Abstract
Lead toxicity is a threat to growth and production of crop plants. In this study, effect of salicylic acid and sodium hydrosulfide pretreatments was investigated on the alteration in the Pb accumulation, protein content, nitrate reductase activity and metabolism of selected free amino acids in maize plants subjected to lead stress. Maize seeds were soaked in 0.5 mM salicylic acid and sodium hydrosulfide for 12 h and then exposed to 2.5 mM Pb (NO3)2 for 9 days. Results demonstrated that lead stress significantly reduced the plant growth, shoot glutathione content and protein content, nitrate reductase activity in the shoots and roots while increased glutathione content in roots of maize plants. We also observed accumulation of most free amino acids composition except tyrosine and tryptophan under lead stress condition. Plants pre-treated with salicylic acid and sodium hydrosulfide exhibited improvement of plant growth, decrease of Pb accumulation, increase of protein and glutathione contents and nitrate reductase activity. Salicylic acid and sodium hydrosulfide pretreatments decreased most amino acids content in shoot of lead stressed plants. In case of roots, salicylic acid and sodium hydrosulfide had different effects on the content of amino acids. Pretreatment of sodium hydrosulfide resulted in greater levels of free amino acids in roots. These results indicate that moderate lead stress can be attributed to effect of salicylic acid and sodium hydrosulfide by improvement of nitrate reductase activity and glutathione content and regulation of amino acids metabolism.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aftab T, Khan MMA, da Silva JAT, Idrees M, Naeem M (2011) Role of salicylic acid in promoting salt stress tolerance and enhanced artemisinin production in Artemisia annua L. J Plant Growth Regul 30(4):425–435. https://doi.org/10.1007/s00344-011-9205-0
Azevedo Neto AD, Prisco JT, Gomes-Filho E (2009) Changes in soluble amino-N, soluble proteins and free amino acids in leaves and roots of salt-stressed maize genotypes. J Plant Interact 4(2):137–144. https://doi.org/10.1080/17429140902866954
Chaffei C, Pageau K, Suzuki A, Gouia H, Ghorbel MH, Masclaux-Daubresse C (2004) Cadmium toxicity induced changes in nitrogen management in Lycopersicon esculentum leading to a metabolic safeguard through an amino acid storage strategy. Plant Cell Physiol 45(11):1681–1693. https://doi.org/10.1093/pcp/pch192
Chen Z, Chen M, Jiang M (2017) Hydrogen sulfide alleviates mercury toxicity by sequestering it in roots or regulating reactive oxygen species productions in rice seedlings. Plant Physiol Biochem 111:179–192. https://doi.org/10.1016/j.plaphy.2016.11.027
Cui W, Chen H, Zhu K, Jin Q, Xie Y, Cui J, Xia Y, Zhang J, Shen W (2014) Cadmium-induced hydrogen sulfide synthesis is involved in cadmium tolerance in Medicago sativa by reestablishment of reduced (Homo) glutathione and reactive oxygen species homeostases. PLoS One 9(10):e109669. https://doi.org/10.1371/journal.pone.0109669
Dixit G, Singh AP, Kumar A, Dwivedi S, Deeba F, Kumar S, Suman S, Adhikar B, Shukla Y, Trivedi PK, Pandey V (2015) Sulfur alleviates arsenic toxicity by reducing its accumulation and modulating proteome, amino acids and thiol metabolism in rice leaves. Sci Rep 5:16205. https://doi.org/10.1038/srep16205
Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–77. https://doi.org/10.1016/0003-9861(59)90090-6
Erika F, Lips SH, Laszlo E (2004) 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 23:865–872. https://doi.org/10.1016/j.jplph.2004.11.015
Farhangi-Abriz S, Ghassemi-Golezani K (2016) Improving amino acid composition of soybean under salt stress by salicylic acid and jasmonic acid. J Appl Bot Food Qual. https://doi.org/10.5073/JABFQ.2016.089.031
Forde BG, Lea PJ (2007) Glutamate in plants: metabolism, regulation, and signalling. J Exp Bot 58(9):2339–2358. https://doi.org/10.1093/jxb/erm121
Gao S, Liu KT, Chung TW (2013) Responses of nitrogen metabolism to lead stress in Jatropha curcas cotyledon. Int J Agric Biol 15(6):1126–1132
Hussein MM, Balbaa LK, Gaballah MS (2007) Salicylic acid and salinity effects on growth of maize plant. Res J Agric Biol Sci 3(4):321–328
Jaworski EG (1971) Nitrate reductase assay in intact plant tissue. Biochem Biophys Res Commun 43:1274–1279. https://doi.org/10.1016/S0006-291X(71)80010-4
Khan MIR, Asgher M, Khan NA (2014) Alleviation of salt-induced photosynthesis and growth inhibition by salicylic acid involves glycinebetaine and ethylene in mungbean (Vigna radiata L.). Plant Physiol Biochem 80:67–74. https://doi.org/10.1016/j.plaphy.2014.03.026
Khan MIR, Fatma M, Per TS, Anjum NA, Khan NA (2015) Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. Front Plant Sci 6:462. https://doi.org/10.3389/fpls.2015.00462
Kohli SK, Handa N, Sharma A, Gautam V, Arora S, Bhardwaj R, Alyemeni MN, Wijaya L, Ahmad P (2018) Combined effect of 24-epibrassinolide and salicylic acid mitigates lead (Pb) toxicity by modulating various metabolites in Brassica juncea L. seedlings. Protoplasma 255(1):11–24. https://doi.org/10.1007/s00709-017-1124-x
Lea PJ, Sodek L, Parry MA, Shewry PR, Halford NG (2007) Asparagine in plants. Ann Appl Biol 150(1):1–26. https://doi.org/10.1111/j.1744-7348.2006.00104.x
Lehmann T, Pollmann S (2009) Gene expression and characterization of a stress-induced tyrosine decarboxylase from Arabidopsis thaliana. FEBS Lett 583(12):1895–1900. https://doi.org/10.1016/j.febslet.2009.05.017
Li Z, Yu J, Peng Y, Huang B (2016a) Metabolic pathways regulated by γ-aminobutyric acid (GABA) contributing to heat tolerance in creeping bentgrass (Agrostis stolonifera). Sci Rep 6:30338. https://doi.org/10.1038/srep30338
Li ZG, Min X, Zhou ZH (2016b) Hydrogen sulfide: a signal molecule in plant cross-adaptation. Front Plant Sci 7:1621. https://doi.org/10.3389/fpls.2016.01621
Lowry OJ, Rosebrough AL, Randall RJ (1951) Protein measurement with the phenol reagent. J Biol Chem 193:265–275
Mostofa MG, Rahman A, Ansary MMU, Watanabe A, Fujita M, Tran LSP (2015) Hydrogen sulfide modulates cadmium-induced physiological and biochemical responses to alleviate cadmium toxicity in rice. Sci Rep. https://doi.org/10.1038/srep14078
Nazar R, Umar S, Khan NA (2015) Exogenous salicylic acid improves photosynthesis and growth through increase in ascorbate-glutathione metabolism and S assimilation in mustard under salt stress. Plant Signal Behav 10(3):e1003751. https://doi.org/10.1080/15592324.2014.1003751
Nemat Alla M, Elbaz Younis M, El-Shihaby OA, El-Bastawisy Z (2002) Kinetin regulation of growth and secondary metabolism in waterlogging and salinity treated Vigna sinensis and Zea mays. Acta Physiol Plant 24(1):19–27
Nóvoa-Muñoz JC, Simal-Gándara J, Fernández-Calviño D, López-Periago E, Arias-Estévez M (2008) Changes in soil properties and in the growth of Lolium multiforum in an acid soil amended with a soil waste from wineries. Bioresour Technol 99:6771–6779. https://doi.org/10.1016/j.biortech.2008.01.035
Pavlíková D, Pavlík M, Procházková D, Zemanová V, Hnilička F, Wilhelmová N (2014) Nitrogen metabolism and gas exchange parameters associated with zinc stress in tobacco expressing an ipt gene for cytokinin synthesis. J Plant Physiol 171(7):559–564. https://doi.org/10.1016/j.jplph.2013.11.016
Planchet E, Limami AM, D'Mello JP (2015) Amino acid synthesis under abiotic stress, 3rd edn. London UK, pp 262–276
Sharma P, Dubey RSH (2005) Lead toxicity in Plants. Br Plant Physiol 17:35–52
Singh B, Usha K (2003) Salicylic acid induced physiological and biochemical changes in wheat seedlings under water stress. Plant Growth Regul 39(2):137–141
Singh VP, Singh S, Kumar J, Prasad SM (2015) Hydrogen sulfide alleviates toxic effects of arsenate in pea seedlings through up-regulation of the ascorbate–glutathione cycle: possible involvement of nitric oxide. J Plant Physiol 181:20–29. https://doi.org/10.1016/j.jplph.2015.03.015
Skopelitis DS, Paranychianakis NV, Paschalidis KA, Pliakonis ED, Delis ID, Yakoumakis DI, Papadakis AK, Stephanou EG, Roubelakis-Angelakis KA (2006) Abiotic stress generates ROS that signal expression of anionic glutamate dehydrogenases to form glutamate for proline synthesis in tobacco and grapevine. Plant Cell 18(10):2767–2781. https://doi.org/10.1105/tpc.105.038323
Stines AP, Naylor DJ, Høj PB, Van Heeswijck R (1999) Proline accumulation in developing grapevine fruit occurs independently of changes in the levels of Δ1-pyrroline-5-carboxylate synthetase mRNA or protein. Plant Physiol 120(3):923. https://doi.org/10.1104/pp.120.3.923
Sujatha B, Priyadarshini B (2009) Influence of lead and cadmium on amino acids and protein content of pigeonpea seedlings. Int J Plant Sci 4(2):482–486
Winter G, Todd CD, Trovato M, Forlani G, Funck D (2015) Physiological implications of arginine metabolism in plants. Front Plant Sci 6:534. https://doi.org/10.3389/fpls.2015.00534
Zafari S, Sharifi M, Chashmi NA, Mur LA (2016) Modulation of Pb-induced stress in Prosopis shoots through an interconnected network of signaling molecules, phenolic compounds and amino acids. Plant Physiol Biochem 99:11–20. https://doi.org/10.1016/j.plaphy.2015.12.004
Zemanová V, Pavlík M, Pavlíková D (2017) Cadmium toxicity induced contrasting patterns of concentrations of free sarcosine, specific amino acids and selected microelements in two Noccaea species. PLoS One 12(5):e0177963. https://doi.org/10.1371/journal.pone.0177963
Zhang H, Hu LY, Hu KD, He YD, Wang SH, Luo JP (2008) Hydrogen sulfide promotes wheat seed germination and alleviates oxidative damage against copper stress. J Integr Plant Biol 50(12):1518–1529. https://doi.org/10.1111/j.1744-7909.2008.00769.x
Acknowledgements
The authors are grateful to Neda Farnad MSc, for her assistance in advancing of this research.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by G. Klobus.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zanganeh, R., Jamei, R. & Rahmani, F. Role of salicylic acid and hydrogen sulfide in promoting lead stress tolerance and regulating free amino acid composition in Zea mays L.. Acta Physiol Plant 41, 94 (2019). https://doi.org/10.1007/s11738-019-2892-z
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-019-2892-z