Skip to main content
Log in

Exogenous nitric oxide mediates alleviation of mercury toxicity by promoting auxin transport in roots or preventing oxidative stress in leaves of rice seedlings

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Nitric oxide (NO), a multifunctional gaseous molecule, mediates a variety of responses to biotic and abiotic stresses. The effects of exogenous NO on rice (Oryza sativa cv. ‘Zhonghua 11’) growth under mercuric chloride (HgCl2) stress were investigated. The results showed that 60 μM Hg significantly inhibited the root elongation of rice plantlets after seed germination. While 100 μM or 200 μM sodium nitroprusside (SNP, a donor of NO) could increase the root length by attenuating the effects of 2,3,5-triiodobenzoic acid (TIBA) and Hg, which indicated the role of NO in auxin transport-promoting in roots. On the other hand, SNP decreased the absorption and transportation of Hg in roots and shoots of rice seedlings at five-leaf stage. Moreover, the levels of superoxide radical (O2·) and hydrogen peroxide (H2O2) in leaves were also decreased significantly. However, the activities of antioxidant enzymes were not enhanced by SNP. Moreover, NO promoted the growth of rice plantlets under Hg stress even when superoxide dismutase (SOD, EC 1.15.1.1) or catalase (CAT, 1.11.1.6) activity was inhibited by diethyldithiocarbamate (DDC, an inhibitor of SOD) or 3-amino-1,2,4-triazole (AT, an inhibitor of catalase), respectively. These results confirmed that NO could act as the direct quencher of O2· and then prevent the oxidative damage caused by Hg ion in leaves.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

Hg:

Mercury

NO:

Nitric oxide

SNP:

Sodium nitroprusside

ROS:

Reactive oxygen species

O2· :

Superoxide radical

H2O2 :

Hydrogen peroxide

SOD:

Superoxide dismutase

CAT:

Catalase

DDC:

Diethyldithiocarbamate

AT:

3-amino-1,2,4-triazole

TIBA:

2,3,5-triiodobenzoic acid

References

  • Abat JK, Deswal R (2013) Nitric oxide modulates the expression of proteins and promotes epiphyllous bud differentiation in Kalanchoe pinnata. J Plant Growth Regul 32:92–101

    Article  CAS  Google Scholar 

  • Aebi HE (1983) Catalase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Verlag Chemie, Weinheim, pp 273–285

    Google Scholar 

  • Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Gwóźdź EA (2011) The message of nitric oxide in cadmium challenged plants. Plant Sci 181:612–620

    Article  CAS  PubMed  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Cargnelutti D, Tabaldi LA, Spanevello RM, de Oliveira Jucoski G, Battisti V, Redin M, Redin M, Linares CEB, Dressler VL, de Moraes Flores ÉM, Nicoloso FT, Morsch VM, Schetinger MRC (2006) Mercury toxicity induces oxidative stress in growing cucumber seedlings. Chemosphere 65:999–1006

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Yang ZM (2012) Mercury toxicity, molecular response and tolerance in higher plants. Biometals 25:847–857

    Article  CAS  PubMed  Google Scholar 

  • Chen Z, Pan YH, Wang SS, Ding YF, Yang WJ, Zhu C (2012) Overexpression of a protein disulfide isomerase-like protein from Methanothermobacter thermoautotrophicum enhances mercury tolerance in transgenic rice. Plant Sci 197:10–20

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Fernández-Marcos M, Sanz L, Lorenzo O (2012) Nitric oxide: an emerging regulator of cell elongation during primary root growth. Plant Signal Behav 7:196–200

    Article  PubMed Central  PubMed  Google Scholar 

  • Gao S, Ou-yang C, Tang L, Zhu JQ, Xu Y, Wang SH, Chen F (2010) Growth and antioxidant responses in Jatropha curcas seedling exposed to mercury toxicity. J Hazard Mater 182:591–597

    Article  CAS  PubMed  Google Scholar 

  • Guo B, Liang YC, Zhu YG, Zhao FJ (2007) Role of salicylic acid in alleviating oxidative damage in rice roots (Oryza sativa) subjected to cadmium stress. Environ Pollut 147:743–749

    Article  CAS  PubMed  Google Scholar 

  • Guo K, Xia K, Yang ZM (2008) Regulation of tomato lateral root development by carbon monoxide and involvement in auxin and nitric oxide. J Exp Bot 59:3443–3452

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Han YH, Moon HJ, You BR, Kim SZ, Kim SH, Park WH (2009) The effects of buthionine sulfoximine, diethyldithiocarbamate or 3-amino-1,2,4-triazole on propyl gallate-treated HeLa cells in relation to cell growth, reactive oxygen species and glutathione. Int J Mol Med 24:261–268

    CAS  PubMed  Google Scholar 

  • He HY, He LF, Gu MH, Li XF (2012) Nitric oxide improves aluminum tolerance by regulating hormonal equilibrium in the root apices of rye and wheat. Plant Sci 183:123–130

    Article  CAS  PubMed  Google Scholar 

  • Inukai Y, Sakamoto T, Ueguchi-Tanaka M, Shibata Y, Gomi K, Umemura I, Hasegawa Y, Ashikari M, Kitano H, Matsuoka M (2005) Crown rootless1, which is essential for crown root formation in rice, is a target of AUXIN RESPONSE FACTOR in auxin signaling. Plant Cell 17:1387–1396

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jana SCM (1981) Glycolate metabolism of three submerged aquatic angiosperms during aging. Aquat Bot 12:345–354

    Article  Google Scholar 

  • Kazemi N, Khavari-Nejad RA, Fahimi H, Saadatmand S, Nejad-Sattari T (2010) Effects of exogenous salicylic acid and nitric oxide on lipid peroxidation and antioxidant enzyme activities in leaves of Brassica napus L. under nickel stress. Sci Hortic 126:402–407

    Article  CAS  Google Scholar 

  • Kim HS, Jung MC (2012) Mercury contamination in agricultural soils from abandoned metal mines classified by geology and mineralization. Environ Geochem Health 34(Suppl 1):55–69

    Article  CAS  PubMed  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 41:1011–1017

    Article  CAS  Google Scholar 

  • Lanteri ML, Pagnussat GC, Lamattina L (2006) Calcium and calcium-dependent protein kinases are involved in nitric oxide- and auxin-induced adventitious root formation in cucumber. J Exp Bot 57:1341–1351

    Article  CAS  PubMed  Google Scholar 

  • Lushchak V, Semchyshyn H, Lushchak O, Mandryk S (2005) Diethyldithiocarbamate inhibits in vivo Cu, Zn-superoxide dismutase and perturbs free radical processes in the yeast Saccharomyces cerevisiae cells. Biochem Biophys Res Commun 338:1739–1744

    Article  CAS  PubMed  Google Scholar 

  • Meng DK, Chen J, Yang ZM (2011) Enhancement of tolerance of Indian mustard (Brassica juncea) to mercury by carbon monoxide. J Hazard Mater 186:1823–1929

    Article  CAS  Google Scholar 

  • Mishra SKSD, Singhal GS (1991) Interrelationship between salt and light stress on the primary process of photosynthesis. J Plant Physiol 138:92–96

    Article  CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Pagnussat GC, Simontacchi M, Puntarulo S, Lamattina L (2002) Nitric oxide is required for root organogenesis. Plant Physiol 129:954–956

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pagnussat GC, Lanteri ML, Lamattina L (2003) Nitric oxide and cyclic GMP are messengers in the indole acetic acid-induced adventitious rooting process. Plant Physiol 132:1241–1248

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rao MV, Paliyath G, Ormrod DP, Murr DP, Watkins CB (1997) Influence of salicylic acid on H2O2 production, oxidative stress, and H2O2-metabolizing enzymes. Salicylic acid-mediated oxidative damage requires H2O2. Plant Physiol 115:137–149

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sahu GKUS, Sahoo BB (2012) Mercury induced phytotoxicity and oxidative stress in wheat (Triticum aestivum L.) plants. Physiol Mol Biol Plants 18:21–31

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Saxena I, Shekhawat GS (2013) Nitric oxide (NO) in alleviation of heavy metal induced phytotoxicity and its role in protein nitration. Nitric Oxide 32:13–20

    Article  CAS  PubMed  Google Scholar 

  • Shiyab S, Chen J, Han FXX, Monts DL, Matta FB, Gu MM, Su Y, Masad MA (2009) Mercury-induced oxidative stress in Indian mustard (Brassica juncea L.). Environ Toxicol 24:462–471

    Article  CAS  PubMed  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 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 

  • Sunderland EM, Selin NE (2013) Future trends in environmental mercury concentrations: implications for prevention strategies. Environ Health 12:2–5

    Article  PubMed Central  CAS  PubMed  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 

  • Xiong J, An L, Lu H, Zhu C (2009a) 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 

  • Xiong J, Lu H, Lu KX, Duan YX, An LY, Zhu C (2009b) Cadmium decreases crown root number 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 

  • Yadav S, David A, Baluška F, Bhatla SC (2013) Rapid auxin-induced nitric oxide accumulation and subsequent tyrosine nitration of proteins during adventitious root formation in sunflower hypocotyls. Plant Signal Behav 8:e23196

    Article  PubMed Central  PubMed  Google Scholar 

  • Yoshida S, Forno DA, Cock JH, Gomez KA (1976) Laboratory manual for physiological studies of rice. International Rice Research Institute, Los Banõs

    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 24:940–948

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the Zhejiang Provincial Natural Science Foundation of China (Grant NO: 3100246) and Taizhou University’s Scientific Research Project (2014PY024).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Cheng Zhu.

Ethics declarations

Conflict of interest

There is no conflict of interest and all authors have read and approved the final manuscript.

Additional information

Communicated by S. Srivastava.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, Z., Zhang, L. & Zhu, C. Exogenous nitric oxide mediates alleviation of mercury toxicity by promoting auxin transport in roots or preventing oxidative stress in leaves of rice seedlings. Acta Physiol Plant 37, 194 (2015). https://doi.org/10.1007/s11738-015-1931-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-015-1931-7

Keywords

Navigation