Abstract
Nitric oxide (NO) is known to induce plant resistance for several environmental stresses. The protective roles of NO in cadmium (Cd) toxicity have been well documented for various plant species; nevertheless, little information is available about its molecular regulation in improving Cd tolerance of barley plants. Therefore, we combined a comparative proteomics with physiological analyses to evaluate the potential roles of NO in alleviating Cd stress (50 μM) in barley (Hordeum vulgare L.) seedlings. Exogenous application of NO donor sodium nitroprusside (SNP, 100 μM) decreased the Cd-mediated seedling growth inhibition. This observation was supported by the reduction of lipid peroxidation as well as the improvement of chlorophyll content and inhibition of hydrogen peroxide accumulation. Activities of the superoxide dismutase and guaiacol peroxidase were reduced following the application of SNP, while ascorbate peroxidase activity was enhanced. In this study, a total of 34 proteins were significantly regulated by NO in the leaves under Cd stress using a gel-based proteomic approach. The proteomic analysis showed that several pathways were noticeably influenced by NO including photosynthesis and carbohydrate metabolism, protein metabolism, energy metabolism, stress defense, and signal transduction. These results provide new evidence that NO induce photosynthesis and energy metabolism which may enhance Cd tolerance in barley seedlings.
Similar content being viewed by others
Data availability
The submitted work is original and has not been published elsewhere in any form or language.
Code availability
Not applicable.
References
Aebi H (1984) Catalase in vitro. Oxygen radicals in biological systems. Elsevier, Amsterdam, pp 121–126
Ahmad P, Ahanger MA, Alyemeni MN, Wijaya L, Alam P (2018) Exogenous application of nitric oxide modulates osmolyte metabolism, antioxidants, enzymes of ascorbate-glutathione cycle and promotes growth under cadmium stress in tomato. Protoplasma 255(1):79–93. https://doi.org/10.1007/s00709-017-1132-x
Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51(2):163–190. https://doi.org/10.1007/s11099-013-0021-6
Bagheri R, Bashir H, Ahmad J, Iqbal M, Qureshi MI (2015) Spinach (Spinacia oleracea L.) modulates its proteome differentially in response to salinity, cadmium and their combination stress. Plant Physiol Biochem 97:235–245. https://doi.org/10.1016/j.plaphy.2015.10.012
Barranco-Medina S, Lazaro JJ, Dietz KJ (2009) The oligomeric conformation of peroxiredoxins links redox state to function. FEBS Lett 583:1809–1816. https://doi.org/10.1016/j.febslet.2009.05.029
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287. https://doi.org/10.1016/0003-2697(71)90370-8
Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254. https://doi.org/10.1006/abio.1976.9999
Candiano G, Bruschi M, Musante L, Santucci L, Ghiggeri GM, Carnemolla B, Orecchia P, Zardi L, Righetti PG (2004) Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 25:1327–1333. https://doi.org/10.1002/elps.200305844
Choppala G, Saifullah BN, Bibi S, Iqbal M, Rengel Z, Ok YS (2014) Cellular mechanisms in higher plants governing tolerance to cadmium toxicity cellular mechanisms in higher plants governing tolerance. Crit Rev Plant Sci 33:374–391. https://doi.org/10.1080/07352689.2014.903747
Domingos P, Prado AM, Wong A, Gehring C, Feijo JA (2015) Nitric oxide: a multitasked signaling gas in plants. Mol Plant 8:506–520. https://doi.org/10.1016/j.molp.2014.12.010
Dzeja P, Terzic A (2009) Adenylate kinase and AMP signaling networks: metabolic monitoring, signal communication and body energy sensing. Int J Mol Sci 10:1729–1772. https://doi.org/10.3390/ijms10041729
Du H, Zhou X, Yang Q, Liu H, Kurtenbach R (2015) Changes in H+-ATPase activity and conjugated polyamine contents in plasma membrane purified from developing wheat embryos under short-time drought stress. Plant Growth Reg 75(1):1–10. https://doi.org/10.1007/s10725-014-9925-9
Finka A, Mattoo RU, Goloubinoff P (2016) Experimental milestones in the discovery of molecular chaperones as polypeptide unfolding enzymes. Annu Rev Biochem 85:715–742. https://doi.org/10.1146/annurev-biochem-060815-014124
Gill SS, Hasanuzzaman M, Nahar K, Macovei A, Tuteja N (2012) Importance of nitric oxide in cadmium stress tolerance in crop plants. Plant Physiol Biochem 63:254–261. https://doi.org/10.1016/j.plaphy.2012.12.001
Gong B, Nie W, Yan Y, Gao Z, Shi Q (2017) Unravelling cadmium toxicity and nitric oxide induced tolerance in Cucumis sativus: Insight into regulatory mechanisms using proteomics. J Hazard Mater 336:202–213. https://doi.org/10.1016/j.jhazmat.2017.04.058
Gupta DK, Palma JM, Corpas FJ (2018) Antioxidants and antioxidant enzymes in higher plants. Springer, Cham
Haider FU, Liqun C, Coulter JA, Cheema SA, Wu J, Zhang R, Wenjuni M, Farooq M (2021) Cadmium toxicity in plants: impacts and remediation strategies. Ecotox Environ Safe 211:111887. https://doi.org/10.1016/j.ecoenv.2020.111887
He CT, Zhou YH, Huang YY, Fu HL, Wang XS, Gong FY, Tan X, Yang ZY (2018) Different proteomic processes related to the cultivar-dependent cadmium accumulation of Amaranthus gangeticus. J Agr Food Chem 66(5):1085–1095. https://doi.org/10.1021/acs.jafc.7b05042
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198. https://doi.org/10.1016/0003-9861(68)90654-1
Hussain B, Ashraf MN, Rahman SU, Abbas A, Lia J, Farooq M (2021) Cadmium stress in paddy fields: effects of soil conditions and remediation strategies. Sci Total Environ 754:142188. https://doi.org/10.1016/j.scitotenv.2020.142188
Kaur G, Singh HP, Batish DR, Mahajan P, Kohli RK, Rishi V (2015) Exogenous nitric oxide (NO) interferes with lead (Pb)-induced toxicity by detoxifying reactive oxygen species in hydroponically grown wheat (Triticum aestivum) roots. PLoS ONE 10:e0138713. https://doi.org/10.1371/journal.pone.0138713
Kaya C, Akram NA, Sürücü A, Ashraf M (2019) Alleviating effect of nitric oxide on oxidative stress and antioxidant defence system in pepper (Capsicum annuum L.) plants exposed to cadmium and lead toxicity applied separately or in combination. Sci Horti 255:52–60. https://doi.org/10.1016/j.scienta.2019.05.029
Kaya C, Ashraf M, Alyemeni MN, Ahmad P (2020) Responses of nitric oxide and hydrogen sulfide in regulating oxidative defence system in wheat plants grown under cadmium stress. Physiol Plant 168(2):345–360. https://doi.org/10.1111/ppl.13012
Khator K, Saxena I, Shekhawat GS (2021) Nitric oxide induced Cd tolerance and phytoremediation potential of B. juncea by the modulation of antioxidant defense system and ROS detoxification. BioMetals 34(1):15–32. https://doi.org/10.1007/s10534-020-00259-9
Krech K, Ruf S, Masduki FF, Thiele W, Bednarczyk D, Albus CA, Bock R (2012) The plastid genome-encoded Ycf4 protein functions as a nonessential assembly factor for photosystem I in higher plants. Plant Physiol 159:579–591. https://doi.org/10.1104/pp.112.196642
Lionaki E, Tavernarakis N (2013) Oxidative stress and mitochondrial protein quality control in aging. J Proteom 92:181–194. https://doi.org/10.1016/j.jprot.2013.03.022
Liu S, Li Y, Liu L, Min J, Liu W, Li X, Pan X, Lu X, Deng Q (2020a) Comparative proteomics in rice seedlings to characterize the resistance to cadmium stress by high-performance liquid chromatography–tandem mass spectrometry (HPLC-MS/MS) with isobaric tag for relative and absolute quantitation (iTRAQ). Anal Lett 53(5):807–820. https://doi.org/10.1080/00032719.2019.1680684
Liu X, Yin L, Deng X, Gong D, Du S, Wang S, Zhang Z (2020b) Combined application of silicon and nitric oxide jointly alleviated cadmium accumulation and toxicity in maize. J Hazard Mat 395:122679. https://doi.org/10.1016/j.jhazmat.2020.122679
Maere S, Heymans K, Kuiper M (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21:3448–3449. https://doi.org/10.1093/bioinformatics/bti551
Mika A, Lüthje S (2003) Properties of guaiacol peroxidase activities isolated from corn root plasma membranes. Plant Physiol 132:1489–1498. https://doi.org/10.1104/pp.103.020396
Mostofa MG, Fujita M, Tran LSP (2015) Nitric oxide mediates hydrogen peroxide and salicylic acid induced salt tolerance in rice (Oryza sativa L.) seedlings. Plant Growth Regul 77:265–277. https://doi.org/10.1007/s10725-015-0061-y
Nabi RBS, Tayade R, Hussain A, Kulkarni KP, Imran QM, Mun BG, Yun BW (2019) Nitric oxide regulates plant responses to drought, salinity, and heavy metal stress. Environ Exp Bot 161:120–133. https://doi.org/10.1016/j.envexpbot.2019.02.003
Nakano Y, Asada K (1981) Hydrogen-peroxide is scavenged by ascorbate-specific peroxidase in spinach-chloroplasts. Plant Cell Physiol 22:867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232
Ormancey M, Thuleau P, Mazars C, Cotelle V (2017) CDPKs and 14–3–3 proteins: emerging duo in signaling. Trends Plant Sci 22(3):263–272. https://doi.org/10.1016/j.tplants.2016.11.007
Pompella A, Maellaro E, Casini AF, Comporti M (1987) Histochemical detection of lipid peroxidation in the liver of bromobenzene-poisoned mice. Amer J Pathol 129:295–301
Prakash V, Singh VP, Tripathi DK, Sharma S, Corpas FJ (2019) Crosstalk between nitric oxide (NO) and abscisic acid (ABA) signalling molecules in higher plants. Environ Exp Bot 161:41–49. https://doi.org/10.1016/j.envexpbot.2018.10.033
Qin S, Liu H, Nie Z, Rengel Z, Gao W, Li C, Zhao P (2020) Toxicity of cadmium and its competition with mineral nutrients for uptake by plants: a review. Pedosphere 30:168–180. https://doi.org/10.1016/S1002-0160(20)60002-9
Rao J, Lv W, Yang J (2017) Proteomic analysis of saffron (Crocus sativus L) grown under conditions of cadmium toxicity. Biosci J 33(3):713–720. https://doi.org/10.14393/BJ-v33n3-36923
Romeropuertas MC, Sandalio LM (2016) Nitric oxide level is self-regulating and also regulates its ROS partners. Front Plant Sci 7:316. https://doi.org/10.3389/fpls.2016.00316
Sandalio LM, Dalurzo HC, Gómez M, Romero-Puertas MC, del Río LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2126. https://doi.org/10.1093/jexbot/52.364.2115
Sarry JE, Kuhn L, Ducruix C, Lafaye A (2006) The early responses of Arabidopsis thaliana cells to cadmium exposure explored by protein and metabolite profiling analyses. Proteomics 6:2180–2198. https://doi.org/10.1002/pmic.200500543
Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365. https://doi.org/10.1093/jexbot/53.372.1351
Singh PK, Maximova SN, Jensen PJ, Lehman BL, Ngugi HK, McNellis TW (2010) FIBRILLIN4 is required for plastoglobule development and stress resistance in apple and Arabidopsis. Plant Physiol 154(3):1281–1293. https://doi.org/10.1104/pp.110.164095
Singh S, Prasad SM, Sharma S, Dubey NK, Ramawat N, Prasad R, Chauhan DK (2020) Silicon and nitric oxide-mediated mechanisms of cadmium toxicity alleviation in wheat seedlings. Physiol Plant. https://doi.org/10.1111/ppl.13065
Sinha P, Poland J, Schnölzer M, Rabilloud T (2001) A new silver staining apparatus and procedure for matrix-assisted laser desorption/ionization-time of flight analysis of proteins after two- dimensional electrophoresis. Proteomics 1:835–840. https://doi.org/10.1002/1615-9861(200107)1:7%3c835::AID-PROT835%3e3.0.CO;2-2
Szklarczyk D, Franceschini A, Kuhn M, Simonovic M, Roth A, Minguez P, Doerks T, Stark M, Muller J, Bork P, Jensen LJ, von Mering C (2011) The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res 39:D561–D568. https://doi.org/10.1093/nar/gkq973
Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11(6):1187–1194. https://doi.org/10.1046/j.1365-313X.1997.11061187.x
Tian B, Qiao Z, Zhang L, Li H, Pei Y (2016) Hydrogen sulfide and proline cooperate to alleviate cadmium stress in foxtail millet seedlings. Plant Physiol Biochem 109:293–299. https://doi.org/10.1016/j.plaphy.2016.10.006
Urano K, Kurihara Y, Seki M, Shinozaki K (2010) ‘Omics’ analyses of regulatory networks in plant abiotic stress responses. Curr Opin Plant Biol 13(2):132–138. https://doi.org/10.1016/j.pbi.2009.12.006
Wang Q, Liang X, Dong Y, Xu L, Zhang X, Kong J, Liu S (2013) Effects of exogenous salicylic acid and nitric oxide on physiological characteristics of perennial ryegrass under cadmium stress. J Plant Growth Regul 32:721–731. https://doi.org/10.1007/s10535-014-0475-9
Wang D, Liu Y, Tan X, Liu H, Zeng G, Hu X, Jian H, Gu Y (2015) Effect of exogenous nitric oxide on antioxidative system and S-nitrosylation in leaves of Boehmeria nivea (L.) Gaud under cadmium stress. Environ Sci Pollut Res 22:3489–3497. https://doi.org/10.1007/s11356-014-3581-5
Wani KI, Naeem M, Castroverde CDM, Kalaji HM, Albaqami M, Aftab T (2021) Molecular mechanisms of nitric oxide (NO) signaling and reactive oxygen species (ROS) homeostasis during abiotic stresses in plants. Int J Mol Sci 22:9656. https://doi.org/10.3390/ijms22179656
Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313. https://doi.org/10.1016/S0176-1617(11)81192-2
Xu J, Wang W, Yin H, Liu X, Sun H, Mi Q (2010) Exogenous nitric oxide improves antioxidative capacity and reduces auxin degradation in roots of Medicago truncatula seedlings under cadmium stress. Plant Soil 326:321–330. https://doi.org/10.1007/s11104-009-0011-4
Yang L, Ji J, Harris-Shultz KR, Wang H, Wang H, Abd-Allah EF, Luo 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 Sci 7:190. https://doi.org/10.3389/fpls.2016.00190
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. https://doi.org/10.1016/s1001-0742(11)60978-9
Zhang F, Liu M, Li Y, Che Y, Xiao Y (2019) Effects of arbuscular mycorrhizal fungi, biochar and cadmium on the yield and element uptake of Medicago sativa. Sci Total Environ 655:1150–1158. https://doi.org/10.1016/j.scitotenv.2018.11.317
Zhong M, Li S, Huang F, Qiu J, Zhang J, Sheng Z, Tang S, Wei X, Hu P (2017) The phosphoproteomic response of rice seedlings to cadmium stress. Int J Mol Sci 18(10):2055. https://doi.org/10.3390/ijms18102055
Acknowledgements
The work was funded by the Scientific Research Projects Coordination Unit (Project No: 19.FEN.BİL.43) of Afyon Kocatepe University. The authors gratefully acknowledge the Medicinal Genetics Laboratory of Afyonkarahisar Health Sciences University and the DEKART Proteomics Laboratory of Kocaeli University for their technical help. The authors are grateful to Afyon Kocatepe University’s Foreign Language Support Unit for language editing.
Funding
This study has been funded by Afyon Kocatepe University Scientific Research Projects Coordination Unit (Project No: 19.FEN.BİL.43).
Author information
Authors and Affiliations
Contributions
All authors have contributed equally to this work.
Corresponding author
Ethics declarations
Conflict of interest
The authors have declared that they have no conflict of interest.
Consent to participate
All authors have approved the article to be submitted to your journal.
Consent for publication
All authors have approved the article to be submitted to your journal for publication.
Ethical approval
The manuscript has not been submitted to more than one journal for simultaneous consideration.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Alp, K., Terzi, H. & Yildiz, M. Proteomic and physiological analyses to elucidate nitric oxide-mediated adaptive responses of barley under cadmium stress. Physiol Mol Biol Plants 28, 1467–1476 (2022). https://doi.org/10.1007/s12298-022-01214-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12298-022-01214-3