Skip to main content
SpringerLink
Log in

Signaling responses in plants to heavy metal stress

  • Review
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Heavy metal toxicity is one of the major abiotic stresses leading to hazardous health effects in animals and plants. Because of their high reactivity they can directly influence growth, senescence and energy synthesis processes. In this review a new indirect mechanism of heavy metal action is proposed. This mechanism is connected with the generation of reactive oxygen species (especially H2O2) and jasmonate and ethylene signaling pathways and shows that toxicity symptoms observed in plants may result from direct heavy metal influence as well as the activity of some signaling molecules induced by the stress action.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

ACC:

Amino-cyclopropane-1-carboxylic acid

CAM-Ca:

Calmodulin-Ca complex

CC:

Calvin cycle

GLV:

Green leaf volatiles

FA-OOH:

Fatty acids hydroperoxides

JA:

Jasmonic acid

LHCII:

Light-harvesting chlorophyll complex of photosystem II

MJ:

Methyl jasmonate

OPDA:

Oxo-phytodienoic acid

PUFA:

Polyunsaturated fatty acid

ROS:

Reactive oxygen species

SA:

Salicylic acid

SOD:

Superoxide dismutase

TBArm:

Thiobarbituric acid reactive material

TMV:

Tobacco mosaic virus

References

  • Agrawal GK, Iwahashi H, Rakwal R (2003a) Rice MAPKs. Biochem Biophys Res Commun 302:171–180

    CAS  Google Scholar 

  • Agrawal GK, Jwa N-S, Agrawal SK, Tamogami S, Iwahashi H, Rakwal R (2003b) Cloning of novel rice allene oxide cyclase (OsAOC): mRNA expression and comparative analysis with allene oxide synthase (OsAOS) gene provide insight into the transcriptional regulation of octadecanoid pathway biosynthetic genes in rice. Plant Sci 164:979–992

    CAS  Google Scholar 

  • Agrawal GK, Tamogami S, Iwahashi H, Agrawal VP, Rakwal R (2003c) Transient regulation of jasmonic acid-inducible rice MAP kinase gene (OsBWMK1) by diverse biotic and abiotic stresses. Plant Physiol Biochem 41:355–361

    CAS  Google Scholar 

  • Ahmed A, Tajmir-Riahi HA (1993) Interaction of toxic metal ions Cd2+, Hg2+ and Pb2+ with light-harvesting proteins of chloroplast thylakoids membranes. An FTR studies. J Inorg Chem 50:235–243

    CAS  Google Scholar 

  • Alaoui-Sossé B, Genet P, Vinit-Dunand F, Toussaint M-L, Epron D, Badot P-M (2004) Effect of copper on growth in cucumber plants (Cucumis sativus) and its relationships with carbohydrate accumulation and changes in ion contents. Plant Sci 166:1213–1218

    Google Scholar 

  • Bishop GJ, Koncz C (2002) Brassionosteroids and plant steroid hormone signaling. Plant Cell 14(Suppl):97–110

    Google Scholar 

  • Blechert S, Brodschelm W, Hölder S, Kammerer L, Kutchan T, Mueller M, Xia Z-Q, Zenk M (1995) The octadecenoic pathway: signal molecule for regulation of secondary pathways. Proc Natl Acad Sci USA 92:4099–4105

    PubMed  CAS  Google Scholar 

  • Böddi B, Oravecz AR, Lehoczki E (1995) Effect of cadmium on organization and photoreduction of protochlorophyllide in dark-grow leaves and etioplast inner membrane preparations of wheat. Photosynthetica 31:411–420

    Google Scholar 

  • Brisson LF, Tenhaken R, Lamb C (1994) Function of oxidative cross-linking of cell wall structural proteins in plant disease resistance. Plant Cell 6:1703–1712

    PubMed  CAS  Google Scholar 

  • Casella S, Frassinetti S, Lupi F, Squartini A (1988) Effect of cadmium, chromium and copper on symbiotic and free-living Rhizobium leguminosarium biovar trifolii. FEMS Microbiol Lett 49:343–347

    CAS  Google Scholar 

  • Chai TY, Didierjean L, Burkard G, Genot G (1998) Expression of a green tissue-specific 11 kDa proline-rich protein gene in bean in response to heavy metals. Plant Sci 133:47–56

    Google Scholar 

  • Chaoui A, Mazhoudi S, Ghorbal MN, Ferjani EE (1997) Cadmium and zinc induction of lipid peroxidation and effects on antioxidant enzymes activities in bean (Phaseolus vulgaris L.). Plant Sci 127:139–147

    CAS  Google Scholar 

  • Cho U-H, Park J-O (2000) Mercury-induced oxidative stress in tomato seedlings. Plant Sci 156:1–9

    PubMed  CAS  Google Scholar 

  • Cho U-H, Seo N-H (2005) Oxidative stress in Arabidopsis thaliana exposed to cadmium is due to hydrogen peroxide accumulation. Plant Sci 168:113–120

    CAS  Google Scholar 

  • Cruz-Ortega R, Ownby JD (1993) A protein similar to PR (pathogen-related) proteins is elicited by metal toxicity in wheat roots. Physiol Plant 89:211–219

    CAS  Google Scholar 

  • Cuypers A, Vangronsfeld J, Clijsters H (2000) Biphasic effect of copper on the ascorbate-glutathione pathway in primary leaves of Phaseolus vulgaris seedlings during the early stages of metal assimilation. Physiol Plant 110:512–517

    CAS  Google Scholar 

  • Delhaise E, Robinson NJ, Jackson PJ (1989) Effects of cadmium on gene expression in cadmium-tolerant and cadmium-sensitive Datura inoxia cells. Plant Mol Biol 12:487–497

    Google Scholar 

  • Demirevska-Kepova K, Simova-Stoilova L, Stoyanova Z, Hölzer R, Feller U (2004) Biochemical changes in barley plants after excessive supply of copper and manganese. Environ Exp Bot 52:253–266

    CAS  Google Scholar 

  • Didierjean L, Frendo P, Nasser W, Genot G, Marivet J, Burkard G (1996) Heavy metal-responsive genes in maize: identification and comparison of their expression upon various forms of abiotic stress. Planta 199:1–8

    PubMed  CAS  Google Scholar 

  • Drążkiewicz M, Skórzyńska-Polit E, Krupa Z (2004) Copper-induced oxidative stress and antioxidant defence in Arabidopsis thaliana. BioMetals 17:379–387

    PubMed  Google Scholar 

  • Durner J, Klessig DF (1999) Nitric oxide as signal in plants. Curr Opin Plant Biol 2:369–374

    PubMed  CAS  Google Scholar 

  • Eckardt NA (2003) A new twist on the systemic acquired resistance: redox control of the NPR1-TGA1 interaction by salicylic acid. Plant Cell 15:1947–1949

    CAS  Google Scholar 

  • Enyedi AJ, Yalpani N, Silverman P, Raskin I (1992) Signal molecules in systemic plant resistance to pathogens and pests. Cell 70:879–886

    PubMed  CAS  Google Scholar 

  • Fang W-Ch, Kao ChH (2000) Enhanced peroxidase activity in rice leaves in response to excess iron, copper and zinc. Plant Sci 158:71–76

    Google Scholar 

  • Farmer EE, Alméras E, Krishnamurthy V (2003) Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Curr Opin Plant Biol 6:372–378

    PubMed  CAS  Google Scholar 

  • Finkelstein RR, Gampala SSL, Rock ChD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14(Suppl):15–45

    Google Scholar 

  • Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownelee C, Jones JDG, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446

    PubMed  CAS  Google Scholar 

  • Foyer CH, Noctor G (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119:355–364

    CAS  Google Scholar 

  • Ghoshroy S, Freedman K, Lartey R, Citovsky V (1998) Inhibition of plant viral systemic infection by non-toxic concentration of cadmium. Plant J 13:591–602

    PubMed  CAS  Google Scholar 

  • Golldack D, Vera P, Dietz KJ (2003) Expression of subtilisin-like serine proteases in Arabidopsis thaliana is cell-specific and responds to jasmonic acid and heavy metals with developmental differences. Physiol Plant 118:64–73

    PubMed  CAS  Google Scholar 

  • Gora L, Clijsters H (1989) Effect of copper and zinc on the ethylene metabolism in Phaseolus vulgaris L. In: Clijsters H (eds) Biochemical and physiological aspects of ethylene production in lower and higher plants, Kluwer, Dordrecht, pp 219–228

    Google Scholar 

  • Gratão PL, Polle A, Lea PJ, Azevedo RA (2005) Making the life of heavy metal-stressed plants a little easier. Funct Plant Biol 32:481–494

    Google Scholar 

  • Guo H, Ecker JR (2004) The ethylene signaling pathway: new insights. Curr Opin Plant Biol 7:40–49

    PubMed  CAS  Google Scholar 

  • Gupta V, Willits MG, Galzebrook J (2000) Arabidopsis thaliana EDS4 contributes to salicylic acid (SA)-dependent expression of defense responses. Evidence for inhibition of jasmonic acid signaling by SA. Mol Plant-Microbe Interact 13:503–511

    PubMed  CAS  Google Scholar 

  • Hensel G, Kunze G, Kunze I (1999) Expression of the tobacco gene CBP20 in response to developmental stage, wounding, salicylic acid and heavy metals. Plant Sci 148:165–174

    CAS  Google Scholar 

  • He Y, Fukushige H, Hildebrand DF, Gan S (2002) Evidence supporting a role of jasmonic acid in Arabidopsis leaf senescence. Plant Physiol 128:876–884

    PubMed  CAS  Google Scholar 

  • Hu X, Neill S, Cai W, Tang Z (2003) Hydrogen peroxide and jasmonic acid mediate oligogalacturonic acid-induced saponin accumulation in suspension-cultured cells of Panax ginseng. Physiol Plant 118:414–421

    CAS  Google Scholar 

  • Irving HR, Dyson G, McConchie R, Parish RW, Gehring CA (1999) Effects of exogenously applied jasmonates on growth and intracellular pH in maize coleoptile segments. J Plant Growth Regul 18:93–100

    PubMed  CAS  Google Scholar 

  • Ivanov AG, Kicheva MI (1993) Chlorophyll fluorescence properties of chloroplast membranes isolated from jasmonic acid-treated barley seedlings. J Plant Physiol 141:410–414

    CAS  Google Scholar 

  • Jonak C, Nagkagami H, Hirt H (2004) Heavy metal stress. Activation of distinct mitogen-activated protein kinase pathways by copper and cadmium. Plant Physiol 136:3276–3283

    PubMed  CAS  Google Scholar 

  • Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol 53:299–328

    PubMed  CAS  Google Scholar 

  • Kim J-A, Agrawal GK, Rakwal R, Han K-S, Kim K-N, Yun Ch-H, Heu S, Park S-Y, Lee Y-H, Jwa N-S (2003) Molecular cloning and mRNA expression analysis of a novel rice (Oryza sativa L.) MAPK kinase kinase, OsEDR1, an ortholog of Arabidopsis AtEDR1, reveal its role in defense/stress signaling pathways and development. Bioch Biophys Res Commun 300:868–876

    CAS  Google Scholar 

  • Kopyra M, Gwóźdź EA (2004) The role of nitric oxide in plant growth regulation and responses to abiotic stresses. Acta Physiol Plant 26:459–472

    CAS  Google Scholar 

  • Kowalewska G, Falkowski L, Hoffmann SK, Szczepaniak L (1987) Replacement of magnesium by copper (II) in the chlorophyll porphyrin ring of planktonic algae. Acta Physiol Plant 9:43052

    Google Scholar 

  • Krupa Z, Baszyński T (1985) Effect of cadmium on the acyl lipid content and fatty acid comosition in thylakoid membranes isolated from tomato leaves. Acta Physiol Plant 2:55–64

    Google Scholar 

  • Krupa Z, Baszyński T (1995) Some aspects of heavy metals toxicity towards photosynthetic apparatus direct and indirect effects on light and dark reactions. Acta Physiol Plant 17:177–190

    CAS  Google Scholar 

  • Krupa Z, Siedlecka A, Maksymiec W, Baszyński T (1993) In vivo response of photosynthetic apparatus of Phaseolus vulgaris L. to nickel toxicity. J Plant Physiol 142:664–668

    CAS  Google Scholar 

  • Kruzmane D, Jankevica L, Ievinsh G (2002) Effect of regurgitant from Leptinotarsa decemlineata on wound responses in Solanum tuberosum and Phaseolus vulgaris. Physiol Plant 115:577–584

    PubMed  CAS  Google Scholar 

  • Lamb C, Dixon R (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48:251–275

    PubMed  CAS  Google Scholar 

  • Lin Ch-Ch, Chen L-M, Liu Z-H (2005) Rapid effect of copper on lignin biosynthesis in soybean roots. Plant Sci 168:855–861

    CAS  Google Scholar 

  • Linger P, Ostwald A, Haensel J (2005) Cannabis sativa L. growing on heavy metal contaminated soil: growth, cadmium uptake and photosynthesis. Biol Plant 49:567–576

    CAS  Google Scholar 

  • Liszkay A, Kenk B, Schopfer P (2003) Evidence for the involvement of cell wall peroxidase in the generation of hydroxyl radicals mediating extension growth. Planta 217:658–667

    PubMed  CAS  Google Scholar 

  • Maciejewska B, Kopcewicz J (2003) Inhibitory effect of methyl jasmonate on flowering and elongation growth in Pharbitis nil. J Plant Growth Regul 21:216–223

    Google Scholar 

  • Maksymiec W (1997) Effect of copper on cellular processes in higher plants. Photosynthetica 34:321–342

    CAS  Google Scholar 

  • Maksymiec W, Baszyński T (1988) The effect of Cd2+ on the release of proteins from thylakoid membranes of tomato leaves. Acta Soc Bot Pol 57:465–474

    CAS  Google Scholar 

  • Maksymiec W, Baszyński T (1996) Chlorophyll fluorescence in primary leaves of excess Cu-treated runner bean plants depends on their growth stages and the duration of Cu-action. J Plant Physiol 149:196–200

    CAS  Google Scholar 

  • Maksymiec W, Baszyński T (1998) The effect of Ca2+ on photosynthetic activity and assimilate distribution in Cu2+ stressed bean plants. In: Garab G (ed) Photosynthesis: mechanisms and effects. Kluwer, Dordrecht, pp 2669–2672

    Google Scholar 

  • Maksymiec W, Baszyński T (1999) Are calcium and calcium channels involved in the mechanisms of Cu2+ toxicity in bean plants? The influence of leaf age. Photosynthetica 36:267–278

    CAS  Google Scholar 

  • Maksymiec W, Russa R, Urbanik-Sypniewska T, Baszyński T (1994) Effect of excess Cu on the photosynthetic apparatus of runner bean leaves treated at two different growth stages. Physiol Plant 91:715–721

    CAS  Google Scholar 

  • Maksymiec W, Bednara J, Baszyński T (1995) Responses of runner plants to excess copper as a function of plant growth stages: effects on morphology and structure of primary leaves and their chloroplast ultrastructure. Photosynthetica 31:427–435

    CAS  Google Scholar 

  • Maksymiec W, Krupa Z (2002a) Jasmonate and heavy metals in Arabidopsis plants—a similar physiological response to both stressors? J Plant Physiol 159:509–515

    CAS  Google Scholar 

  • Maksymiec W, Krupa Z (2002b) The in vivo and in vitro influence of methyl jasmonate on oxidative processes in Arabidopsis thaliana leaves. Acta Physiol Plant 24:351–357

    CAS  Google Scholar 

  • Maksymiec W, Wianowska D, Dawidowicz AL, Radkiewicz S, Mardarowicz M, Krupa Z (2005) The level of jasmonic acid in Arabidopsis thaliana and Phaseolus coccineus plants under heavy metal stress. J Plant Physiol 162:1338–1346

    PubMed  CAS  Google Scholar 

  • Maksymiec W, Krupa Z (2006a) Effects of methyl jasmonate and excess copper on root and leaf growth. Biol Plant (In Press)

  • Maksymiec W, Krupa Z (2006b) The effects of short-term exposition to Cd, excess Cu ions and jasmonate on oxidative stress appearing in Arabidopsis thaliana. Environ Exp Bot 57:187–194

    CAS  Google Scholar 

  • Matto AK, Baker JE, Moline HE (1986) Induction by copper ions of ethylene production in Spirodela oligorrhiza: evidence for a pathway independent of a 1-aminocyclopropane-1-carboxylic acid. J Plant Physiol 123:193–202

    Google Scholar 

  • Merkouropoulos G, Shirsat AH (2003) The unusual Arabidopsis extensin gene atExt1 is expressed throughout plant development and is induced by a variety of biotic and abiotic stresses. Planta 217:356–366

    PubMed  Google Scholar 

  • Metwally A, Finkemeier I, Georgi M, Dietz KJ (2003) Salicylic acid alleviates the cadmium toxicity in barley seedlings. Plant Physiol 132:272–281

    PubMed  CAS  Google Scholar 

  • Mira H, Martinez N, Peñarrubia L (2002) Expression of vegetative-storage protein gene from Arabidopsis is regulated by copper, senescence and ozone. Planta 214:939–946

    PubMed  CAS  Google Scholar 

  • Mittra B, Ghosh P, Henry SL, Mishra J, Das TK, Ghosh S, Babu CR, Mohanty P (2004) Novel mode of resistance to Fusarium infection by a mild dose pre-exposure of cadmium in wheat. Plant Physiol Biochem 42:781–787

    PubMed  CAS  Google Scholar 

  • Molas J (2002) Changes of chloroplast ultrastructure and total chlorophyll concentration in cabbage leaves caused by excess of organic Ni(II) complexes. Environ Exp Bot 47:115–126

    CAS  Google Scholar 

  • Moya JL, Ros R, Picazo I (1993) Influence of cadmium and nickel on growth, net photosynthesis and carbohydrate distribution on rice plants. Photosynth Res 36:75–80

    CAS  Google Scholar 

  • Nasser W, de Tapia M, Burkard G (1990) Maize pathogenesis-related proteins: characterization and cellular distribution of 1,3-β-glucanases and chitinases induced by brome mosaic virus infection or mercury chloride treatment. Physiol Mol Plant Pathol 36:1–14

    CAS  Google Scholar 

  • Neill SJ, Desikan R, Clarke A, Hurs RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signaling molecules in plants. J Exp Bot 53:1237–1247

    PubMed  CAS  Google Scholar 

  • Nouairi I, Ammar WB, Yousef NB, Daoud DBM, Ghorbal NH, Zarrouk M (2006) Comparative study of cadmium effects on membrane lipid composition of Brassica juncea and Brassica napus leaves. Plant Sci 170:511–519

    CAS  Google Scholar 

  • Orozco-Cárdenas ML, Ryan CA (1999) Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proc Natl Acad Sci USA 96:6553–6557

    PubMed  Google Scholar 

  • Orozco-Cárdenas ML, Narváez-Vásquez J, Ryan CA (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 13:179–191

    PubMed  Google Scholar 

  • Ouzounidou G, Giamparova M, Moustakas M, Karataglis S (1995) Responses of maize (Zea mays L.) plants to copper stress. I. Growth Environ Exp Bot 35:167–176

    CAS  Google Scholar 

  • Papadakis AK, Roubelakis-Angelakis KA (1999) The generation of active oxygen species differs in tobacco and grapevine mesophyll protoplasts. Plant Physiol 121:197–205

    PubMed  CAS  Google Scholar 

  • 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 52:199–223

    CAS  Google Scholar 

  • Pei Z-M, Murata Y, Benning G, Thomine S, Klüsener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406:731–734

    PubMed  CAS  Google Scholar 

  • Pell EJ, Schlagnahaufer CD, Arteca RN (1997) Ozone-induced oxidative stress: mechanisms of action and reaction. Physiol Plant 100:264–273

    CAS  Google Scholar 

  • Pitta-Alvarez SI, Spollansky TC, Giulietti AM (2000) The influence of different biotic and abiotic elicitors on the production and profile of tropane alkaloids in hairy root cultures of Brugmansia candida. Enzym Microb Technol 26:252–258

    CAS  Google Scholar 

  • Poschenrieder C, Gunsé B, Barceló J (1989) Influence of cadmium on water relations, stomatal resistance, an abscisic acid content in expanding bean leaves. Plant Physiol 90:1365–1371

    Article  PubMed  CAS  Google Scholar 

  • Przymusiński R, Gwóźdź EA (1999) Heavy metal-induced polypeptides in lupin roots are similar to pathogenesis-related proteins. J Plant Physiol 154:703–708

    Google Scholar 

  • Quartacci MF, Cosi E, Navari-Izzo F (2001) Lipids and NADPH-dependent superoxide production in plasma membrane vesicles from roots of wheat grown under copper deficiency or excess. J Exp Bot 52:77–84

    PubMed  CAS  Google Scholar 

  • Radmer R, Kok B (1974) Kinetic observation of the system II electron acceptor pool isolated by mercury ion. Bioch Biophys Acta 337:177–180

    Google Scholar 

  • Rakwal R, Tomogami S, Kodama O (1996) Role of jasmonic acid as a signalling molecule in copper chloride-elicited rice phytoalexein production. Biosci Biotechnol Biochem 60:1046–1048

    Article  CAS  Google Scholar 

  • Rakwal R, Tomogami S, Agrawal GK, Iwahashi H (2002) Octadecanoid signaling component “burst” in rice (Oryza sativa L.) seedling leaves upon wounding by cut and treatment with fungal elicitor chitosan. Bioch Biophys Res Commun 295:1041–1045

    CAS  Google Scholar 

  • Razem FA, EL-Kereamy A, Abrams SR, Hill RD (2006) The RNA-binding protein FCA is an abscisic acid receptor. Nature 439:290–294

    PubMed  CAS  Google Scholar 

  • Rentel M, Knight MR (2004) Oxidative stress-induced calcium signaling in Arabidopsis. Plant Physiol 135:1471–1479

    PubMed  CAS  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

    CAS  Google Scholar 

  • Romero-Puertas MC, McCarthy I, Sandalio LM, Palma JM, Corpas FJ, Gomez M, del Rio LA (1999) Cadmium toxicity and antioxidative metabolism of pea leaf peroxisomes. Free Rad Res 31:25–31

    Google Scholar 

  • Romero-Puertas MC, Rodriquez-Serrano M, Corpas FJ, Gómez M, Del Rio LA, Sandalio LM (2004) Cadmium-induced subcellular accumulation of O −2 and H2O2 in pea leaves. Plant Cell Environ 27:1122–1134

    CAS  Google Scholar 

  • Rucińska R, Waplak S, Gwóźdź EA (1999) Free radical formation and activity of antioxidant enzymes in lupin roots exposed to lead. Plant Physiol Biochem 37:187–194

    Google Scholar 

  • Salin ML (1988) Toxic oxygen species and protective systems of the chloroplasts. Physiol Plant 72:681–689

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Sandmann G, Böger P (1980) Copper-mediated lipid peroxidation processes in photosynthetic membranes. Plant Physiol 66:797–800

    PubMed  CAS  Google Scholar 

  • Saniewski M, Ueda J, Miyamoto K (2002) Relationships between jasmonates and auxin in regulation of some physiological processes in higher plants. Acta Physiol Plant 24:211–220

    CAS  Google Scholar 

  • Saniewski M, Ueda J, Miyamoto K, Urbanek H (2003) Interaction between ethylene and other plant hormones in regulation of plant growth and development in natural conditions and under abiotic and biotic stresses. In: Vendrell M, Klee H, Pech JC, Romojaro F (eds) Biology and Biotechnology of the Plant Hormone Ethylene III, IOS Press, pp 263–270

  • Sanitá di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130

    Google Scholar 

  • Schaller F, Weiler EW (2002) Wound- and mechanical signalling. In: Scheel D, Wasternack C (eds) Plant signal transduction, Oxford University Press, Oxford, pp 20–44

    Google Scholar 

  • Scheer JM, Ryan CA (2002) The systemin receptor SR160 Lycopersicon peruvianum is a member of the LRR receptor kinase family. Proc Natl Acad Sci USA 99:9585–9590

    PubMed  CAS  Google Scholar 

  • Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365

    PubMed  Google Scholar 

  • Schützendübel A, Schwanz P, Teichmann T, Gross K, Langenfeld-Heyser R, Goldbold DL, Polle A (2001) Cadmium-induced changes in antioxidant systems, hydrogen peroxide content and differentiation in Scot pine roots. Plant Physiol 127:887–898

    PubMed  Google Scholar 

  • Showden KC, Richards KD, Gardner RC (1995) Aluminum-induced genes. Induction by toxic metals, low calcium and wounding and pattern of expression in root tips. Plant Physiol 107:341–348

    Google Scholar 

  • Siedlecka A (1995) Some aspects of interactions between heavy metals and plant mineral nutrients. Acta Soc Bot Pol 64:265–272

    CAS  Google Scholar 

  • Siedlecka A, Tukendorf A, Skórzyńska-Polit E, Maksymiec W, Wójcik M, Baszyński T, Krupa Z (2001) Angiosperms (Asteraceae, Convolvulaceae, Fabaceae and Poaceae, other than Brassicaceae). In: Prasad MNV (ed) Metals in the environment, Marcel Dekker, New York, pp 171–215

    Google Scholar 

  • Skórzyńska E, Baszyński T (1993) The changes in PSII complex polypeptides under cadmium treatment are they of direct or indirect nature. Acta Physiol Plant 15:263–269

    Google Scholar 

  • Skórzyńska-Polit E, Baszyński T (1997) Differences in the sensitivity of the photosynthetic apparatus in Cd-stressed runner bean plants in relation to their age. Plant Sci 128:11–21

    Google Scholar 

  • Skórzyńska E, Baszyński T (1998) The modifying effect of calcium on Cd-treated runner bean plants. The level of carbohydrates. In: Garab G (ed) Photosynthesis: mechanisms and effects, Kluwer, Dordrecht, pp 2673–2676

    Google Scholar 

  • Skórzyńska E, Baszyński T (2000) Does Cd2+ use Ca2+ channels to penetrate into chloroplast ?—a preliminary study. Acta Physiol Plant 22:171–178

    Google Scholar 

  • Sobkowiak R, Deckert J (2003) Cadmium-induced changes in growth and cell cycle gene expression in suspension-culture cells of soybean. Plant Physiol Biochem 41:767–772

    CAS  Google Scholar 

  • Somashekaraiah BV, Padmaja K, Prasad ARK (1992) Phytotoxicity of cadmium ions on germinating seedlings of mung bean (Phaseolus vulgaris): involvement of lipid peroxides in chlorophyll degradation. Physiol Plant 85:85–89

    CAS  Google Scholar 

  • Stepanova AN, Ecker JR (2000) Ethylene signaling: from mutants to molecules. Curr Opin Plant Biol 3:353–360

    PubMed  CAS  Google Scholar 

  • Stintzi A, Weber H, Reymond P, Browse J, Farmer EE (2001) Plant defense in the absence of jasmonic acid: the role of cyclopentanones. Proc Natl Acad Sci USA 98:12837–12842

    PubMed  CAS  Google Scholar 

  • Suhita D, Raghavendra AS, Kwak JM, Vasasseur A (2004) Cytoplasmic alkalization precedes reactive oxygen species production during methyl jasmonate- and abscisic acid-induced stomatal closure. Plant Physiol 134:1536–1545

    PubMed  CAS  Google Scholar 

  • Świątek A, Lenjou M, Van Bockstaele D, Inzé D, Van Onckelen H (2002) Differential effect of jasmonic acid and abscisic acid on cell cycle progression in tobacco BY-2 cells. Plant Physiol 128:201–211

    PubMed  Google Scholar 

  • Tewari RK, Kumar P, Sharma PN, Bisht SS (2002) Modulation of oxidative stress responsive enzymes by excess cobalt. Plant Sci 162:381–388

    CAS  Google Scholar 

  • Turner JG, Ellis Ch, Devoto A (2002) The jasmonate signal pathway. Plant Cell 14(Suppl):153–164

    Google Scholar 

  • Urao T, Yakubov B, Satoh R, Yamaguchi-Shinozaki K, Seki M, Hirayama T, Shinozaki K (2001) A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. Plant Cell 11:1743–1754

    Google Scholar 

  • Vassiliev A, Lidon F, Da Graca M, Yordanov I (2004) Cadmium-induced changes in chloroplast lipids and photosystem activities in barley plants. Biol Plant 48:153–156

    Google Scholar 

  • Vecchia FD, La Rocca N, Moro I, De Faveri S, Andreoli C, Rascio N (2005) Morphogenetic, ultrastructural and physiological damages by submerged leaves of Elodea Canadensis exposed to cadmium. Plant Sci 168:329–338

    Google Scholar 

  • Vierke G, Struckmeier P (1977) Binding of copper (II) to proteins of the photosynthetic membrane and its correlation with inhibition of electron transport in class II chloroplasts of spinach. Z Naturforsch 32c:605–610

    CAS  Google Scholar 

  • Vinit-Dunand F, Epron D, Alaoui-Sossé B, Badot P-M (2002) Effects of copper on growth and on photosynthesis of mature and expanding leaves in cucumber plants. Plant Sci 163:53–58

    CAS  Google Scholar 

  • Waisberg M, Joseph P, Hale B, Beyermann D (2003) Molecular and cellular mechanisms of cadmium carcinogenesis. Toxicology 192:95–117

    PubMed  CAS  Google Scholar 

  • Wang KL-C, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14(Suppl):131–151

    Google Scholar 

  • Weckx JEJ, Clijsters HMM (1996) Oxidative damage and defense mechanisms in primary leaves of Phaseolus vulgaris as a result of root assimilation of toxic amounts of copper. Physiol Plant 96:506–512

    CAS  Google Scholar 

  • Weckx JEJ, Clijsters HMM (1997) Zn phytotoxicity induces oxidative stress in primary leaves of Phaseolus vulgaris. Plant Physiol Biochem 35:405–410

    CAS  Google Scholar 

  • Wierzbicka M (1999) The effect of lead on the cell cycle in the root meristem of Allium cepa L. Protoplasma 207:186–194

    CAS  Google Scholar 

  • Wise RR, Naylor AW (1988) Stress ethylene does not originate directly from lipid peroxidation during chilling-enhanced photooxidation. J Plant Physiol 133:62–66

    CAS  Google Scholar 

  • Xiang C, Oliver DJ (1998) Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10:1539–1550

    PubMed  CAS  Google Scholar 

  • Xiao S, Dai L, Liu F, Wang Z, Peng W, Xie D (2004) COS1: an Arabidopsis coronatine insensitive 1 suppressor essential for regulation of jasmonate-mediated plant defense and senescence. Plant Cell 16:1132–1142

    PubMed  CAS  Google Scholar 

  • Xiong L, Schumaker KS, Zhu J-K (2002) Cell signaling during cold, drought and salt stress. Plant Cell 14(Suppl):165–183

    Google Scholar 

  • Yamauchi M, Peng XX (1995) Iron toxicity and stress-induced ethylene production in rice leaves. Plant Soil 173:21–28

    CAS  Google Scholar 

  • Yeh Ch-M, Hung W-Ch, Huang H-J (2003) Copper treatment activates mitogen-activated protein kinase signalling in rice. Physiol Plant 119:392–399

    CAS  Google Scholar 

  • Yun H-K, Yi S-H, Yu S-H, Choi D (1999) Cloning of a pathogenesis-related protein-1 gene from Nicotiana glutinosa L. and its salicylic acid-independent induction by copper and β-aminobutyric acid. J Plant Physiol 154:327–333

    CAS  Google Scholar 

  • Zhang Y, Chai T-Y, Dong J, Zhao W, An Ch-C, Chen Z-L, Burkard G (2001) Cloning and expression analysis of the heavy-metal responsive gene PvSR2 from bean. Plant Sci 161:783–790

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Plant Physiology, Maria Curie-Skłodowska University, Akademicka 19, 20-033, Lublin, Poland

    Waldemar Maksymiec

Authors
  1. Waldemar Maksymiec
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Waldemar Maksymiec.

Additional information

Communicated by P. Wojtaszek.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Maksymiec, W. Signaling responses in plants to heavy metal stress. Acta Physiol Plant 29, 177–187 (2007). https://doi.org/10.1007/s11738-007-0036-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11738-007-0036-3

Keywords

Search

Navigation