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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Synergistic mitigation of nickel toxicity in pepper (Capsicum annuum) by nitric oxide and thiourea via regulation of nitrogen metabolism and subcellular nickel distribution

Ferhat Uğurlar https://orcid.org/0000-0002-3663-3497 A and Cengiz Kaya https://orcid.org/0000-0001-8938-3463 A *
+ Author Affiliations
- Author Affiliations

A Soil Science and Plant Nutrition Department, Harran University, Sanliurfa, Turkey.

* Correspondence to: c_kaya70@yahoo.com

Handling Editor: Vadim Demidchik

Functional Plant Biology 50(12) 1099-1116 https://doi.org/10.1071/FP23122
Submitted: 8 June 2023  Accepted: 11 October 2023  Published: 25 October 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Nickel (Ni) contamination hinders plant growth and yield. Nitric oxide (NO) and thiourea (Thi) aid plant recovery from heavy metal damage, but their combined effects on pepper (Capsicum annuum) plant tolerance to Ni stress need more study. Sodium nitroprusside (0.1 mM, SNP) and 400 mg L−1 Thi, alone and combined, were studied for their impact on pepper growth under Ni toxicity. Ni stress reduces chlorophyll, PSII efficiency and leaf water and sugar content. However, SNP and Thi alleviate these effects by increasing leaf water, proline and sugar content. It also increased the activities of superoxide dismutase, catalase, ascorbate peroxidase and peroxidase. Nickel stress lowered nitrogen assimilation enzymes (nitrate reductase, nitrite reductase, glutamine synthetase, glutamate synthase and glutamate dehydrogenase) and protein content, but increased nitrate, ammonium and amino acid content. SNP and Thi enhanced nitrogen assimilation, increased protein content and improved pepper plant growth and physiological functions during Ni stress. The combined treatment reduced Ni accumulation, increased Ni in leaf cell walls and potentially in root vacuoles, and decreased Ni concentration in cell organelles. It effectively mitigated Ni toxicity to vital organelles, surpassing the effects of SNP or Thi use alone. This study provides valuable insights for addressing heavy metal contamination in agricultural soils and offers potential strategies for sustainable and eco-friendly farming practices.

Keywords: antioxidant system, nickel toxicity, nitric oxide, nitrogen metabolism, oxidative stress, pepper, subcellular distribution, thiourea.

References

Aebi H (1984) Catalase in vitro. Methods in Enzymology 105, 121-126.
| Crossref | Google Scholar | PubMed |

Agbaria H, Heuer B, Zieslin N (1998) Rootstock-imposed alterations in nitrate reductase and glutamine synthetase activities in leaves of rose plants. Biologia Plantarum 41(1), 85-91.
| Crossref | Google Scholar |

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.
| Crossref | Google Scholar | PubMed |

Ahmad A, Khan WU, Ali Shah A, Yasin NA, Naz S, Ali A, Tahir A, Iram Batool A (2021) Synergistic effects of nitric oxide and silicon on promoting plant growth, oxidative stress tolerance and reduction of arsenic uptake in Brassica juncea. Chemosphere 262, 128384.
| Crossref | Google Scholar | PubMed |

Ali A, Khan SU, Qayyum A, Billah M, Ahmed W, Malik S (2019) Silicon and thiourea mediated stimulation of salt tolerance varying between three fodder beet (Beta vulgaris L.) genotypes. Applied Ecology and Environmental Research 17(5), 10781-10791.
| Crossref | Google Scholar |

Ali B (2022) Physiological role, toxicity, hyperaccumulation, and tolerance of nickel in plants. In ‘Appraisal of metal(loids) in the ecosystem’. (Eds V Kumar, A Sharma, R Setia) pp. 105–134. (Elsevier: Amsterdam, Netherlands)

Alnusairi GSH, Mazrou YSA, Qari SH, Elkelish AA, Soliman MH, Eweis M, Abdelaal K, El-Samad GA, Ibrahim MFM, ElNahhas N (2021) Exogenous nitric oxide reinforces photosynthetic efficiency, osmolyte, mineral uptake, antioxidant, expression of stress-responsive genes and ameliorates the effects of salinity stress in wheat. Plants 10(8), 1693.
| Crossref | Google Scholar | PubMed |

Altaf MA, Shahid R, Ren M-X, Altaf MM, Jahan MS, Khan LU (2021) Melatonin mitigates nickel toxicity by improving nutrient uptake fluxes, root architecture system, photosynthesis, and antioxidant potential in tomato seedling. Journal of Soil Science and Plant Nutrition 21(3), 1842-1855.
| Crossref | Google Scholar |

Altaf MA, Hao Y, He C, Mumtaz MA, Shu H, Fu H, Wang Z (2022) Physiological and biochemical responses of pepper (Capsicum annuum L.) seedlings to nickel toxicity. Frontiers in Plant Science 13, 950392.
| Crossref | Google Scholar | PubMed |

Aqeel U, Parwez R, Aftab T, Khan MMA, Naeem M (2022) Exogenous calcium repairs damage caused by nickel toxicity in fenugreek (Trigonella foenum-graecum L.) by strengthening its antioxidant defense system and other functional attributes. South African Journal of Botany 150, 153-160.
| Crossref | Google Scholar |

Arikan B, Yildiztugay E, Ozfidan-Konakci C (2023) Protective role of quercetin and kaempferol against oxidative damage and photosynthesis inhibition in wheat chloroplasts under arsenic stress. Physiologia Plantarum 175, e13964.
| Crossref | Google Scholar |

Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology 24, 1-15.
| Crossref | Google Scholar | PubMed |

Badawy IH, Hmed AA, Sofy MR, Al-Mokadem AZ (2022) Alleviation of cadmium and nickel toxicity and phyto-stimulation of tomato plant L. by endophytic Micrococcus luteus and Enterobacter cloacae. Plants 11(15), 2018.
| Crossref | Google Scholar | PubMed |

Barcelos JPQ, Reis HPG, Godoy CV, Gratão PL, Furlani Junior E, Putti FF, Campos M, Reis AR (2018) Impact of foliar nickel application on urease activity, antioxidant metabolism and control of powdery mildew (Microsphaera diffusa) in soybean plants. Plant Pathology 67(7), 1502-1513.
| Crossref | Google Scholar |

Barrs HD, Weatherley PE (1962) A re-examination of the relative turgidity technique for estimating water deficits in leaves. Australian Journal of Biological Sciences 15, 413-428.
| Crossref | Google Scholar |

Bashir K, Rasheed S, Kobayashi T, Seki M, Nishizawa NK (2016) Regulating subcellular metal homeostasis: the key to crop improvement. Frontiers in Plant Science 7, 1192.
| Crossref | Google Scholar | PubMed |

Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant and Soil 39, 205-207.
| Crossref | Google Scholar |

Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry 44, 276-287.
| Crossref | Google Scholar | PubMed |

Beri A, Sharma R (2016) Nickel toxicity to photosynthetic attributes in the leaves of lentil (Lens culnaris Medic. Masar). International Journal of Advanced Research 2(8), 239-242.
| Google Scholar |

Berwal MK, Kumar R, Prakash K, Rai GK, Hebbar KB (2021) Antioxidant defense system in plants against abiotic stress. In ‘Abiotic stress tolerance mechanisms in plants’. (Eds GK Rai, RR Kumar, S Bagati) pp. 175–202. (CRC Press: London, UK)

Bhalerao SA, Sharma AS, Poojari AC (2015) Toxicity of nickel in plants. International Journal of Pure & Applied Bioscience 3(2), 345-355.
| Google Scholar |

Bhardwaj S, Verma T, Raza A, Kapoor D (2023) Silicon and nitric oxide-mediated regulation of growth attributes, metabolites and antioxidant defense system of radish (Raphanus sativus L.) under arsenic stress. Phyton-International Journal of Experimental Botany 92(3), 763-782.
| Crossref | Google Scholar |

Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248-254.
| Crossref | Google Scholar |

Cataldo DA, Maroon M, Schrader LE, Youngs VL (1975) Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. Communications in Soil Science and Plant Analysis 6(1), 71-80.
| Crossref | Google Scholar |

Chapman HD, Pratt PF (1982) ‘Methods of plant analysis. I. Methods of analysis for soils, plants and water.’ (Chapman Publishers: Riverside, CA, USA)

Chen T, Liu X, Zhang X, Chen X, Tao K, Hu X (2016) Effect of alkyl polyglucoside and nitrilotriacetic acid combined application on lead/pyrene bioavailability and dehydrogenase activity in co-contaminated soils. Chemosphere 154, 515-520.
| Crossref | Google Scholar | PubMed |

Chen X, Zhao Y, Zhong Y, Chen J, Qi X (2023) Deciphering the functional roles of transporter proteins in subcellular metal transportation of plants. Planta 258(1), 17.
| Crossref | Google Scholar | PubMed |

Cvikrová M, Hrubcová M, Vägner M, Macháčková I, Eder J (1994) Phenolic acids and peroxidase activity in alfalfa (Medicago sativa) embryogenic cultures after ethephon treatment. Physiologia Plantarum 91, 226-233.
| Crossref | Google Scholar |

Dionisio-Sese ML, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Science 135, 1-9.
| Crossref | Google Scholar |

Doğru A, Altundağ H, Dündar MŞ (2021) Gelişmiş Bitkilerde Nikel Elementinin Fizyolojik Fonksiyonları ve Nikel Toksisitesi. Fırat Üniversitesi Fen Bilimleri Dergisi 33(1), 1-19 [In Turkish].
| Google Scholar |

Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Analytical Chemistry 28, 350-356.
| Crossref | Google Scholar |

Erdal S, Turk H (2016) Cysteine-induced upregulation of nitrogen metabolism-related genes and enzyme activities enhance tolerance of maize seedlings to cadmium stress. Environmental and Experimental Botany 132, 92-99.
| Crossref | Google Scholar |

Fawzy E, Soltan M-E (2022) Existence, extraction, and behaviour of some elements in the system of water–soil–plant. International Journal of Environmental Analytical Chemistry 102, 7911-7927.
| Crossref | Google Scholar |

Gioseffi E, de Neergaard A, Schjoerring JK (2012) Interactions between uptake of amino acids and inorganic nitrogen in wheat plants. Biogeosciences 9(4), 1509-1518.
| Crossref | Google Scholar |

Groat RG, Vance CP (1981) Root nodule enzymes of ammonia assimilation in alfalfa (Medicago sativa L.) developmental patterns and response to applied nitrogen. Plant Physiology 67(6), 1198-1203.
| Crossref | Google Scholar |

Hashem HA, Hassanein AA, Esmail NY (2018) Nitric oxide enhances the adaptive responses of lupine plants against heavy-metal stress. Australian Journal of Crop Science 12, 1962-1974.
| Crossref | Google Scholar |

Hassan MU, Chattha MU, Khan I, Chattha MB, Aamer M, Nawaz M, Ali A, Khan MAU, Khan TA (2019) Nickel toxicity in plants: reasons, toxic effects, tolerance mechanisms, and remediation possibilities – a review. Environmental Science and Pollution Research 26, 12673-12688.
| Crossref | Google Scholar | PubMed |

He C, Zhao Y, Wang F, Oh K, Zhao Z, Wu C, Zhang X, Chen X, Liu X (2020) Phytoremediation of soil heavy metals (Cd and Zn) by castor seedlings: tolerance, accumulation and subcellular distribution. Chemosphere 252, 126471.
| Crossref | Google Scholar | PubMed |

Hussain I, Saleem MH, Mumtaz S, Rasheed R, Ashraf MA, Maqsood F, Ali S (2022) Choline chloride mediates chromium tolerance in spinach (Spinacia oleracea L.) by restricting its uptake in relation to morpho-physio-biochemical attributes. Journal of Plant Growth Regulation 41(4), 1594-1614.
| Crossref | Google Scholar |

Husted S, Hebbern CA, Mattsson M, Schjoerring JK (2000) A critical experimental evaluation of methods for determination of NH4+ in plant tissue, xylem sap and apoplastic fluid. Physiologia Plantarum 109(2), 167-179.
| Crossref | Google Scholar |

Ishtiyaq S, Kumar H, Varun M, Kumar B, Paul MS (2018) Heavy metal toxicity and antioxidative response in plants: an overview. In ‘Plants under metal and metalloid stress’. (Eds M Hasanuzzaman, K Nahar, M Fujita) pp. 77–106. (Springer: Singapore)

Israr M, Jewell A, Kumar D, Sahi SV (2011) Interactive effects of lead, copper, nickel and zinc on growth, metal uptake and antioxidative metabolism of Sesbania drummondii. Journal of Hazardous Materials 186(2-3), 1520-1526.
| Crossref | Google Scholar | PubMed |

Jaworski EG (1971) Nitrate reductase assay in intact plant tissues. Biochemical and Biophysical Research Communications 43(6), 1274-1279.
| Crossref | Google Scholar | PubMed |

Jayaprakasha GK, Bae H, Crosby K, Jifon JL, Patil BS (2012) Bioactive compounds in peppers and their antioxidant potential. In ‘Hispanic foods: chemistry and bioactive compounds’. (Eds MH Tunick, EG de-Mejia) pp. 43–56. (American Chemical Society: Washington DC, USA)

Joseph PS, Musa DA, Egwim EC, Uthman A (2022) Function of urease in plants with reference to legumes: a review. In ‘Legumes research, Vol. 2’. (Eds JC Jimenez-Lopez, A Clemente) pp. 1–19. (IntechOpen: London, UK) doi:10.1080/17429145.2012.725480

Kaya C, Sonmez O, Aydemir S, Ashraf M, Dikilitas M (2013) Exogenous application of mannitol and thiourea regulates plant growth and oxidative stress responses in salt-stressed maize (Zea mays L.). Journal of Plant Interactions 8(3), 234-241.
| Crossref | Google Scholar |

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. Scientia Horticulturae 255, 52-60.
| Crossref | Google Scholar |

Kaya C, Ugurlar F, Ashraf M, Noureldeen A, Darwish H, Ahmad P (2021) Methyl jasmonate and sodium nitroprusside jointly alleviate cadmium toxicity in wheat (Triticum aestivum L.) plants by modifying nitrogen metabolism, cadmium detoxification, and AsA–GSH cycle. Frontiers in Plant Science 12, 654780.
| Crossref | Google Scholar |

Kaya C, Ugurlar F, Farooq S, Ashraf M, Alyemeni MN, Ahmad P (2022a) Combined application of asparagine and thiourea improves tolerance to lead stress in wheat by modulating AsA-GSH cycle, lead detoxification and nitrogen metabolism. Plant Physiology and Biochemistry 190, 119-132.
| Crossref | Google Scholar | PubMed |

Kaya C, Sarıoglu A, Ashraf M, Alyemeni MN, Ahmad P (2022b) The combined supplementation of melatonin and salicylic acid effectively detoxifies arsenic toxicity by modulating phytochelatins and nitrogen metabolism in pepper plants. Environmental Pollution 297, 118727.
| Crossref | Google Scholar | PubMed |

Khan KM, Naz F, Taha M, Khan A, Perveen S, Choudhary MI, Voelter W (2014) Synthesis and in vitro urease inhibitory activity of N, N′-disubstituted thioureas. European Journal of Medicinal Chemistry 74, 314-323.
| Crossref | Google Scholar | PubMed |

Kiran , Bharti R, Sharma R (2022) Effect of heavy metals: an overview. Materials Today: Proceedings 51, 880-885.
| Crossref | Google Scholar |

Kumar S, Wang M, Liu Y, Fahad S, Qayyum A, Jadoon SA, Chen Y, Zhu G (2022a) Nickel toxicity alters growth patterns and induces oxidative stress response in sweetpotato. Frontiers in Plant Science 13, 1054924.
| Crossref | Google Scholar |

Kumar S, Rani V, Singh S, Kapoor D, Dhanjal DS, Thakur A, Pujari M, Ramamurthy PC, Singh J (2022b) Arsenic-induced responses in plants: impacts on biochemical processes. In ‘Arsenic in plants: uptake, consequences and remediation techniques’. (Eds PK Srivastava, R Singh, P Parihar, SM Prasad) pp. 112–128. (Wiley: Weinheim, Germany)

Lee YP, Takahashi T (1966) An improved colorimetric determination of amino acids with the use of ninhydrin. Analytical Biochemistry 14, 71-77.
| Crossref | Google Scholar |

Liu J, Duan C-Q, Zhang X-H, Zhu Y-N, Hu C (2009) Subcellular distribution of chromium in accumulating plant Leersia hexandra Swartz. Plant and Soil 322, 187-195.
| Crossref | Google Scholar |

Loqué D, Tillard P, Gojon A, Lepetit M (2003) Gene expression of the NO3 transporter NRT1.1 and the nitrate reductase NIA1 is repressed in Arabidopsis roots by NO2, the product of NO3 reduction. Plant Physiology 132(2), 958-967.
| Crossref | Google Scholar | PubMed |

Loreto F, Velikova V (2001) Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiology 127, 1781-1787.
| Crossref | Google Scholar | PubMed |

Lubyanova AR, Bezrukova MV, Shakirova FM (2022) Involvement of nitric oxide in methyl jasmonate-mediated regulation of water metabolism in wheat plants under drought stress. Stresses 2(4), 477-492.
| Crossref | Google Scholar |

Ma J, Saleem MH, Yasin G, Mumtaz S, Qureshi FF, Ali B, Ercisli S, Alhag SK, Ahmed AE, Vodnar DC, Hussain I, Marc RA, Chen F (2022) Individual and combinatorial effects of SNP and NaHS on morpho-physio-biochemical attributes and phytoextraction of chromium through Cr-stressed spinach (Spinacia oleracea L.). Frontiers in Plant Science 13, 973740.
| Crossref | Google Scholar | PubMed |

Maxwell K, Johnson GN (2000) Chlorophyll fluorescence – a practical guide. Journal of Experimental Botany 51, 659-668.
| Crossref | Google Scholar | PubMed |

Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Analytica Chimica Acta 27, 31-36.
| Crossref | Google Scholar |

Mustafa A, Zulfiqar U, Mumtaz MZ, Radziemska M, Haider FU, Holatko J, Hammershmiedt T, Naveed M, Ali H, Kintl A, Saeed Q, Kucerik J, Brtnicky M (2023) Nickel (Ni) phytotoxicity and detoxification mechanisms: a review. Chemosphere 328, 138574.
| Crossref | Google Scholar |

Nabi A, Parwez R, Aftab T, Khan MMA, Naeem M (2021) Triacontanol protects Mentha arvensis L. from nickel-instigated repercussions by escalating antioxidant machinery, photosynthetic efficiency and maintaining leaf ultrastructure and root morphology. Journal of Plant Growth Regulation 40(4), 1594-1612.
| Crossref | Google Scholar |

Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environmental Chemistry Letters 8, 199-216.
| Crossref | Google Scholar |

Najafi-Kakavand S, Karimi N, Ghasempour H-R, Raza A, Chaichi M, Modarresi M (2023) Role of jasmonic and salicylic acid on enzymatic changes in the root of two Alyssum inflatum Náyr. Populations exposed to nickel toxicity. Journal of Plant Growth Regulation 42, 1647-1664.
| Crossref | Google Scholar |

Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and Cell Physiology 22(5), 867-880.
| Crossref | Google Scholar |

Nie J, Pan Y, Shi J, Guo Y, Yan Z, Duan X, Xu M (2015) A comparative study on the uptake and toxicity of nickel added in the form of different salts to maize seedlings. International Journal of Environmental Research and Public Health 12(12), 15075-15087.
| Crossref | Google Scholar | PubMed |

Ohri P, Bhardwaj R, Kaur R, Jasrotia S, Khajuria A, Khanna K, Sharma N (2022) Nitric oxide: a key player in mitigating heavy metal toxicity in plants. In ‘Nitric oxide in plant biology’. (Eds VP Singh, S Singh, DK Tripathi, MC Romero-Puertas, LM Sandalio) pp. 169–196. (Elsevier: London, UK)

O’Leary B, Plaxton WC (2015) The central role of glutamate and aspartate in the post-translational control of respiration and nitrogen assimilation in plant cells. In ‘Amino acids Higher plants’. (Ed. JPF D’Mello) pp. 277–297. (CABI International: London, UK)

Palma JM, Freschi L, Rodríguez-Ruiz M, González-Gordo S, Corpas FJ (2019) Nitric oxide in the physiology and quality of fleshy fruits. Journal of Experimental Botany 70(17), 4405-4417.
| Crossref | Google Scholar | PubMed |

Paul P, Sharma S, Pandey R (2023) Phosphorus scavenging and remobilization from root cell walls under combined nitrogen and phosphorus stress is regulated by phytohormones and nitric oxide cross-talk in wheat. Journal of Plant Growth Regulation 42, 1614-1630.
| Crossref | Google Scholar |

Rahim W, Khan M, Al Azzawi TNI, Pande A, Methela NJ, Ali S, Imran M, Lee D-S, Lee G-M, Mun B-G, Moon Y-S, Lee I-J, Yun B-W (2022) Exogenously applied sodium nitroprusside mitigates lead toxicity in rice by regulating antioxidants and metal stress-related transcripts. International Journal of Molecular Sciences 23(17), 9729.
| Crossref | Google Scholar | PubMed |

Rezayian M, Niknam V, Ebrahimzadeh H (2019) Oxidative damage and antioxidative system in algae. Toxicology Reports 6, 1309-1313.
| Crossref | Google Scholar | PubMed |

Rizwan M, Imtiaz M, Dai Z, Mehmood S, Adeel M, Liu J, Tu S (2017) Nickel stressed responses of rice in Ni subcellular distribution, antioxidant production, and osmolyte accumulation. Environmental Science and Pollution Research 24, 20587-20598.
| Crossref | Google Scholar | PubMed |

Rizwan M, Mostofa MG, Ahmad MZ, Imtiaz M, Mehmood S, Adeel M, Dai Z, Li Z, Aziz O, Zhang Y, Tu S (2018) Nitric oxide induces rice tolerance to excessive nickel by regulating nickel uptake, reactive oxygen species detoxification and defense-related gene expression. Chemosphere 191, 23-35.
| Crossref | Google Scholar | PubMed |

Rizwan M, Mostofa MG, Ahmad MZ, Zhou Y, Adeel M, Mehmood S, Ahmad MA, Javed R, Imtiaz M, Aziz O, Ikram M, Tu S, Liu Y (2019) Hydrogen sulfide enhances rice tolerance to nickel through the prevention of chloroplast damage and the improvement of nitrogen metabolism under excessive nickel. Plant Physiology and Biochemistry 138, 100-111.
| Crossref | Google Scholar | PubMed |

Rizwan M, Usman K, Alsafran M, Jabri HA, Samreen T, Saleem MH, Tu S (2022) Nickel toxicity interferes with NO3/NH4+ uptake and nitrogen metabolic enzyme activity in rice (Oryza sativa L.). Plants 11(11), 1401.
| Crossref | Google Scholar | PubMed |

Saad R, Kobaissi A, Robin C, Echevarria G, Benizri E (2016) Nitrogen fixation and growth of Lens culinaris as affected by nickel availability: a pre-requisite for optimization of agromining. Environmental and Experimental Botany 131, 1-9.
| Crossref | Google Scholar |

Saito A, Saito M, Ichikawa Y, Yoshiba M, Tadano T, Miwa E, Higuchi K (2010) Difference in the distribution and speciation of cellular nickel between nickel-tolerant and non-tolerant Nicotiana tabacum L. cv. BY-2 cells. Plant, Cell & Environment 33(2), 174-187.
| Crossref | Google Scholar | PubMed |

Sanaullah T, Wahid A, Sadia B, Hanif A, Maqbool N, Arshad T, Kabir Z (2016) Exogenous application of thiourea ameliorates salt stress effects by alleviation of oxidative damage in hybrid maize. Journal of Agricultural Science and Technology 6, 220-231.
| Crossref | Google Scholar |

Sayyadi G, Niknezhad Y, Fallah H (2023) Sodium nitroprusside ameliorates lead toxicity in rice (Oryza sativa L.) by modulating the antioxidant scavenging system, nitrogen metabolism, lead sequestration mechanism, and proline metabolism. Environmental Science and Pollution Research 30, 24408-24423.
| Crossref | Google Scholar | PubMed |

Seregin IV, Kozhevnikova AD (2021) Low-molecular-weight ligands in plants: role in metal homeostasis and hyperaccumulation. Photosynthesis Research 150(1-3), 51-96.
| Crossref | Google Scholar | PubMed |

Shukla A, Pathak SK, Singh S, Srivastava S (2023) Application of thiourea ameliorates stress and reduces accumulation of arsenic in wheat (Triticum aestivum L.) plants grown in contaminated field. Journal of Plant Growth Regulation 42, 6171-6182.
| Crossref | Google Scholar |

Soares C, de Sousa A, Pinto A, Azenha M, Teixeira J, Azevedo RA, Fidalgo F (2016) Effect of 24-epibrassinolide on ROS content, antioxidant system, lipid peroxidation and Ni uptake in Solanum nigrum L. under Ni stress. Environmental and Experimental Botany 122, 115-125.
| Crossref | Google Scholar |

Soliman M, Alhaithloul HA, Hakeem KR, Alharbi BM, El-Esawi M, Elkelish A (2019) Exogenous nitric oxide mitigates nickel-induced oxidative damage in eggplant by upregulating antioxidants, osmolyte metabolism, and glyoxalase systems. Plants 8(12), 562.
| Crossref | Google Scholar | PubMed |

Srivastava AK, Sablok G, Hackenberg M, Deshpande U, Suprasanna P (2017) Thiourea priming enhances salt tolerance through co-ordinated regulation of microRNAs and hormones in Brassica juncea. Scientific Reports 7(1), 45490.
| Crossref | Google Scholar |

Sytar O, Ghosh S, Malinska H, Zivcak M, Brestic M (2021) Physiological and molecular mechanisms of metal accumulation in hyperaccumulator plants. Physiologia Plantarum 173(1), 148-166.
| Crossref | Google Scholar | PubMed |

Talukdar D (2016) Exogenous thiourea modulates antioxidant defence and glyoxalase systems in lentil genotypes under arsenic stress. Journal of Plant Stress Physiology 2, 9-21.
| Crossref | Google Scholar |

Terrón-Camero LC, Peláez-Vico MÁ, Del-Val C, Sandalio LM, Romero-Puertas MC (2019) Role of nitric oxide in plant responses to heavy metal stress: exogenous application versus endogenous production. Journal of Experimental Botany 70(17), 4477-4488.
| Crossref | Google Scholar | PubMed |

Upadhyay MK, Majumdar A, Srivastava AK, Bose S, Suprasanna P, Srivastava S (2022) Antioxidant enzymes and transporter genes mediate arsenic stress reduction in rice (Oryza sativa L.) upon thiourea supplementation. Chemosphere 292, 133482.
| Crossref | Google Scholar | PubMed |

Valivand M, Amooaghaie R (2021) Calcium signaling confers nickel tolerance in Cucurbita pepo L. International Journal of Phytoremediation 23(4), 362-373.
| Crossref | Google Scholar | PubMed |

Wang Y, Yu Q, Li Y, Li J, Chen J, Liu Z, Huang J, Al-Harbi MS, Ali EF, Eissa MA (2021) Mechanisms of nitric oxide in the regulation of chilling stress tolerance in Camellia sinensis. Horticulturae 7(10), 410.
| Crossref | Google Scholar |

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. International Journal of Molecular Sciences 22(17), 9656.
| Crossref | Google Scholar | PubMed |

Waqas MA, Kaya C, Riaz A, Farooq M, Nawaz I, Wilkes A, Li Y (2019) Potential mechanisms of abiotic stress tolerance in crop plants induced by thiourea. Frontiers in Plant Science 10, 1336.
| Crossref | Google Scholar | PubMed |

Wei L, Zhang J, Wei S, Hu D, Liu Y, Feng L, Li C, Qi N, Wang C, Liao W (2022) Nitric oxide enhanced salt stress tolerance in tomato seedlings, involving phytohormone equilibrium and photosynthesis. International Journal of Molecular Sciences 23(9), 4539.
| Crossref | Google Scholar | PubMed |

Weisany W, Sohrabi Y, Heidari G, Siosemardeh A, Ghassemi-Golezani K (2012) Changes in antioxidant enzymes activity and plant performance by salinity stress and zinc application in soybean (Glycine max L). Plant Omics 5, 60-67.
| Google Scholar |

Xalxo R, Keshavkant S (2019) Melatonin, glutathione and thiourea attenuates lead and acid rain-induced deleterious responses by regulating gene expression of antioxidants in Trigonella foenum graecum L. Chemosphere 221, 1-10.
| Crossref | Google Scholar | PubMed |

Zhang X, Chen J, Liu X, Gao M, Chen X, Huang C (2019) Nickel uptake and distribution in Agropyron cristatum L. in the presence of pyrene. Ecotoxicology and Environmental Safety 174, 370-376.
| Crossref | Google Scholar | PubMed |

Zhao H, Jin Q, Wang Y, Chu L, Li X, Xu Y (2016) Effects of nitric oxide on alleviating cadmium stress in Typha angustifolia. Plant Growth Regulation 78(2), 243-251.
| Crossref | Google Scholar |