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The diversity of nitric oxide function in plant responses to metal stress

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Abstract

Nitric oxide (NO) emerges as signalling molecule, which is involved in diverse physiological processes in plants. High mobility metal interferes with NO signaling. The exogenous NO alleviates metal stress, whereas endogenous NO contributes to metal toxicity in plants. Owing to different cellular localization and concentration, NO may act as multifunctional regulator in plant responses to metal stress. It not only plays a crucial role in the regulation of gene expression, but serves as a long-distance signal. Through tight modulation of redox signaling, the integration among NO, reactive oxygen species and stress-related hormones in plants determines whether plants stimulate death pathway or activate survival signaling.

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Abbreviations

ABA:

Abscisic acid

ACO:

1-Aminocyclopropane-1-carboxylate oxidase

ACS:

1-Aminocyclopropane-1-carboxylate synthase

APX:

Ascorbate peroxidase

As:

Arsenic

BRs:

Brassinosteroids

CAT:

Catalase

Cu:

Copper

Cd:

Cadmium

cPTIO:

2-(4-Carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide

CTK:

Cytokinin

DAF-FM:

4-Amino-5-methylamino-2′,7′-difluorofluorescein

ET:

Ethylene

GSNOR1 :

S-Nitrosoglutathione reductase gene

Hsp71.2 :

Heat shock protein 71.2

JA:

Jasmonic acid

L-NMMA:

N G-Monomethyl-arginine monoacetate

MAPK:

Mitogen-activated protein kinase

MAT-1:

Met adenosyltransferases

Ni:

Nickel

NO:

Nitric oxide

NOS:

Nitric oxide synthase

NOX:

NADPH oxidase

NR:

Nitrate reductase

PA:

Polyamines

PAL:

Phenylalanine ammonialyase

PCD:

Programmed cell death

POX:

Peroxidase

PrP4A :

Pathogen-related proteins

ROS:

Reactive oxygen species

SAG12:

Senescence-associated gene 12

SNP:

Sodium nitroprusside

Zn:

Zinc

ZR:

Zeatin

References

  • Abdel-Kader DZE (2007) Role of nitric oxide, glutathione and sulfhydryl groups in zinc homeostasis in plants. Am J Plant Physiol 2:59–75

    Article  CAS  Google Scholar 

  • Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Deckert J, Rucinska-Sobkowiak R, Gzyl J, Pawlak-Sprada S, Abramowski D, Jelonek T, Gwozdz 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 

  • Arnaud N, Murgia I, Boucherez J, Briat JF, Cellier F, Gaymard F (2006) An iron-induced nitric oxide burst precedes ubiquitin-dependent protein degradation for Arabidopsis AtFer1 ferritin gene expression. J Biol Chem 281:23579–23588

    Article  CAS  PubMed  Google Scholar 

  • Bajauz A (2011) Suppression of Chlorella vulgaris growth by cadmium, lead, and copper stress and its restoration by endogenous brassinolide. Arch Environ Contam Toxicol 60:406–416

    Article  Google Scholar 

  • Balestrazzi A, Macovei A, Testoni C, Raimondi E, Dona M, Carbonera D (2009) Nitric oxide biosynthesis in white poplar (Populus alba L.) suspension cultures challenged with heavy metals. Plant Stress 3:1–6

    Google Scholar 

  • Barroso JB, Corpas FJ, Carreras A, Rodriguez-Serrano M, Esteban FJ, Fernandez-Ocana A, Chaki M, Romero-Puertas MC, Valderrama R, Sandalio LM, del Rio LA (2006) Localization of S-nitrosoglutathione and expression of S-nitrosoglutathione reductase in pea plants under cadmium stress. J Exp Bot 57:1785–1793

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Belenghi B, Romero-Puertas MC, Vercammen D, Bracjenier A, Inze D, Delledonne M, Van Breusegem F (2007) Metacaspase activity of Arabidopsis thaliana is regulated by S-nitrosylation of a critical cycteine residues. J Biol Chem 282:1352–1358

    Article  CAS  PubMed  Google Scholar 

  • Beligni MV, Lamattina L (1999) Nitric oxide counteracts cytotoxic processes mediated by reactive oxygen species in plant tissues. Planta 208:337–344

    Article  CAS  Google Scholar 

  • Besson-Bard A, Wendehenne D (2009) NO contributes to cadmium toxicity in Arabidopsis thaliana by mediating an iron deprivation response. Plant Signal Behav 4:252–254

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Clark D, Durner J, Navarre DA, Klessig DF (2000) Nitric oxide inhibition of tobacco catalase and ascorbate peroxidase. Mol Plant Microbe Interact 13:1380–1384

    Article  CAS  PubMed  Google Scholar 

  • Corpas FJ, Carreras A, Esteban FJ, Chaki M, Valderrama R, del Rio LA, Barroso JB (2008) Localization of S-nitrosothiols and assay of nitric oxide synthesis and S-nitrosoglutathione reductase activity in plants. Meth Enzymol 437:561–574

    Article  CAS  PubMed  Google Scholar 

  • Crawford NM (2006) Mechanisms for nitric oxide synthesis in plants. J Exp Bot 57:471–478

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  PubMed  Google Scholar 

  • De Stefano M, Ferranrini A, Delledonne M (2005) Nitric oxide functions in the plant hypersensitive disease resistance response. BMC Plant Biol 5:S10

    Article  PubMed Central  Google Scholar 

  • Delledonne M, Xia Y, Dixon RA, Lamb C (1998) Nitric oxide functions as a signal in plant disease resistance. Nature 394:585–588

    Article  CAS  PubMed  Google Scholar 

  • Di Baccio D, Minnocci A, Sebastiani L (2013) Lead structural modifications in Populus × euramericana subjected to Zn excess. Biol Plantarum 57:313–324

    Article  Google Scholar 

  • Feechan A, Kwon E, Yun BW, Wang Y, Pallas JA, Loake GJ (2005) A central role for S-nitrosothiols in plant disease resistance. Proc Natl Acad Sci USA 102:8054–8059

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Feigl G, Kumar D, Lehotai N, Tugyi N, Molnar A, Ordog A, Szepesi A, Gemes K, Laskay G, Erdei L, Kolbert Z (2012) Physiological and morphological responses of the root system of Indian mustard (Brassica juncea L. Czern.) and rapeseed (Brassica napus L.) to copper stress. Ecotoxicol Environ Saf 94:179–189

    Article  Google Scholar 

  • Fojtova M, Kovarik A (2000) Genotoxic effect of cadmium is associated with apoptotic changes in tobacco cells. Plant Cell Environ 23:531–537

    Article  CAS  Google Scholar 

  • Graziano M, Lamattina L (2007) Nitric oxide accumulation is required for molecular and physiological responses to iron deficiency in tomato roots. Plant J 52:949–960

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Grün S, Lindermayr C, Sell S, Durner J (2006) Nitric oxide and gene regulation in plants. J Exp Bot 57:507–516

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • He H, Zhan J, He L, Gu M (2012) Nitric oxide signaling in aluminum stress in plants. Protoplasma 249:483–492

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hsu YT, Kao CH (2005) Abscisic acid accumulation and cadmium tolerance in rice seedlings. Physiol Plant 124:71–80

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Iakimova ET, Woltering EJ, Kapchina-Toteva VM, Harren FJM, Cristescu SM (2008) Cadmium toxicity in cultured tomato cells—role of ethylene, pro teases and oxidative stress in cell death signaling. Cell Biol Int 32:1521–1529

    Article  CAS  PubMed  Google Scholar 

  • Jarup L, Akesson A (2009) Current status of cadmium as an environmental health problem. Toxicol Appl Pharmacol 238:201–208

    Article  PubMed  Google Scholar 

  • Jhanji S, Setia RC, Kaur N, Kaur P, Setia N (2012) Role of nitric oxide in cadmium-induced stress on growth, photosynthetic components and yield of Brassica napus L. J Environ Biol 33:1027–1032

    CAS  PubMed  Google Scholar 

  • Kazemi N (2012) Effect of exogenous nitric oxide alleviating nickel-induced oxidative stress in leaves of tomato plants. Int J AgriSci 2:799–809

    CAS  Google Scholar 

  • Kopyra M, Gwóźdź EA (2003) Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus. Plant Physiol Biochem 441:1011–1017

    Article  Google Scholar 

  • Kopyra M, Stachon-Wilk M, Gwozdz 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 

  • Kroutil M, Hejtmankova A, Lachman J (2010) Effect of spring wheat (Triticum aestivum L.) treatment with brassinosteroids on the content of cadmium and lead in plant aerial biomass and grain. Plant Soil Environ 56:43–50

    CAS  Google Scholar 

  • Lamotte O, Courtois C, Dobrowolska G, Besson A, Pugin A, Wendehenne D (2006) Mechanisms of nitric oxide-induced increase of free cytosolic Ca2+ concentration in Nicotiana plumbaginifolia cells. Free Radical Biol Med 40(8):1369–1376

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Leshem YY (2000) Nitric oxide in plants: occurrence, function and use. Kluwer Academis Press, Dordrecht

    Book  Google Scholar 

  • Lin A, Wang Y, Tang J, Xue P, Li C, Liu L, Hu B, Yang F, Loake GJ, Chu C (2012) Nitric oxide and protein S-nitrosylation are integral to hydrogen peroxide-induced leaf cell death in rice. Plant Physiol 158(1):451–464

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lindemayr C, Saalbach G, Durner J (2005) Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiol 137:921–930

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Mihailovic N, Drazic G (2011) Incomplete alleviation of nickel toxicity in bean by nitric oxide supplementation. Plant Soil Environ 57:396–401

    Article  CAS  Google Scholar 

  • Navarre DA, Wendehenne D, Durner J, Noad R, Klessig DF (2000) Nitric oxide modulates the activity of tobacco aconitase. Plant Physiol 122:573–582

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signalling molecules in plants. J Exp Bot 372:1237–1247

    Article  Google Scholar 

  • Noriega GO, Yannarelli GG, Balestrasse KB, Batlle A, Tomaro ML (2007) The effect of nitric oxide on heme oxygenase gene expression in soybean leaves. Planta 226:1155–1163

    Article  CAS  PubMed  Google Scholar 

  • Overmyer K, Brosche M, Kangasjarvi J (2003) Reactive oxygen species and hormonal control of cell death. Trends Plant Sci 8:335–342

    Article  CAS  PubMed  Google Scholar 

  • Pagnussat GC, Lanteri ML, Lombardo MC, Lamattina L (2004) Nitric oxide mediates the indole acetic acid induction activation of a mitogen-activated protein kinase cascade involved in adventitious root development. Plant Physiol 135(1):279–286

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pawlak-Sprada S, Arasimowicz-Jelonek M, Podgorska M, Deckert J (2011) Activation of phenylpropanoid pathway in legume plants exposed to heavy metals. Part I. Effects of cadmium and lead on phenylalanine ammonia-lyase gene expression, enzyme activity and lignin content. Acta Biochim Pol 58:211–216

    CAS  PubMed  Google Scholar 

  • Peto A, Lehotai N, Lozano-Juste J, Leon J, Tari I, Erdei L, Kolbert Z (2011) Involvement of nitric oxide and auxin in signal transduction of copper-induced morphological responses in Arabidopsis seedlings. Ann Bot 108:449–457

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rodriguez-Serrano M, Romero-Puertas MC, Zabalza A, Corpas FJ, Gomez M, del Rio LA, Sandalio LM (2006) Cadmium effect on oxidative metabolism of pea (Pisum sativum L.) roots. Imaging of reactive oxygen species and nitric oxide accumulation in vivo. Plant Cell Environ 29:1532–1544

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Romero-Puertas MC, Laxa M, Matte A, Zaninotto F, Finkemeier I, Jones AME, Perazzolli M, Vandelle E, Dietz K, Delledonne M (2007) S-nitrosylation of peroxiredoxin II E promotes peroxynitrite-mediated tyrosine nitration. Plant Cell 19:4120–4130

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Singh AK, Sharma L, Mallick N (2004) Antioxidative role of nitric oxide on copper toxicity to a chlorophycean alga, Chlorella. Ecotoxicol Environ Safe 59:223–227

    Article  CAS  Google Scholar 

  • Singh HP, Batish DR, Kaur G, Arora K, Kohli RK (2008) Nitric oxide (as sodium nitroprusside) supplementation ameliorates Cd toxicity in hydroponically grown wheat roots. Environ Exp Bot 63:158–167

    Article  CAS  Google Scholar 

  • Singh HP, Kaur S, Batish DR, Sharma VP, Sharma N, Kohli R (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 

  • Sivaci A, Elmas E, Gumus F (2008) Changes in abscisic acid contents of some aquatic plants exposed to cadmium and salinity. Int J Bot 4:104–108

    Article  CAS  Google Scholar 

  • Štork F, Backor M, Klejdus B, Hedbavny J, Kovacik J (2013) Changes of metal-induced toxicity by H2O2/NO modulators in Scenedesmus quadricauda (Chlorophyceae). Environ Sci Pollut Res Int 20(8):5502–5511

    Article  PubMed  Google Scholar 

  • Tewari RK, Hahn EJ, Paek KY (2008) Modulation of copper toxicity-induced oxidative damage by nitric oxide supply in the adventitious roots of Panax ginseng. Plant Cell Rep 27:171–181

    Article  CAS  PubMed  Google Scholar 

  • Tran TA, Vassileva V, Petrov P, Popova LP (2012) Cadmium-induced structural disturbances in Pisum sativum leaves are alleviated by nitric oxide. Turk J Bot 37:698–707

    Google Scholar 

  • Valentovicova K, Haluskova L, Huttova J, Mistrık I, Tamas L (2010) Effect of cadmium on diaphorase activity and nitric oxide production in barley root tips. J Plant Physiol 167:10–14

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Veselov D, Kudoyarova G, Symonyan M, Veselov St (2003) Effect of cadmium on ion uptake, transpiration and cytokinin content in wheat seedlings. Bulg J Plant Physiol Special issue: 353–359

  • Vitti A, Nuzzaci M, Scopa A, Tataranni G, Remans T, Vangronsveld J, Sofo A (2013) Auxin and cytokinin metabolism and root morphological modification in Arabidopsis thaliana seedlings infected with cucumber mosaic virus (CMV) of exposed to cadmium. Int J Mol Sci 14:6889–6902

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang WY, Xu J, Liu XJ, Yu Y, Ge Q (2012) Cadmium induces early flowering in Arabidopsis. Biol Plant 56(1):117–120

    Article  CAS  Google Scholar 

  • Wilson ID, Neill SJ, Hancock JT (2008) Nitric oxide synthesis and signaling in plants. Plant Cell Environ 31:622–631

    Article  CAS  PubMed  Google Scholar 

  • Xiong J, Lu H, Lu K, Duan Y, An L, Zhu C (2009a) Cadmium decreases crown root numbers by decreasing endogenous nitric oxide, which is indispensable for crown root primordia initiation in rice seedlings. Planta 230:599–610

    Article  CAS  PubMed  Google Scholar 

  • Xiong J, An L, Lu H, Zhu C (2009b) Exogenous nitric oxide enhances cadmium tolerance of rice by increasing pectin and hemicellulose contents in root cell wall. Planta 230:755–765

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Xu J, Yin H, Li Y, Liu X (2010b) Nitric oxide is associated with long-term zinc tolerance in Solanum nigrum. Plant Physiol 154(3):1319–1334

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yang JL, Chen WW, Chen LQ, Qin C, Jin CW, Shi YZ, Zheng SJ (2013) The 14-3-3 protein GENERAL REGULATORY FACTOR11 (GRF11) acts downstream of nitric oxide to regulate iron acquisition in Arabidopsis thaliana. New Phytol 197(3):815–824

    Article  CAS  PubMed  Google Scholar 

  • Ye Y, Li Z, Xing D (2013) Nitric oxide promotes MPK6-mediated caspase-3-like activation in cadmium-induced Arabidopsis thaliana programmed cell death. Plant Cell Environ 36:1–15

    Article  CAS  PubMed  Google Scholar 

  • Yu CC, Hung KT, Kao CH (2005) Nitric oxide reduces Cu toxicity and Cu-induced NH4 + accumulation in rice leaves. J Plant Physiol 162:1319–1330

    Article  CAS  PubMed  Google Scholar 

  • Yu Q, Sun L, Jin H, Chen Q, Chen Z, Xu M (2012) Lead-induced nitric oxide generation plays a critical role in lead uptake by Pogonatherum crinitum root cells. Plant Cell Physiol 53(10):1728–1736

    Article  CAS  PubMed  Google Scholar 

  • Zeigler J, Stenzel I, Hause B, Maucher H, Hamberg M, Grimm R, Ganal M, Wasternack C (2000) Molecular cloning of allene oxide cyclase. The enzyme establishing the stereochemistry of octadecanoids and jasmonates. J Biol Chem 275:19132–19138

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Chen Z, Zhu C (2012) Endogenous nitric oxide mediates alleviation of cadmium toxicity induced by calcium in rice seedlings. J Environ Sci 24(5):940–948

    Article  CAS  Google Scholar 

  • Zhou T, Zheng LP, Yuan HY, Yuan YF, Wang JW (2012) The nitric oxide production and NADPH-diaphorase activity in root tips of Vicia faba L. under copper toxicity. Plant Omics J 5:115–121

    Google Scholar 

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

    Article  Google Scholar 

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (No. 30960181 and 31260296) and 2011 Guangxi Innovation Program for Graduates (GXU11T31076).

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Authors and Affiliations

  1. College of Agronomy, Guangxi University, Nanning, 530004, People’s Republic of China

    Huyi He, Longfei He & Minghua Gu

  2. Cash Crops Research Institute, Guangxi Academy of Agricultural Sciences, Nanning, 530007, People’s Republic of China

    Huyi He

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He, H., He, L. & Gu, M. The diversity of nitric oxide function in plant responses to metal stress. Biometals 27, 219–228 (2014). https://doi.org/10.1007/s10534-014-9711-1

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