Abstract
Upon toxic metal stress numerous defence mechanisms have been induced, including the synthesis of metal-binding ligands and plant hormones or plant growth regulators in plants. As several elements in the promoter region of the heavy metal-responsive genes can be activated by plant hormones and growth regulators, understanding and revealing possible and special relationships between these regulator compounds and the metal chelator phytochelatins, which are in the first line of heavy metal defence mechanism is of great important. Phytochelatins are synthetized from glutathione and have a structure of [(γ-Glu-Cys)n]-Gly, where n is the number of repetition of the (γ-Glu-Cys) units. Evidences for the role of PCs in heavy metal tolerance are very strong; however, little information is available on how plant growth regulators influence the phytochelatin synthesis at molecular or even gene expression level. In the present review we provide an overview of the role and synthesis of phytochelatins in metal-tolerance mechanism from a new point of view, i.e. their relation to the plant growth regulator molecules, with special regard also on those cases, when close direct relationship exists because of the partly overlapped synthesis pathways of plant growth regulators and glutathione/phytochelatins.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- ABA:
-
Abscisic acid
- ACC:
-
1-Aminocyclopropane-1-carboxylic acid
- ACO:
-
ACC-oxidase
- ACS:
-
ACC-synthase
- BRs:
-
Brassinosteroids
- CKs:
-
Cytokinins
- dcSAM:
-
Decarboxylated S-adenosyl-methionine
- γ-GCS:
-
γ-Glutamyl-cysteine synthase
- GA:
-
Gibberelins
- GSH:
-
Glutathione
- GSS:
-
Glutathione synthase
- JA:
-
Jasmonic acid
- MeJA:
-
Methyl jamonic acid
- NaSA:
-
Sodium salicylate
- PA:
-
Polyamine
- PC:
-
Phytochelatin
- PCS:
-
Phytochelatin synthase
- PUT:
-
Putrescine
- SA:
-
Salicylic acid
- SAM:
-
S-adenosyl-methionine
- SPD:
-
Spermidine
- SPDS:
-
Spermidine synthase
- SPM:
-
Spermine
- SPMS:
-
Spermine synthase
References
Agrawal SB, Agrawal M, Lee EH et al (1992) Changes in polyamine and glutathione contents of a green alga, Chlorogonium elongatum (Dang) France exposed to mercury. Environ Exp Bot 32:145–151. https://doi.org/10.1016/0098-8472(92)90039-5
Ahmad P, Rasool S, Gul A et al (2016) Jasmonates: multifunctional roles in stress tolerance. Front Plant Sci 7:813. https://doi.org/10.3389/fpls.2016.00813
Ahmad P, Alyemeni MN, Wijaya L et al (2017) Jasmonic acid alleviates negative impacts of cadmium stress by modifying osmolytes and antioxidants in faba bean (Vicia faba L.). Arch Agron Soil Sci 63:1889–1899. https://doi.org/10.1080/03650340.2017.1313406
Al-Hakimi AMA (2007) Modification of cadmium toxicity in pea seedlings by kinetin. Plant Soil Environ 53:129–135
Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Gwóźdź EA (2011) The message of nitric oxide in cadmium challenged plants. Plant Sci 181:612–620. https://doi.org/10.1016/j.plantsci.2011.03.019
Arnao MB, Hernández-Ruiz J (2007) Melatonin promotes adventitious- and lateral root regeneration in etiolated hypocotyls of Lupinus albus L. J Pineal Res 42:147–152. https://doi.org/10.1111/j.1600-079X.2006.00396.x
Asgher M, Khan MIR, Anjum NA, Khan NA (2015) Minimising toxicity of cadmium in plants—role of plant growth regulators. Protoplasma 252:399–413
Astolfi S, Zuchi S, Passera C (2004) Role of sulphur availability on cadmium-induced changes of nitrogen and sulphur metabolism in maize (Zea mays L.) leaves. J Plant Physiol 161:795–802. https://doi.org/10.1016/j.jplph.2003.11.005
Bai X, Dong Y, Kong J et al (2015) Effects of application of salicylic acid alleviates cadmium toxicity in perennial ryegrass. Plant Growth Regul 75:695–706. https://doi.org/10.1007/s10725-014-9971-3
Bajguz A (2002) Brassinosteroids and lead as stimulators of phytochelatins synthesis in Chlorella vulgaris. J Plant Physiol 159:321–324. https://doi.org/10.1078/0176-1617-00654
Bajguz A (2010) An enhancing effect of exogenous brassinolide on the growth and antioxidant activity in Chlorella vulgaris cultures under heavy metals stress. Environ Exp Bot 68:175–179. https://doi.org/10.1016/j.envexpbot.2009.11.003
Begum MC, Islam M, Sarkar MR et al (2016) Auxin signaling is closely associated with Zn-efficiency in rice (Oryza sativa L.). J Plant Interact 11:124–129. https://doi.org/10.1080/17429145.2016.1220026
Bočová B, Huttová J, Mistrík I, Tamás L (2013) Auxin signalling is involved in cadmium-induced glutathione-S-transferase activity in barley root. Acta Physiol Plant 35:2685–2690. https://doi.org/10.1007/s11738-013-1300-3
Bruno L, Pacenza M, Forgione I et al (2017) In Arabidopsis thaliana cadmium impact on the growth of primary root by altering SCR expression and auxin-cytokinin cross-talk. Front Plant Sci 8:1323. https://doi.org/10.3389/fpls.2017.01323
Bücker-Neto L, Paiva ALS, Machado RD et al (2017) Interactions between plant hormones and heavy metals responses. Genet Mol Biol 40:373–386. https://doi.org/10.1590/1678-4685-gmb-2016-0087
Byeon Y, Lee HY, Hwang OJ et al (2015) Coordinated regulation of melatonin synthesis and degradation genes in rice leaves in response to cadmium treatment. J Pineal Res 58:470–478. https://doi.org/10.1111/jpi.12232
Cao S, Chen Z, Liu G et al (2009) The Arabidopsis ethylene-insensitive 2 gene is required for lead resistance. Plant Physiol Biochem 47:308–312. https://doi.org/10.1016/j.plaphy.2008.12.013
Cassina L, Tassi E, Morelli E et al (2011) Exogenous cytokinin treatments of an NI hyper-accumulator, Alyssum Murale, grown in a serpentine soil: implications for phytoextraction. Int J Phytoremed 13:90–101. https://doi.org/10.1080/15226514.2011.568538
Chang C (2016) Q&A: how do plants respond to ethylene and what is its importance? BMC Biol 14:7. https://doi.org/10.1186/s12915-016-0230-0
Chao YY, Chen CY, Huang WD, Kao CH (2010) Salicylic acid-mediated hydrogen peroxide accumulation and protection against Cd toxicity in rice leaves. Plant Soil 329:327–337. https://doi.org/10.1007/s11104-009-0161-4
Chen J, Zhou J, Goldsbrough PB (1997) Characterization of phytochelatin synthase from tomato. Physiol Plant 101:165–172. https://doi.org/10.1111/j.1399-3054.1997.tb01833.x
Cheng MC, Ko K, Chang WL et al (2015) Increased glutathione contributes to stress tolerance and global translational changes in Arabidopsis. Plant J 83:926–939. https://doi.org/10.1111/tpj.12940
Chmielowska-Bąk 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. https://doi.org/10.1016/j.jplph.2013.06.019
Chmielowska-Bąk J, Gzyl J, Rucińska-Sobkowiak R et al (2014) The new insights into cadmium sensing. Front Plant Sci 5:245. https://doi.org/10.3389/fpls.2014.00245
Choudhary SP, Bhardwaj R, Gupta BD et al (2010) Epibrassinolide induces changes in indole-3-acetic acid, abscisic acid and polyamine concentrations and enhances antioxidant potential of radish seedlings under copper stress. Physiol Plant 140:280–296. https://doi.org/10.1111/j.1399-3054.2010.01403.x
Choudhary SP, Kanwar M, Bhardwaj R et al (2011) Epibrassinolide ameliorates Cr(VI) stress via influencing the levels of indole-3-acetic acid, abscisic acid, polyamines and antioxidant system of radish seedlings. Chemosphere 84:592–600. https://doi.org/10.1016/j.chemosphere.2011.03.056
Choudhary SP, Kanwar M, Bhardwaj R et al (2012) Chromium stress mitigation by polyamine-brassinosteroid application involves phytohormonal and physiological strategies in Raphanus sativus L. PLoS ONE 7:e33210. https://doi.org/10.1371/journal.pone.0033210
Cobbett CS (2000) Phytochelatins and their roles in heavy metal detoxification. Plant Physiol 123:825–832. https://doi.org/10.1104/pp.123.3.825
Colebrook EH, Thomas SG, Phillips AL, Hedden P (2014) The role of gibberellin signalling in plant responses to abiotic stress. J Exp Biol 217:67–75. https://doi.org/10.1242/jeb.089938
D’Souza RM, Devaraj VR (2012) Induction of oxidative stress and antioxidative mechanisms in hyacinth bean under zinc stress. African Crop Sci J 20:17–29
De Benedictis M, Brunetti C, Brauer EK et al (2018) The Arabidopsis thaliana knockout mutant for phytochelatin synthase1 (cad1-3) is defective in callose deposition, bacterial pathogen defense and auxin content, but shows an increased stem lignification. Front Plant Sci 9:19. https://doi.org/10.3389/fpls.2018.00019
Dempsey DA, Klessig DF (2017) How does the multifaceted plant hormone salicylic acid combat disease in plants and are similar mechanisms utilized in humans? BMC Biol 15:23. https://doi.org/10.1186/s12915-017-0364-8
Di Toppi LS, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130. https://doi.org/10.1016/S0098-8472(98)00058-6
Di Toppi LS, Lambardi M, Pazzagli L et al (1998) Response to cadmium in carrot in vitro plants and cell suspension cultures. Plant Sci 137:119–129. https://doi.org/10.1016/S0168-9452(98)00099-5
Eckardt NA (2010) Redox regulation of auxin signaling and plant development. Plant Cell 22:295. https://doi.org/10.1105/tpc.110.220212
Emamverdian A, Ding Y, Mokhberdoran F, Xie Y (2015) Heavy metal stress and some mechanisms of plant defense response. Sci World J 2015:1–18. https://doi.org/10.1155/2015/756120
Fariduddin Q, Yusuf M, Ahmad I, Ahmad A (2014) Brassinosteroids and their role in response of plants to abiotic stresses. Biol Plant 58:9–17. https://doi.org/10.1007/s10535-013-0374-5
Farooq H, Asghar HN, Khan MY et al (2015) Auxin-mediated growth of rice in cadmium-contaminated soil. Turkish J Agric For 39:272–276. https://doi.org/10.3906/tar-1405-54
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. https://doi.org/10.1016/j.jplph.2004.11.015
Freeman JL, Garcia D, Kim D et al (2005) Constitutively elevated salicylic acid signals glutathione-mediated nickel tolerance in thlaspi nickel hyperaccumulators. Plant Physiol 137:1082–1091. https://doi.org/10.1104/pp.104.055293
Gemrotová M, Kulkarni MG, Stirk WA et al (2013) Seedlings of medicinal plants treated with either a cytokinin antagonist (PI-55) or an inhibitor of cytokinin degradation (INCYDE) are protected against the negative effects of cadmium. Plant Growth Regul 71:137–145. https://doi.org/10.1007/s10725-013-9813-8
Ghanta S, Datta R, Bhattacharyya D et al (2014) Multistep involvement of glutathione with salicylic acid and ethylene to combat environmental stress. J Plant Physiol 171:940–950. https://doi.org/10.1016/j.jplph.2014.03.002
Gondor OK, Pál M, Darkó É et al (2016) Salicylic acid and sodium salicylate alleviate cadmium toxicity to different extents in maize (Zea mays L.). PLoS ONE 11:e0160157. https://doi.org/10.1371/journal.pone.0160157
Groppa MD, Tomaro ML, Benavides MP (2001) Polyamines as protectors against cadmium or copper-induced oxidative damage in sunflower leaf discs. Plant Sci 161:481–488. https://doi.org/10.1016/S0168-9452(01)00432-0
Groppa MD, Tomaro ML, Benavides MP (2007) Polyamines and heavy metal stress: the antioxidant behavior of spermine in cadmium- and copper-treated wheat leaves. Biometals 20:185–195. https://doi.org/10.1007/s10534-006-9026-y
Guan C, Ji J, Wu D et al (2015) The glutathione synthesis may be regulated by cadmium-induced endogenous ethylene in Lycium chinense, and overexpression of an ethylene responsive transcription factor gene enhances tolerance to cadmium stress in tobacco. Mol Breed 35:1–13. https://doi.org/10.1007/s11032-015-0313-6
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. https://doi.org/10.1016/j.jplph.2008.01.002
Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11
Han Y, Mhamdi A, Chaouch S, Noctor G (2013) Regulation of basal and oxidative stress-triggered jasmonic acid-related gene expression by glutathione. Plant Cell Environ 36:1135–1146. https://doi.org/10.1111/pce.12048
Hasan MK, Ahammed GJ, Yin L et al (2015) Melatonin mitigates cadmium phytotoxicity through modulation of phytochelatins biosynthesis, vacuolar sequestration, and antioxidant potential in Solanum lycopersicum L. Front Plant Sci 6:601. https://doi.org/10.3389/fpls.2015.00601
Hayward AR, Coates KE, Galer AL et al (2013) Chelator profiling in Deschampsia cespitosa (L.) Beauv. Reveals a Ni reaction, which is distinct from the ABA and cytokinin associated response to Cd. Plant Physiol Biochem 64:84–91. https://doi.org/10.1016/j.plaphy.2012.12.018
Howden R, Goldsbrough PB, Andersen CR, Cobbett CS (1995) Cadmium-sensitive, cad1 mutants of Arabidopsis thaliana are phytochelatin deficient. Plant Physiol 107:1059–1066
Hsu YT, Kao CH (2003) Role of abscisic acid in cadmium tolerance of rice (Oryza sativa L.) seedlings. Plant Cell Environ 26:867–874. https://doi.org/10.1046/j.1365-3040.2003.01018.x
Hsu YT, Kao CH (2007) Cadmium-induced oxidative damage in rice leaves is reduced by polyamines. Plant Soil 291:27–37. https://doi.org/10.1007/s11104-006-9171-7
Hu YF, Zhou G, Na XF et al (2013) Cadmium interferes with maintenance of auxin homeostasis in Arabidopsis seedlings. J Plant Physiol 170:965–975. https://doi.org/10.1016/j.jplph.2013.02.008
Huang W-L, Lee C-H, Chen Y-R (2012) Levels of endogenous abscisic acid and indole-3-acetic acid influence shoot organogenesis in callus cultures of rice subjected to osmotic stress. Plant Cell Tissue Organ Cult 108:257–263. https://doi.org/10.1007/s11240-011-0038-0
Huda AKMN., Swaraz AM, Reza MA et al (2016) Remediation of chromium toxicity through exogenous salicylic acid in rice (Oryza sativa L.). Water Air Soil Pollut. https://doi.org/10.1007/s11270-016-2985-x
Inouhe M (2005) Phytochelatins. Braz J Plant Physiol 17:65–78. https://doi.org/10.1590/S1677-04202005000100006
Iqbal N, Masood A, Khan MIR et al (2013) Cross-talk between sulfur assimilation and ethylene signaling in plants. Plant Signal Behav 8:e22478. https://doi.org/10.4161/psb.22478
Janda T, Horváth E, Szalai G, Páldi E (2007) Role of salicylic acid in the induction of abiotic stress tolerance. In: Salicylic acid: a plant hormone. Springer, Dordrecht, pp 91–150
Jozefczak M, Remans T, Vangronsveld J, Cuypers A (2012) Glutathione is a key player in metal-induced oxidative stress defenses. Int J Mol Sci 13:3145–3175. https://doi.org/10.3390/ijms13033145
Kaminek M, Motyka V, Vankova R (1997) Regulation of cytokinin content in plant cells. Physiol Plant 101:689–700. https://doi.org/10.1034/j.1399-3054.1997.1010404.x
Kellős T, Tímár I, Szilágyi V et al (2008) Stress hormones and abiotic stresses have different effects on antioxidants in maize lines with different sensitivity. Plant Biol 10:563–572. https://doi.org/10.1111/j.1438-8677.2008.00071.x
Keunen E, Schellingen K, Vangronsveld J, Cuypers A (2016) Ethylene and metal stress: small molecule, big impact. Front Plant Sci 7:1–18. https://doi.org/10.3389/fpls.2016.00023
Khan MIR, Khan NA (2014) Ethylene reverses photosynthetic inhibition by nickel and zinc in mustard through changes in PSII activity, photosynthetic nitrogen use efficiency, and antioxidant metabolism. Protoplasma 251:1007–1019. https://doi.org/10.1007/s00709-014-0610-7
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. https://doi.org/10.1104/pp.107.113175
Koprivova A, Mugford ST, Kopriva S (2010) Arabidopsis root growth dependence on glutathione is linked to auxin transport. Plant Cell Rep 29:1157–1167. https://doi.org/10.1007/s00299-010-0902-0
Kovács V, Gondor OK, Szalai G et al (2014) Synthesis and role of salicylic acid in wheat varieties with different levels of cadmium tolerance. J Hazard Mater 280:12–19. https://doi.org/10.1016/j.jhazmat.2014.07.048
Krantev A, Yordanova R, Janda T et al (2008) Treatment with salicylic acid decreases the effect of cadmium on photosynthesis in maize plants. J Plant Physiol 165:920–931. https://doi.org/10.1016/j.jplph.2006.11.014
Lee S, Moon JS, Ko T-S et al (2003) Overexpression of Arabidopsis phytochelatin synthase paradoxically leads to hypersensitivity to cadmium stress. Plant Physiol 131:656–663. https://doi.org/10.1104/pp.014118
Li X, Yu B, Cui Y, Yin Y (2017) Melatonin application confers enhanced salt tolerance by regulating Na+ and Cl– accumulation in rice. Plant Growth Regul 83:441–454. https://doi.org/10.1007/s10725-017-0310-3
Lomozik L, Gasowska A, Bregier-Jarzebowska R, Jastrzab R (2005) Coordination chemistry of polyamines and their interactions in ternary systems including metal ions, nucleosides and nucleotides. Coord Chem Rev 249:2335–2350
Maksymiec W (2011) Effects of jasmonate and some other signalling factors on bean and onion growth during the initial phase of cadmium action. Biol Plant 55:112–118. https://doi.org/10.1007/s10535-011-0015-9
Maksymiec W, Krupa Z (2002) Jasmonic acid and heavy metals in Arabidopsis plants: a similar physiological response to both stressors? J Plant Physiol 159:509–515. https://doi.org/10.1078/0176-1617-00610
Maksymiec W, Wianowska D, Dawidowicz AL et al (2005) The level of jasmonic acid in Arabidopsis thaliana and Phaseolus coccineus plants under heavy metal stress. J Plant Physiol 162:1338–1346. https://doi.org/10.1016/j.jplph.2005.01.013
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. https://doi.org/10.1111/j.1365-3040.2011.02432.x
Merlos Rodrigo MA, Michálek P, Kryštofová O et al (2014) The role of phytochelatins in plant and animals: a review. J Met Nanotechnol 1:22–77
Metwally A, Finkemeier I, Georgi M, Dietz K-J (2003) Salicylic acid alleviates the cadmium toxicity in barley seedlings. Plant Physiol 132:272–281. https://doi.org/10.1104/pp.102.018457
Mohan TC, Castrillo G, Navarro C et al (2016) Cytokinin determines thiol-mediated arsenic tolerance and accumulation in Arabidopsis thaliana. Plant Physiol 171:00372. https://doi.org/10.1104/pp.16.003722016
Nahar K, Hasanuzzaman M, Alam MM et al (2016) Polyamine and nitric oxide crosstalk: antagonistic effects on cadmium toxicity in mung bean plants through upregulating the metal detoxification, antioxidant defense and methylglyoxal detoxification systems. Ecotoxicol Environ Saf 126:245–255. https://doi.org/10.1016/j.ecoenv.2015.12.026
Noctor G, Mhamdi A, Chaouch S et al (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35:454–484. https://doi.org/10.1111/j.1365-3040.2011.02400.x
Pal M, Horvath E, Janda T et al (2006) The effect of cadmium stress on phytochelatin, thiol and polyamine content in maize. Cereal Res Commun 34:65–68. https://doi.org/10.2307/23788895
Pál M, Horváth E, Janda T et al (2005) Cadmium stimulates the accumulation of salicylic acid and its putative precursors in maize (Zea mays) plants. Physiol Plant 125:356–364. https://doi.org/10.1111/j.1399-3054.2005.00545.x
Pál M, Horváth E, Janda T et al (2006) Physiological changes and defense mechanisms induced by cadmium stress in maize. J Plant Nutr Soil Sci 169:239–246. https://doi.org/10.1002/jpln.200520573
Pál M, Szalai G, Kovács V et al (2013) Salicylic acid-mediated abiotic stress tolerance. In: Hayat S, Ahmad A, AM (eds) Salicylic acid. Springer, Dordrecht, pp 183–247
Pál M, Szalai G, Janda T (2015) Speculation: polyamines are important in abiotic stress signaling. Plant Sci 237:16–23
Pál M, Csávás G, Szalai G et al (2017) Polyamines may influence phytochelatin synthesis during Cd stress in rice. J Hazard Mater 340:272–280. https://doi.org/10.1016/j.jhazmat.2017.07.016
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. https://doi.org/10.1046/j.1365-313X.2002.01442.x
Piotrowska A, Bajguz A, Godlewska-Zyłkiewicz B et al (2009) Jasmonic acid as modulator of lead toxicity in aquatic plant Wolffia arrhiza (Lemnaceae). Environ Exp Bot 66:507–513. https://doi.org/10.1016/j.envexpbot.2009.03.019
Piotrowska-Niczyporuk A, Bajguz A, Zambrzycka E, Godlewska-z̈yłkiewicz B (2012) Phytohormones as regulators of heavy metal biosorption and toxicity in green alga Chlorella vulgaris (Chlorophyceae). Plant Physiol Biochem 52:52–65. https://doi.org/10.1016/j.plaphy.2011.11.009
Poonam S, Kaur H, Geetika S (2013) Effect of jasmonic acid on photosynthetic pigments and stress markers in Cajanus cajan (L.) Millsp. Seedlings under copper stress. Am J Plant Sci 4:817–823. https://doi.org/10.4236/ajps.2013.44100
Rady MM, Osman AS (2012) Response of growth and antioxidant system of heavy metal-contaminated tomato plants to 24-epibrassinolide. Afr J Agric Res 7:3249–3254. https://doi.org/10.5897/AJAR12.079
Raines T, Shanks C, Cheng C-Y et al (2016) The cytokinin response factors modulate root and shoot growth and promote leaf senescence in Arabidopsis. Plant J 85:134–147. https://doi.org/10.1111/tpj.13097
Rajewska I, Talarek M, Bajguz A (2016) Brassinosteroids and response of plants to heavy metals action. Front Plant Sci 7:629. https://doi.org/10.3389/fpls.2016.00629
Schellingen K, Van Der Straeten D, Vandenbussche F et al (2014) Cadmium-induced ethylene production and responses in Arabidopsis thaliana rely on ACS2 and ACS6 gene expression. BMC Plant Biol 14:214. https://doi.org/10.1186/s12870-014-0214-6
Schellingen K, Van Der Straeten D, Remans T et al (2015) Ethylene signalling is mediating the early cadmium-induced oxidative challenge in Arabidopsis thaliana. Plant Sci 239:137–146. https://doi.org/10.1016/j.plantsci.2015.07.015
Singh S, Prasad SM (2014) Growth, photosynthesis and oxidative responses of Solanum melongena L. seedlings to cadmium stress: mechanism of toxicity amelioration by kinetin. Sci Hortic (Amsterdam) 176:1–10. https://doi.org/10.1016/j.scienta.2014.06.022
Singh I, Shah K (2014) Exogenous application of methyl jasmonate lowers the effect of cadmium-induced oxidative injury in rice seedlings. Phytochemistry 108:57–66. https://doi.org/10.1016/j.phytochem.2014.09.007
Singh S, Singh A, Bashri G, Prasad SM (2016) Impact of Cd stress on cellular functioning and its amelioration by phytohormones: an overview on regulatory network. Plant Growth Regul 80:253–263. https://doi.org/10.1007/s10725-016-0170-2
Sirhindi G, Mir MA, Abd-Allah EF et al (2016) Jasmonic acid modulates the physio-biochemical attributes, antioxidant enzyme activity, and gene expression in glycine max under nickel toxicity. Front Plant Sci 7:591. https://doi.org/10.3389/fpls.2016.00591
Sofo A, Vitti A, Nuzzaci M et al (2013) Correlation between hormonal homeostasis and morphogenic responses in Arabidopsis thaliana seedlings growing in a Cd/Cu/Zn multi-pollution context. Physiol Plant 149:487–498. https://doi.org/10.1111/ppl.12050
Stroiński A, Chadzinikolau T, Gizewska K, Zielezińska M (2010) ABA or cadmium induced phytochelatin synthesis in potato tubers. Biol Plant 54:117–120. https://doi.org/10.1007/s10535-010-0017-z
Stroiński A, Gizewska K, Zielezińska M (2013) Abscisic acid is required in transduction of cadmium signal to potato roots. Biol Plant 57:121–127. https://doi.org/10.1007/s10535-012-0135-x
Szalai G, Krantev A, Yordanova R et al (2013) Influence of salicylic acid on phytochelatin synthesis in Zea mays during Cd stress. Turk J Bot 37:708–714. https://doi.org/10.3906/bot-1210-6
Tajti J, Janda T, Majláth I et al (2018) Comparative study on the effects of putrescine and spermidine pre-treatment on cadmium stress in wheat. Ecotoxicol Environ Saf 148:546–554. https://doi.org/10.1016/j.ecoenv.2017.10.068
Tang CF, Liu YG, Zeng GM et al (2005) Effects of exogenous spermidine on antioxidant system responses of Typha latifolia L. under Cd2+ stress. J Integr Plant Biol 47:428–434. https://doi.org/10.1111/j.1744-7909.2005.00074.x
Tanou G, Ziogas V, Belghazi M et al (2014) Polyamines reprogram oxidative and nitrosative status and the proteome of citrus plants exposed to salinity stress. Plant Cell Environ 37:864–885. https://doi.org/10.1111/pce.12204
Tao S, Sun L, Ma C et al (2013) Reducing basal salicylic acid enhances Arabidopsis tolerance to lead or cadmium. Plant Soil 372:309–318. https://doi.org/10.1007/s11104-013-1749-2
Thao NP, Khan MI, Thu NB et al (2015) Role of ethylene and its cross talk with other signaling molecules in plant responses to heavy metal stress. Plant Physiol 169:73–84. https://doi.org/10.1104/pp.15.00663
Veselov D, Veselov D, Kudoyarova G et al (2003) Effect of cadmium on ion uptake, transpiration and cytokinin content in wheat seedlings. Bulg J Plant Physiol 29:353–359
Villiers F, Jourdain A, Bastien O et al (2012) Evidence for functional interaction between brassinosteroids and cadmium response in Arabidopsis thaliana. J Exp Bot 63:1185–1200. https://doi.org/10.1093/jxb/err335
Vishwakarma K, Upadhyay N, Kumar N et al (2017) Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Front Plant Sci 8:161. https://doi.org/10.3389/fpls.2017.00161
Wen X-P, Ban Y, Inoue H et al (2010a) Spermidine levels are implicated in heavy metal tolerance in a spermidine synthase overexpressing transgenic European pear by exerting antioxidant activities. Transgenic Res 19:91–103. https://doi.org/10.1007/s11248-009-9296-6
Wen XP, Ban Y, Inoue H et al (2010b) Spermidine levels are implicated in heavy metal tolerance in a spermidine synthase overexpressing transgenic European pear by exerting antioxidant activities. Transgenic Res 19:91–103. https://doi.org/10.1007/s11248-009-9296-6
Wójcik M, Tukendorf A (1999) Cd-tolerance of maize, rye and wheat seedlings. ACTA Physiol Plant 21:99–107. https://doi.org/10.1007/s11738-999-0063-3
Wu Z, Zhang C, Yan J et al (2015) Effects of sulfur supply and hydrogen peroxide pretreatment on the responses by rice under cadmium stress. Plant Growth Regul 77:299–306. https://doi.org/10.1007/s10725-015-0064-8
Xiang C, Oliver DJ (1998) Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10:1539–1550. https://doi.org/10.1105/tpc.10.9.1539
Yadav SK (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S Afr J Bot 76:167–179
Yamaguchi C, Ohkama-Ohtsu N, Shinano T, Maruyama-Nakashita A (2017) Plants prioritize phytochelatin synthesis during cadmium exposure even under reduced sulfate uptake caused by the disruption of SULTR1;2. Plant Signal Behav 12:e1325053
Yan Z, Zhang W, Chen J, Li X (2015) Methyl jasmonate alleviates cadmium toxicity in Solanum nigrum by regulating metal uptake and antioxidative capacity. Biol Plant 59:373–381. https://doi.org/10.1007/s10535-015-0491-4
Yuan H-M, Huang X (2016) Inhibition of root meristem growth by cadmium involves nitric oxide-mediated repression of auxin accumulation and signalling in Arabidopsis. Plant Cell Environ 39:120–135. https://doi.org/10.1111/pce.12597
Yun IIS, Hwang ID, Moon BY, Kwon YM (1997) Effect of spermine on the phytochelatin concentration and composition in cadmium-treated roots of Canavalia lineata seedlings. J Plant Biol 40:275–278. https://doi.org/10.1007/BF03030460
Zacchini M, Iori V, Mugnozza GS et al (2011) Cadmium accumulation and tolerance in. Biol Plant 55:383–386
Zagorchev L, Seal CE, Kranner I, Odjakova M (2013) A central role for thiols in plant tolerance to abiotic stress. Int J Mol Sci 14:7405–7432. https://doi.org/10.3390/ijms14047405
Zenk MH (1996) Heavy metal detoxification in higher plants: a review. Gene 179:21–30. https://doi.org/10.1016/S0378-1119(96)00422-2
Zhao Y (2010) Auxin biosynthesis and its role in plant development. Annu Rev Plant Biol 61:49–64. https://doi.org/10.1146/annurev-arplant-042809-112308
Zhao H, Yang H (2008) Exogenous polyamines alleviate the lipid peroxidation induced by cadmium chloride stress in Malus hupehensis Rehd. Sci Hortic (Amsterdam) 116:442–447. https://doi.org/10.1016/j.scienta.2008.02.017
Zhu YL, Pilon-Smits EA, Tarun AS et al (1999) Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing gamma-glutamylcysteine synthetase. Plant Physiol 121:1169–1178
Zhu XF, Wang ZW, Dong F et al (2013) Exogenous auxin alleviates cadmium toxicity in Arabidopsis thaliana by stimulating synthesis of hemicellulose 1 and increasing the cadmium fixation capacity of root cell walls. J Hazard Mater 263:398–403. https://doi.org/10.1016/j.jhazmat.2013.09.018
Acknowledgements
This work was supported by the grant of the National Research, Development and Innovation Office, KH 124472, which is gratefully acknowledged.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Pál, M., Janda, T. & Szalai, G. Interactions between plant hormones and thiol-related heavy metal chelators. Plant Growth Regul 85, 173–185 (2018). https://doi.org/10.1007/s10725-018-0391-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-018-0391-7