rahat Nazar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shahid Umar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Noushina Iqbal .

Editor information

Editors and Affiliations

  1. Department of Botany, Jamia Hamdard University, New Delhi, Delhi, India

    Noushina Iqbal

  2. Department of Botany, Jamia Hamdard University, New Delhi, Delhi, India

    Rahat Nazar

  3. Department of Botany, Aligarh Muslim University, Aligarh, Uttar Pradesh, India

    Nafees A. Khan

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer India

About this chapter

Cite this chapter

Iqbal, N., Nazar, R., Umar, S. (2016). Evaluating the Importance of Proline in Cadmium Tolerance and Its Interaction with Phytohormones. In: Iqbal, N., Nazar, R., A. Khan, N. (eds) Osmolytes and Plants Acclimation to Changing Environment: Emerging Omics Technologies. Springer, New Delhi. https://doi.org/10.1007/978-81-322-2616-1_8

Download citation

Publish with us

Policies and ethics

Search

Navigation