SpringerLink
Log in

ROS Signaling in Plants Under Heavy Metal Stress

  • Chapter
  • First Online:
Reactive Oxygen Species and Antioxidant Systems in Plants: Role and Regulation under Abiotic Stress

Abstract

Contamination of soil with toxic heavy metals is a major reason for retarded growth of crops and harmful effects on human health. Cultivation of large number of agricultural crops in contaminated soil is a major concern of environmentalist in the present times. Increased level of heavy metals can enter in to the food chain and may available for human consumption. Metal toxicity-induced oxidative stress eventually leads to refrained enzyme activities due to displacement of essential cofactors with other metal ions and blocking of functional groups such as carboxyl, histidyl and thiol, and proteins. Oxidative burst releases large quantities of reactive oxygen species (ROS) such as superoxide anion, hydrogen peroxide, hydroxyl radical, singlet oxygen, etc., which is one of the primary response of plants to heavy metal stress. Production of ROS is an inherent feature of plant cell and contributes to the process of oxidative damage leading to cell death. Its production is restricted to several cellular compartments such as mitochondria, chloroplast, and peroxisomes etc. ROS production leads to alteration of several physiological processes including degradation of enzymes, proteins, and amino acids and change in structure of cells. ROS are well described as secondary messengers in variety of cellular processes including acclimatization of cells to stress conditions. The signaling of ROS as a result of oxidative damage is regulated by several other signaling cascades which are interlinked. Their role has been studied under various stress conditions specifically heavy metals which leads to production of NO, H2O2, synthetic electrophilic compounds, lipid peroxidation molecules, etc.

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

Access this chapter

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
EUR 29.95
Price includes VAT (France)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
EUR 117.69
Price includes VAT (France)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
EUR 158.24
Price includes VAT (France)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info
Hardcover Book
EUR 158.24
Price includes VAT (France)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

Abbreviations

ǀO2 :

Superoxide radical

ABA:

Abscisic acid

ACC Synthase:

Aminocyclopropane-1-carboxylic acid synthase

APX:

Ascorbate peroxidase

As:

Arsenic

BRs:

Brassinosteroids

Ca:

Calcium

cADPR:

Cyclic ADP ribose

CAT:

Catalase

Cd:

Cadmium

CDPKs:

Calcium-dependent protein kinases

Co:

Cobalt

Cr:

Chromium

Cu:

Copper

DHAR:

Dehydroascorbate reductase

DNA:

Deoxyribonucleic acid

EBR:

24-Epibrassinolide

EGTA:

Ethylene Glycol-bis-aminoethyether-N,N,Nǀ,Nǀ tetra acetic acid

Fe:

Iron

GPX:

Glutathione peroxidase

GR:

Glutathione reductase

GSH:

Reduced glutathione

GSSG:

Oxidized glutathione

H2O:

Water

H2O2 :

Hydrogen peroxide

HSP:

Heat shock proteins

I:

Iodine

IAA:

Indole-3-acetic acid

IP3:

Inositol 1,4,5- triphosphate

K:

Potassium

LMWOAs:

Low molecular weight organic acids

LOX:

Lipoxygenase

MAPK:

Mitogen-activated protein kinase

MAPKK:

Mitogen-activated protein kinase kinase

MAPKKK:

Mitogen-activated protein kinase kinase kinase

MDA:

Malondialdehyde

MDHAR:

Monodehydroascorbate reductase

Mg:

Magnesium

miRNA:

MicroRNA

NADPH oxidase:

Nicotinamide adenine dinucleotide phosphate-oxidase

NO:

Nitric oxide

O2 :

Oxygen

O2.− :

Superoxide anion

OH:

Hydroxyl ion

OONO− :

Peroxynitrite

OXII:

Oxylipin

Pb:

Lead

PLD:

Phospholipase D

POD:

Peroxidases

PSI:

Photosystem I

PSII:

Photosystem II

ROS:

Reactive oxygen species

SNAP:

S-nitroso-N-acetyl-1,1-pencillamine

SNP:

Sodium nitroprusside

SOD:

Superoxide dismutase

V:

Vanadium

Zn:

Zinc

References

  • Ali B, Mwamba TM, Gill RA, Yang C, Ali S, Daud MK, Wu Y, Zhou W (2014) Improvement of element uptake and antioxidative defense in Brassica napus under lead stress by application of hydrogen sulfide. Plant Growth Regul 74:261–273

    Article  CAS  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  PubMed  Google Scholar 

  • Arasimowicz M, Floryszak-Wieczorek J (2007) Nitric oxide as a bioactive signaling molecule in plants stress responses. Plant Sci 172:876–887

    Article  CAS  Google Scholar 

  • Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Deckert J, Rucińska-Sobkowiak R, Gzyl J, Pawlak-Sprada S, Abramowski D, Jelonek T, Gwóźdź EA (2012) Nitric oxide implication in cadmium-induced programmed cell death in roots and signaling response of yellow lupine plants. Plant Physiol Biochem 58:124–134

    Article  CAS  PubMed  Google Scholar 

  • Asai S, Ichikawa T, Nomura H, Kobayashi M, Kamiyoshihara Y, Mori H et al (2013) The variable domain of a plant calcium-dependent protein kinase (CDPK) confers sub cellular localization and substrate recognition for NADPH oxidase. J Biol Chem 288:14332–14340

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Autreaux BD, Toledano MB (2007) ROS as signaling molecules: mechanisms that generate specificity in ROS homeostasis. Mol Cell Biol 8:813–824

    Google Scholar 

  • Ayano M, Kani T, Kojima M, Sakakibara H, Kitaoka T, Kuroha T, Angeles-Shim RB, Kitano H, Nagai K, Ashikari M (2014) Gibberellin biosynthesis and signal transduction is essential for internode elongation in deepwater rice. Plant Cell Environ 37:2313–2324

    CAS  PubMed Central  PubMed  Google Scholar 

  • Baliardini C, Meyer CL, Salis P, Saumitou-Laprade P, Verbruggen N (2015) CATIONEXCHANGER1 cosegregates with cadmium tolerance in the metal hyperaccumulator Arabidopsis halleri and plays a role in limiting oxidative stress in Arabidopsis Spp. Plant Physiol 169:549–559

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Begara-Morales JC, Sánchez-Calvo B, Luque F, Leyva-Pérez MO, Leterrier M, Corpas FJ, Barroso JB (2014) Differential transcriptomic analysis by RNA-Seq of GSNO-responsive genes between Arabidopsis roots and leaves. Plant Cell Physiol 55:1080–1095

    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  CAS  PubMed Central  PubMed  Google Scholar 

  • Bharwana SA, Ali S, Farooq MA, Farid M, Bashir N, Ahmad R (2016) Physiological and biochemical changes induced by lead stress in cotton (Gossypium hirsutum L.) seedlings. Acad J Agri Res 4:160–167

    Google Scholar 

  • Bhattacharjee S (2005) Reactive oxygen species and oxidative burst: roles in stress, senescence and signal transduction in plants. Curr Sci 89:1113–1121

    CAS  Google Scholar 

  • Bongiovanni GA, Soria FA, Eynard AR (2007) Effects of the plant flavonoids silymarin and quercetin on arsenite-induced oxidative stress in CHO-K1 cells. Food Chem Toxicol 45:971–976

    Article  CAS  PubMed  Google Scholar 

  • Bouche N, Yellin A, Snedden WA, Fromm H (2005) Plant-specific calmodulin-binding proteins. Annu Rev Plant Biol 56:435–466

    Article  CAS  PubMed  Google Scholar 

  • Broniowska KA, Hogg N (2012) The chemical biology of S-nitrosothiols. Antioxid Redox Signal 17:969–980

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Choudhary SP, Kanwar M, Bhardwaj R, Yu JQ, Tran LSP (2012a) Chromium stress mitigation by polyamine-brassinosteroid application involves phytohormonal and physiological strategies in Raphanus sativus L. PLoS One 7(3):e33210

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Choudhary SP, Oral HV, Bhardwaj R, Yu JQ, Tran LSP (2012b) Interaction of brassinosteroids and polyamines enhances copper stress tolerance in Raphanus sativus. J Exp Bot 63:5659–5675. doi:10.1093/jxb/ers219

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Contreras L, Mella D, Moenne A, Correa JA (2009) Differential responses to copper-induced oxidative stress in the marine macroalgae Lessonia nigrescens and Scytosiphon lomentaria (Phaeophyceae). Aquat Toxicol 94:94–102

    Article  CAS  PubMed  Google Scholar 

  • Corpas FJ, Alché JD, Barroso JB (2013) Current overview of S-nitrosoglutathione (GSNO) in higher plants. Front Plant Sci 4:126. doi:10.3389/fpls.2013.00126

    PubMed Central  PubMed  Google Scholar 

  • Corpas FJ, Barroso JB (2014) Peroxynitrite (ONOO−) is endogenously produced in Arabidopsis peroxisomes and is overproduced under cadmium stress. Ann Bot 113:87–96

    Article  CAS  PubMed  Google Scholar 

  • Corpas FJ, Barroso JB (2015) Functions of Nitric Oxide (NO) in roots during development and under adverse stress conditions. Plants 4:240–252. doi:10.3390/plants4020240

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Costa A, Drago I, Behera S, Zottini M, Pizzo P, Schroeder JI et al (2010) H2O2 in plant peroxisomes: an in vivo analysis uncovers a Ca2+-dependent scavenging system. Plant J 62:760–772

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cuypers A, Hendrix S, dos Reis RA, Smet SD, Deckers J, Giel H, Jozefczak M, Loix C, Vercampt H, Vangronsveld J, Keunen E (2016) Hydrogen peroxide, signaling in disguise during metal phytotoxicity. Front Plant Sci 7:1–25

    Article  Google Scholar 

  • Danon A, Miersch O, Felix G, Camp RG, Apel K (2005) Concurrent activation of cell death-regulating signalling pathways by singlet oxygen in Arabidopsis thaliana. Plant J 41:68–80

    Article  CAS  PubMed  Google Scholar 

  • Das R, Pandey GK (2010) Expressional analysis and role of calcium regulated kinases in abiotic stress signaling. Curr Genomics 11:2–13

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2:53. doi:10.3389/fenvs.2014.00053

    Article  Google Scholar 

  • De Michele R, Vurro E, Rigo C, Costa A, Elviri L, Di Valentin M, Careri M, Zottini M, Sanità di Toppi L, Lo Schiavo F (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 

  • del Río LA (2015) ROS and RNS in plant physiology: an overview. J Exp Bot 66:2827–2837

    Article  PubMed  CAS  Google Scholar 

  • Ding HD, Zhang XH, Xu SC, Sun LL, Jiang MY, Zhang AY, ** YG (2009) Induction of protection against paraquat-induced oxidative damage by abscisic acidin maize leaves is mediated through mitogen-activated protein kinase. J Integr Plant Biol 51:961–972

    Article  CAS  PubMed  Google Scholar 

  • Dodd AN, Kudla J, Sanders D (2010) The language of calcium signaling. Annu Rev Plant Biol 61:593–620

    Article  CAS  PubMed  Google Scholar 

  • Dong Y, Xu L, Wang Q, Fan Z, Kong J, Bai X (2014) Effects of exogenous nitric oxide on photosynthesis, antioxidative ability, and mineral element contents of perennial ryegrass under copper stress. J Plant Interact 9:402–411

    Article  CAS  Google Scholar 

  • Duan XLX, Ding F, Zhao J, Guo A, Zhang L, Yao J, Yang Y (2015) Interaction of nitric oxide and reactive oxygen species and associated regulation of root growth in wheat seedlings under zinc stress. Ecotoxicol Environ Saf 113:95–102

    Article  CAS  PubMed  Google Scholar 

  • Erguuml N, Oncel I (2012) Effects of some heavy metals and heavy metal hormone interactions on wheat (Triticum aestivum L. cv. Gun 91) seedlings. Afri J Agri Res 7:1518–1523

    Google Scholar 

  • Fischer BB, Krieger-Liszkay A, Hideg E, Šnyrychová I, Wiesendanger M, Eggen RIL (2011) Role of singlet oxygen in chloroplast to nucleus retrograde signaling in Chlamydomonas reinhardtii. FEBS Let 581:5555–5560

    Article  CAS  Google Scholar 

  • Flora SJS, Mittal M, Mehta A (2008) Heavy metal induced oxidative stress & its possible reversal by chelation therapy. Indian J Med Res 128:501–523

    CAS  PubMed  Google Scholar 

  • Foroozesh P, Bahmani R, Pazouki A, Asgharzadeh A, Rahimdabbagh S, Ahmadvand S (2012) Effect of cadmium stress on antioxidant enzymes activity in different bean genotypes. J Agri Biol Sci 7:351–356

    Google Scholar 

  • Foyer CH, Noctor G (2005) Oxidant and antioxidant signaling in plants: are-evaluation of concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071

    Article  CAS  Google Scholar 

  • Fusco N, Micheletto L, Dal Corso G, Borgato L, Furini A (2005) Identification of cadmium-regulated genes by cDNA-AFLP in the heavy metal accumulator Brassica juncea L. J Exp Bot 56:3017–3027

    Article  CAS  PubMed  Google Scholar 

  • Gadjev I, Vanderauwera S, Gechev TS, Laloi C, Minkov IN, Shulaev V, Apel K, Inze D, Mittler R, Van Breusegem F (2006) Transcriptomic footprints disclose specificity of reactive oxygen species signalling in Arabidopsis. Plant Physiol 141:436–445

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Garnier L, Simon-Plas F, Thuleau P, Agnel JP, Blein JP, Ranjeva R et al (2006) Cadmium affects tobacco cells by a series of three waves of reactive oxygen species that contribute to cytotoxicity. Plant Cell Environ 29:1956–1969

    Article  CAS  PubMed  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  PubMed  Google Scholar 

  • Gill RA, Ali B, Islam F, Farooq MA, Gill MB, Mwamba TM, Zhou W (2015) Physiological and molecular analyses of black and yellow seeded Brassica napus regulated by 5-aminolivulinic acid under chromium stress. Plant Physiol Biochem 94:130–143

    Article  CAS  PubMed  Google Scholar 

  • Glatz A, Vass I, Los DA, Vigh L (1999) The synechocystis model of stress: from molecular chaperones to membranes. Plant Physiol Biochem 37:1–12

    Article  CAS  Google Scholar 

  • Gommers CMM, Visser EJW, St Onge KR, Voesenek LACJ, Pierik R (2013) Shade tolerance: when growing tall is not an option. Trends Plant Sci 18:65–71. doi:10.1016/j.tplants.2012.09.008

    Article  CAS  PubMed  Google Scholar 

  • González A, Cabrera M, Henríquez MJ, Contreras RA, Morales B, Moenne A (2012) Crosstalk among calcium, hydrogen peroxide and nitric oxide and activation of gene expression involving calmodulins and calcium-dependent protein kinases in Ulva compressa exposed to copper excess. Plant Physiol 158:1451–1462

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Gropa MD, Rosales EP, Lannone MF, Benavides MP (2008) Nitric oxide, polyamines and Cd induced phytotoxicity in wheat roots. Phytochemistry 69:2609–2615

    Article  CAS  Google Scholar 

  • Groß F, Dumer J, Gaupels F (2013) Nitricoxide, antioxidants and prooxidants in plant defence responses. Front Plant Sci 29:419. doi:10.3389/fpls.2013.00419

    Google Scholar 

  • Gupta M, Sharma P, Sarin N, Sinha AK (2009) Differential response of arsenic stress in two varieties of Brassicajuncea L. Chemosphere 74:1201–1208

    Article  CAS  PubMed  Google Scholar 

  • Gupta DK, Pena LB, Romero-Puertas MC, Hernández A, Inouhe M, Sandalio LM (2016) NADPH oxidases differentially regulate ROS metabolism and nutrient uptake under cadmium toxicity. Plant Cell Environ. doi:10.1111/pce.12711

  • Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hanaka A, Wójcik M, Dresler S, Mroczek-Zdyrska M, Maksymiec W (2016) Does methyl jasmonate modify the oxidative stress response in Phaseolus coccineus treated with Cu? Ecotoxicol Environ Saf 124:480–488

    Article  CAS  PubMed  Google Scholar 

  • Hansch R, Mendel RR (2009) Physiological functions mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Curr Opin Plant Biol 12:259–266

    Article  PubMed  CAS  Google Scholar 

  • Hayat S, Ali B, Aiman Hasan S, Ahmad A (2007) Brassinosteroid enhanced the level of antioxidants under cadmium stress in Brassica juncea. Environ Exp Bot 60(1):33–41

    Article  CAS  Google Scholar 

  • Hu KD, Hu LY, Li YH, Zhang FQ, Zhang H (2007) Protective roles of nitric oxide on germination and antioxidant metabolism in wheat seeds under copper stress. Plant Growth Regul 53:173–183

    Article  CAS  Google Scholar 

  • Hu YL, Ge Y, Zhang CH, Ju T, Cheng WD (2009) Cadmium toxicity and translocation in rice seedlings are reduced by hydrogen peroxide pre-treatment. Plant Growth Regul 59:51–61

    Article  CAS  Google Scholar 

  • Huang TL, Huang HJ (2008) ROS and CDPK-like kinase-mediated activation of MAP kinase in rice roots exposed to lead. Chemosphere 71:1377–1385

    Article  CAS  PubMed  Google Scholar 

  • Huang D, Wu W, Abrams SR, Cutler AJ (2008) The relationship of drought related gene expression in Arabidopsis thaliana to hormonal and environmental factors. J Exp Bot 59:2991–3007

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hughes MF (2002) Arsenic toxicity and potential mechanisms of action. Toxicol Lett 133:1–16

    Article  CAS  PubMed  Google Scholar 

  • Jajic I, Sarna T, Strzalka K (2015) Senescence, stress, and reactive oxygen species. Plants 4:393–411

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jaspers P, Kandasjarvi J (2010) Reactive oxygen species in abiotic stress signalling. Physiol Plant 138:405–413

    Article  CAS  PubMed  Google Scholar 

  • Jonak C, Nakagami H, Hirt H (2004) Heavy metal stress. Activation of distinct mitogen-activated protein kinase pathways by copper and cadmium. Plant Physiol 136(2):3276–3283

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Joshi RK, Kar B, Nayak S (2011) Characterization of mitogenactivated protein kinases (MAPKs) in the Curcuma longa expressed sequence tag database. Bioinformation 7:180–183

    Article  PubMed Central  PubMed  Google Scholar 

  • Karuppanapandian T, Kim W (2013) Cobalt-induced oxidative stress causes growth inhibition associated with enhanced lipid peroxidation and activates antioxidant responses in Indian mustard (Brassica juncea L.) leaves. Acta Physiol Plant 35:2429–2443

    Article  CAS  Google Scholar 

  • 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. doi:10.1007/s00709-014-0610-7

    Article  CAS  PubMed  Google Scholar 

  • Khan TA, Mazid M, da Silva JAT, Mohammad F, Khan MN (2014) Role of NO-mediated signaling under abiotic stress (heavy metal)-induced oxidative stress in plants: An overview. Fun Plant Sci Biotech 6:91–107

    Google Scholar 

  • Kim C, Meskauskiene R, Apel K, Laloi C (2008) No single way to understand singlet oxygen signaling in plants. EMBO Rep 9:435–439

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kobayashi M, Yamamoto M (2006) Nrf2-keap1 regulation of cellular defense mechanism against electrophiles and reactive oxygen species. Adv Enzym Regul 46:113–140

    Article  CAS  Google Scholar 

  • Kobayashi M, Ohura I, Kawakita K, Yokota N, Fujiwara M, Shimamoto K et al (2007) Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19:1065–1080

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kochevar IE (2004) Singlet oxygen signaling: from intimate to global. Sci STKE 2004:e7

    Google Scholar 

  • Kopyra M, Stachon-Wilk M, Gwó’zd’z EA (2006) Effects of exogenous nitric oxide on the antioxidant capacity of cadmium-treated soybean cell suspension. Acta Physiol Plant 28:525–536

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kudla J, Batistic O, Hashimoto K (2010) Calcium signals: the lead currency of plant information processing. Plant Cell 22:541–563

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kurepin LV, Ivanov AG, Zaman M, Pharis RP, Allakhverdiev SI, Hurry V, Hüner NPA (2015) Stress-related hormones and glycinebetaine interplay in protection of photosynthesis under abiotic stress conditions. Photosynth Res. doi:10.1007/s11120-015-0125-x

  • Laloi C, Przybyla D, Apel K (2006) A genetic approach towards elucidating the biological activity of different reactive oxygen species in Arabidopsis thaliana. J Exp Bot 57:1719–1724

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lee KP, Kim C, Landgraf F, Apel K (2007) EXECUTER-1 and EXECUTER-2 dependent transfer of stress related signals from the plastid to the nucleus of Arabidopsis thaliana. Proc Nat Acad Sci USA 104:10270–10275

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Leterrier M, Airaki M, Palma JM, Chaki M, Barroso JB, Corpas FJ (2012) Arsenic triggers the nitric oxide (NO) and S-nitrosoglutathione (GSNO) metabolism in Arabidopsis. Environ Pollut 166:136–143

    Article  CAS  PubMed  Google Scholar 

  • Li DH, Yuan Y (2016) Hydrogen peroxide enhances antioxidative defense in the leaves of water caltrop (Trapa bicornis) seedlings treated with lead. Biologia 71:100–108

    CAS  Google Scholar 

  • Li A, Wang X, Leseberg CH, Jia J, Mao L (2008) Biotic and abiotic stress responses through calcium-dependent protein kinase (CDPK) signaling in wheat (Triticum aestivumL.) Plant Signal Behav 3:654–656

    Article  PubMed Central  PubMed  Google Scholar 

  • Lin YF, Aarts MG (2012) The molecular mechanism of zinc and cadmium stress response in plants. Cell Mol Life Sci 69:3187–3206

    Article  CAS  PubMed  Google Scholar 

  • Liu XM, Kim KE, Kim KC, Nguyen XC, Han HJ, Jung MS (2010) Cadmium activates Arabidopsis MPK3 and MPK6 via accumulation of reactive oxygen species. Phytochemistry 71:614–618

    Article  CAS  PubMed  Google Scholar 

  • Lombardi L, Sebastian L (2015) Copper toxicity in Prunus cerasifera: growth and antioxidant 715 enzymes responses of in vitro grown plants. Plant Sci 168:797–802

    Google Scholar 

  • Maheshwari R, Dubey RS (2009) Nickel-induced oxidative stress and the role of antioxidant defence in rice seedlings. Plant Growth Regul 59:37–49

    Article  CAS  Google Scholar 

  • Maksimovic’ JD, Mojovic’ M, Maksimovic’ V, Römheld V, Nikolic M (2012) Silicon ameliorates manganese toxicity in cucumber by decreasing hydroxyl radical accumulation in the leaf apoplast. J Exp Bot 63:2411–2420

    Article  CAS  Google Scholar 

  • Manara A (2012) Plant responses to heavy metal toxicity. In: Furini A (ed) Plants and heavy 722 metals. Springer briefs in biometals. Springer, New York, pp 27–53

    Google Scholar 

  • Mazars C, Thuleau P, Lamotte O, Bourque S (2010) Cross-talk between ROS and calcium in regulation of nuclear activities. Mol Plant 3:706–718

    Article  CAS  PubMed  Google Scholar 

  • McAinsh MR, Pittman JK (2009) Sha** the calcium signature. New Phytol 181:275–294

    Article  CAS  PubMed  Google Scholar 

  • McCormack E, Tsai YC, Braam J (2005) Handling calcium signaling: Arabidopsis CaMs and CMLs. Trends Plant Sci 10:383–389

    Article  CAS  PubMed  Google Scholar 

  • Mediouni C, Benzarti O, Tray B, Ghorbel MH, Jemal F (2006) Cadmium and copper toxicity for tomato seedlings. Agr Sustan Devel 26:227–232

    Article  CAS  Google Scholar 

  • Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467

    Article  CAS  PubMed  Google Scholar 

  • Mishra S, Jha AB, Dubey RS (2011) Arsenite treatment induces oxidative stress, upregulates antioxidant system, and causes phytochelatin synthesis in rice seedlings. Protoplasma 248:565–577

    Article  CAS  PubMed  Google Scholar 

  • Moan J (1990) On the diffusion length of singlet oxygen in cells and tissues. J Photochem Photobiol 6:343–344

    Article  CAS  Google Scholar 

  • Moller IM, Sweetlove LJ (2010) ROS signaling-specificity is required. Trends Plant Sci 7:370–374

    Article  CAS  Google Scholar 

  • Montero-Palmero MB, Martín-Barranco A, Escobar C, Hernández LE (2014a) Early transcriptional responses to mercury: a role for ethylene in mercury-induced stress. New Phytol 201:116–130

    Article  CAS  PubMed  Google Scholar 

  • Montero-Palmero MB, Ortega-Villasante C, Escobar C, Hernández LE (2014b) Are plant endogenous factors like ethylene modulators of the early oxidative stress induced by mercury? Environ Toxicol 2:34

    Google Scholar 

  • Mostofa MG, Hossain MA, Fujita M, Tran LSP (2015) Physiological and biochemical mechanisms associated with trehalose-induced copper-stress tolerance in rice. Sci Rep 5:11433. doi:10.1038/srep11433

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Munne-Bosch S, Queval G, Foyer CH (2013) The impact of global change factors on redox signaling under pinning stress tolerance. Plant Physiol 161:5–19

    Article  CAS  PubMed  Google Scholar 

  • Nathan C (2003) Specificity of a third kind: reactive oxygen and nitrogen intermediates in cell signaling. J Clin Invest 111:769–778

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Niedre M, Patterson MS, Wilson BC (2002) Direct near-infrared luminescence detection of singlet oxygen generated by photodynamic therapy in cells in vitro and tissues in vivo. J Photochem Photobiol 75:382–391

    Article  CAS  Google Scholar 

  • Ochsenbein C, Przybyla D, Danon A, Landgraf F, Gobel C, Imboden A, Feussner I, Apel K (2006) The role of EDS1 (enhanced disease susceptibility) during singlet oxygen-mediated stress responses of Arabidopsis. Plant J 47:445–456

    Article  CAS  PubMed  Google Scholar 

  • Ogasawara Y, Kaya H, Hiraoka G, Yumoto F, Kimura S, Kadota Y et al (2008) Synergistic activation of the Arabidopsis NADPH oxidase AtrbohD by Ca2+ and phosphorylation. J Biol Chem 283:8885–8892

    Article  CAS  PubMed  Google Scholar 

  • Op den Camp RG (2003) Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15:2320–2332

    Article  CAS  Google Scholar 

  • Opdenakker K, Remans T, Vangronsveld J, Cuypers A (2012) Mitogen – Activated Protein (MAP) kinases in plant metal stress: regulation and responses in comparison to other biotic and abiotic stresses. Int J Mol Sci 13:7828–7853

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Palmieri MC, Sell S, Huang X et al (2008) Nitric oxide-responsive genes and promoters in Arabidopsis thaliana: a bioinformatics approach. J Exp Bot 59:177–186

    Article  CAS  PubMed  Google Scholar 

  • Patsikka E, Aro EM, Tyystjärvi E (1998) Increase in the quantum yield of photo inhibition contributes to copper toxicity in vivo. Plant Physiol 117:619–627

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Penarrubia L, Romero P, Carrio-Segui A, Andres-Bordería A, Moreno J, Sanz A (2015) Temporal aspects of copper homeostasis and its crosstalk with hormones. Front Plant Sci 6:255. doi:10.3389/fpls.2015.00255

    Article  PubMed Central  PubMed  Google Scholar 

  • Pesko M, Král’ová A (2013) Physiological response of Brassica napus L. plants to Cu (II) treatment. Proceedings of ECOpole 7:155–161

    CAS  Google Scholar 

  • Qiaoa W, Li C, Fan LM (2013) Cross-talk between nitric oxide and hydrogen peroxide in plant responses to abiotic stresses. Environ Exp Bot 100:84–93

    Article  CAS  Google Scholar 

  • Radi R (2013) Peroxynitrite, a stealthy biological oxidant. J Biol Chem 288:26464–26472

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Raina SK, Wankhede DP, Sinha AK (2013) Catharanthus roseus mitogen-activated protein kinase 3 confers UV and heat tolerance to Saccharomyces cerevisiae. Plant Signal Behav 8:1

    Article  CAS  Google Scholar 

  • Rao KP, Richa T, Kumar K, Raghuram B, Sinha AK (2010) In silico analysis reveals 75 members of mitogen-activated protein kinase kinase kinase gene family in rice. DNA Res 17:139–153

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rao KP, Vani G, Kumar K, Wankhede DP, Misra M, Gupta M, Sinha AK (2011) Arsenic stress activates MAP kinase in rice roots and leaves. Arch Biochem Biophys 506:73–82

    Article  CAS  PubMed  Google Scholar 

  • Remans T, Opdenakker K, Smeets K, Mathijsen D, Vangronsveld J, Cuypers A (2010) Metal-specific and NADPH oxidase dependent changes in lipoxygenase and NADPH oxidase gene expression in Arabidopsis thaliana exposed to cadmium or excess copper. Funct Plant Biol 37:532–544

    Article  CAS  Google Scholar 

  • Rentel MC, Lecourieux D, Ouaked F, Usher SL, Petersen L, Okamoto H et al (2004) OXI1 kinase is necessary for oxidative burst-mediated signaling in Arabidopsis. Nature 427:858–861

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez MC, Petersen M, Mundy J (2010) Mitogen activated protein kinase signaling in plants. Annu Rev Plant Biol 6:621–649

    Google Scholar 

  • Rodríguez-Serrano M, Romero-Puertas MC, Pazmino DM, Testillano PS, Risueno MC, Luis A, 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 

  • Roel GL, Przybyla D, Ochsenbein C, Laloi C, Kim C, Danon A, Wagner D, Hideg E, Göbel C, Feussner I, Nater M, Apel K (2003) Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15:2320–2332

    Article  CAS  Google Scholar 

  • Romero-Puertas MC, Rodriguez-Serrano M, Corpas FJ, Gomez M, Del Rio LA, Sandalio LM (2004) Cadmium-induced subcellular accumulation of O2 ·−and H2O2 in pea leaves. Plant Cell Environ 27:1122–1134

    Article  CAS  Google Scholar 

  • Sablina AA, Budanov AV, Llyinskaya GV, Aqapova LS, Kravchenko JE, Chumakov PM (2005) The antioxidant function of p53 tumor suppressor. Nat Med 11:1306–1313

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sagi M, Fluhr R (2006) Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol 141:336–340

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Šamajová O, Plíhal O, Al-Yousif M, Hirt H, Šamaj J (2013) Improvement of stress tolerance in plants by genetic manipulation of mitogen-activated protein kinases. Bioteh Adv 31:118–128

    Article  CAS  Google Scholar 

  • Saniewski M, Ueda J, Miyamoto K, Urbanek H (2003) Interactions 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, Amsterdam, pp 263–270

    Google Scholar 

  • Scandalios JG (2005) Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Braz J Med Biol Res 38:995–1014

    Article  CAS  PubMed  Google Scholar 

  • Schellingen K, Van Der Straeten D, Remans T, Loix C, Vangronsveld J, Cuypers A (2015) Ethylene biosynthesis is involved in the early oxidative challenge induced by moderate Cd exposure in Arabidopsis thaliana. Environ Exp Bot 117:1–11

    Article  CAS  Google Scholar 

  • Schulz P, Herde M, Romeis T (2013) Calcium-dependent protein kinases: hubs in plant stress signaling and development. Plant Physiol 163:523–530

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Sewelam N, Kazan K, Schenk PM (2016) Global plant stress signaling: reactive oxygen species at the cross-road. Front Plant Sci 7:1–21

    Article  Google Scholar 

  • Sharma SS, Dietz KJ (2009) The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci:144–150

    Google Scholar 

  • Sharma RK, Devi S, dan Dhyani PP (2010) Comparative assessment of the toxic effects of copper and cypermethrin using seeds of Spinacia Oleracea L. plants. Trop Ecol 51:375–387

    Google Scholar 

  • Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage and antioxidative defense mechanism in plants under stressful conditions. J Bot Article ID 217037 1–26

    Google Scholar 

  • Shi H, Ye T, Zhu JK, Chan Z (2014) Constitutive production of nitric oxide leads to enhanced drought stress resistance and extensive transcriptional reprogramming in Arabidopsis. J Exp Bot 65:4119–4131

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Singh HP, Kaur S, Batish DR, Sharma VP, Sharma N, Kohli RK (2009) Nitric oxide alleviates arsenic toxicity by reducing oxidative damage in the roots of Oryza sativa (rice). Nitric Oxide 20:289–297

    Article  CAS  PubMed  Google Scholar 

  • Sinha AK, Jaggi M, Raghuram B, Tuteja N (2011) Mitogen activated protein kinase signaling in plants under abiotic stress. Plant Signal Behav 6:196–203

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sinha P, Shukla AK, Sharma YK (2015) Amelioration of heavy-metal toxicity in cauliflower by application of salicylic acid. Commun Soil Sci Plant Anal 46:1309–1319

    Article  CAS  Google Scholar 

  • Smeets K, Opdenakker K, Remans T (2013) The role of the kinase OXI1 in cadmium- and copper-induced molecular responses in Arabidopsis thaliana. Plant Cell Environ 36:1228–1238

    Article  CAS  PubMed  Google Scholar 

  • Stael S, Wurzinger B, Mair A, Mehlmer N, Vothknecht UC, Teige M (2012) Plant organellar calcium signaling: an emerging field. J Exp Bot 63:1525–1542

    Article  CAS  PubMed  Google Scholar 

  • Sun P, Tian QY, Chen J, Zhang WH (2010) Aluminium-induced inhibition of root elongation in Arabidopsis is mediated by ethylene and auxin. J Exp Bot 61:347–356

    Article  CAS  PubMed  Google Scholar 

  • Taj G, Agarwal P, Grant M, Kumar A (2010) MAPK machinery in plants: recognition and response to different stresses through multiple signal transduction pathways. Plant Signal Behav 5:1370–1378

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tanou G, Molassiotis A, Diamantidis G (2009) Induction of reactive oxygen species and necrotic death-like destruction in strawberry leaves by salinity. Environ Exp Bot 65:270–281

    Article  CAS  Google Scholar 

  • Temple MD, Perrone GG, Dawes IW (2005) Complex cellular responses to recative oxygen species. Trends Cell Biol 15:319–326

    Article  CAS  PubMed  Google Scholar 

  • Thapa G, Sadhukhan A, Panda SK, Sahoo L (2012) Molecular mechanistic model of plant heavy metal tolerance. Biometals 25:489–505

    Article  CAS  PubMed  Google Scholar 

  • Tian S, Wang X, Li P, Wang H, Ji H, **e J, Qiu Q, Shen D, Dong H (2016) Plant aquaporin AtPIP1;4 links apoplastic H2O2 induction to disease immunity pathways. Plant Physiol 171:1635–1650

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Trewavas A (1999) Le calcium, c’est la vie: calcium makes waves. Plant Physiol 120:1–6

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Triantaphylidès C, Havaux M (2009) Singlet oxygen in plants: production, detoxification and signaling. Trends Plant Sci 14:219–228

    Article  PubMed  CAS  Google Scholar 

  • Triantaphylides C, Krischke M, Hoeberichts FA, Ksas B, Gresser G, Havaux M, Van-Breusegem FV, Mueller MJ (2008) Singlet oxygen is major reactive oxygen species involved in photo-oxidative damage to plants. Plant Physiol 148:960–968

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tsai TM, Huang HJ (2006) Effects of iron excess on cell viability and mitogen-activated protein kinase activation in rice roots. Physiol Plant 127:583–592

    Article  CAS  Google Scholar 

  • Tuteja N, Mahajan S (2007) Calcium signaling network in plants. Plant Signal Behav 2:79–85

    Article  PubMed Central  PubMed  Google Scholar 

  • Vijendra PD, Huchappa KM, Lingappa R, Basappa G, Jayanna SG, Kumar V (2016) Physiological and biochemical changes in moth bean (Vigna aconitifolia L.) under cadmium stress. J Bot 1–13

    Google Scholar 

  • Wang YS, Yang ZM (2005) Nitric oxide reduces aluminum toxicity by preventing oxidative stress in the roots of Cassia tora L. Plant Cell Physiol 46:1915–1923

    Article  CAS  PubMed  Google Scholar 

  • Wang C, Zhang SH, Wang PF, Hou J, Zhang WJ, Li W, Lin ZP (2009) The effect of excess Zn on mineral nutrition and antioxidative response in rapeseed seedlings. Chemosphere 75:1468–1476

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Ding H, Zhang A, Ma F, Cao J, Jiang M (2010) A novel mitogen-activated protein kinase gene in maize (Zea mays), ZmMPK3, is involved in response to diverse environmental cues. J Integr Plant Biol 52:442–452

    CAS  PubMed  Google Scholar 

  • Wen JF, Gong M, Liu Y, Hu JL, Deng MH (2013) Effect of hydrogen peroxide on growth and activity of some enzymes involved in proline metabolism of sweet corn seedlings under copper stress. Sci Hortic 164:366–371

    Article  CAS  Google Scholar 

  • Wimalasekera R, Villar C, Begum T, Scherer GF (2011) Copper amine oxidase1 (CuAO1) of Arabidopsis thaliana contributes to abscisic acid-and polyamine-induced nitric oxide biosynthesis and abscisic acid signal transduction. Mol Plant 4:663–678. doi:10.1093/mp/ssr023

    Article  CAS  PubMed  Google Scholar 

  • Yan S, Dong X (2014) Perception of the plant immune signal salicylic acid. Curr Opin Plant Biol 20:64–68. doi:10.1016/j.pbi.2014.04.006

    Article  CAS  PubMed  Google Scholar 

  • Yan J, Tsuichihara N, Etoh T, Iwai S (2007) Reactive oxygen species and nitric oxide are involved in ABA inhibition of stomatal opening. Plant Cell Environ 30:1320–1325

    Article  CAS  PubMed  Google Scholar 

  • Yang T, Poovaiah BW (2002) Hydrogen peroxide homeostasis: activation of plant catalase by calcium/calmodulin. Proc Nat Acad Sci USA 99:4097–4102

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yang L, Ji J, Harris-Shultz KR, Wang H, Wang H, Abd-Allah EF, Luoand Y, Hu X (2016) The dynamic changes of the plasma membrane proteins and the protective roles of nitric oxide in Rice subjected to heavy metal cadmium stress. Front Plant Sc 7:190. doi:10.3389/fpls.2016.00190

    Google Scholar 

  • Yeh CM, Chien PS, Huang HJ (2007) Distinct signaling pathways for induction of MAP kinase activities by cadmium and copper in rice roots. J Exp Bot 58:659–671

    Article  CAS  PubMed  Google Scholar 

  • Yun BW, Feechan A, Yin M, Saidi NB, Le Bihan T, Yu M, Moore JW, Kang JG, Kwon E, Spoel SH, Pallas JA, Loake GJ (2011) S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478:264–268

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Li YH, Hu LY, Wang SH, Zhang FQ, Hu KD (2008) Effects of exoge-nous nitric oxide donor on antioxidant metabolism in wheat leaves under aluminum stress. Russ J Plant Physiol 55:469–474

    Article  CAS  Google Scholar 

  • Zhang S, Cai Z, Wang X (2009) The primary signaling outputs of brassionosteroid are regulated by abscisic acid signaling. Proc Natl Acad Sci 106:4543–4548

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang A, Zhang J, Zhang J, Ye N, Zhang H, Tan M, Jiang M (2011) Nitric oxide mediates brassinosteroid-induced ABA biosynthesis involved in oxidative stress tolerance in maize leaves. Plant Cell Physiol 52:181–192. doi:10.1093/pcp/pcq187

    Article  CAS  PubMed  Google Scholar 

  • Zhang F, ** X, Wang L, Li S, Wu S, Cheng C, Zhang T, Guo W (2016) GhFAnnxA affects fiber elongation and secondary cell wall biosynthesis associated with Ca21 influx, ROS homeostasis, and actin filament reorganization. Plant Physiol 171:1750–1770

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhao H, ** Q, Wang Y, Chu L, Li X, Xu Y (2016) Effects of nitric oxide on alleviating cadmium stress in Typha angustifolia. Plant Growth Regul 78:243–251

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Botanical and Environment Sciences, Guru Nanak Dev University, Amritsar, Punjab, 143005, India

    Sukhmeen Kaur Kohli, Neha Handa, Vandana Gautam, Shagun Bali, Anket Sharma, Kanika Khanna, Saroj Arora, Ashwani Kumar Thukral & Renu Bhardwaj

  2. Department of Zoology, Guru Nanak Dev University, Amritsar, Punjab, 143005, India

    Puja Ohri

  3. Dokuchaev Kharkiv National Agrarian University, Kharkiv, 62483, Ukraine

    Yuriy Victorovich Karpets & Yuriy Evgenovich Kolupaev

Authors
  1. Sukhmeen Kaur Kohli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Neha Handa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vandana Gautam
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shagun Bali
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Anket Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kanika Khanna
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Saroj Arora
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ashwani Kumar Thukral
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Puja Ohri
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Yuriy Victorovich Karpets
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Yuriy Evgenovich Kolupaev
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Renu Bhardwaj
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Renu Bhardwaj .

Editor information

Editors and Affiliations

  1. Crop and Environmental Sciences Division, International Rice Research Institute, Los Banos, Philippines

    M. Iqbal R. Khan

  2. Department of Botany, Aligarh Muslim University, Aligarh, India

    Nafees A. Khan

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer Nature Singapore Pte Ltd.

About this chapter

Cite this chapter

Kohli, S.K. et al. (2017). ROS Signaling in Plants Under Heavy Metal Stress. In: Khan, M., Khan, N. (eds) Reactive Oxygen Species and Antioxidant Systems in Plants: Role and Regulation under Abiotic Stress. Springer, Singapore. https://doi.org/10.1007/978-981-10-5254-5_8

Download citation

Publish with us

Policies and ethics

Search

Navigation