Abstract
Lead (Pb) is one of the most abundant toxic heavy metals, which have a serious impact on the growth and yield of crop plants. Nitric oxide (NO) is a natural signaling molecule that regulates the growth and productivity of plants. Here, exogenous NO was found to enhance Pb tolerance in watermelon, which resulted in more Pb restriction in roots and less up-translocated Pb to aerial parts. Pb stress, however, led to an increase in shoot dry weight, root biomass, root relative water content, leaf malondialdehyde (MDA) content, and the total soluble protein content in leaves and roots. By contrast, shoot height and fresh weight, leaf biomass, and root MDA content were decreased under Pb stress. NO treatments alleviated Pb toxicity by decreasing Pb translocation, enhancing root growth (elongation and biomass), inducing antioxidant enzymes activities, and reducing root MDA contents in watermelon seedlings. In conclusion, our results provide useful insights into the mechanism of Pb tolerance in cucurbit crops and information for the cultivation management of watermelon in the presence of this heavy metal (Pb).
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The authors confirm that data supporting this study’s findings are available in the manuscript.
References
Ahmad I, Akhtar MJ, Mehmood S, Akhter K, Tahir M, Saeed MF, Hussain MB, Hussain S (2018a) Combined application of compost and Bacillus sp. CIK-512 ameliorated the lead toxicity in radish by regulating the homeostasis of antioxidants and lead. Ecotoxicol Environ Saf 148:805–812. https://doi.org/10.1016/j.ecoenv.2017.11.054
Ahmad P, Ahanger MA, Alyemeni MN, Wijaya L, Alam P (2018b) Exogenous application of nitric oxide modulates osmolyte metabolism, antioxidants, enzymes of ascorbate-glutathione cycle and promotes growth under cadmium stress in tomato. Protoplasma 255:79–93. https://doi.org/10.1007/s00709-017-1132-x
Ahmad W, Ayyub CM, Shehzad MA, Ziaf K, Ijaz M, Sher A, Abbas T, Shafi J (2019) Supplemental potassium mediates antioxidant metabolism, physiological processes, and osmoregulation to confer salt stress tolerance in cabbage (Brassica oleracea L.). Hortic Environ Biotechnol 60:853–869. https://doi.org/10.1007/s13580-019-00172-2
Almasi A, Mohammadi M, Mosavi S, Eghbali S (2019) Phytoremediation potential of sewage sludge using native plants: Gossypium hirsutum L. and Solanum lycopersicum L. Int J Environ Sci Technol 16:6237–6246. https://doi.org/10.1007/s13762-018-2030-2
Amooaghaie R, Enteshari S (2017) Role of two-sided crosstalk between NO and H2S on improvement of mineral homeostasis and antioxidative defense in Sesamum indicum under lead stress. Ecotoxicol Environ Saf 139:210–218. https://doi.org/10.1016/j.ecoenv.2017.01.037
An Z, Liu F, Feng D, Xu Q, Zhou C (2019) Production of nitric oxide and phosphatidic acid is involved in activation of plasma membrane H+-ATPase in maize root tips in simulated drought dtress. Russ J Plant Physiol 66:50–58. https://doi.org/10.1134/S1021443719010035
Asgher M, Per TS, Masood A, Fatma M, Freschi L, Corpas FJ, Khan NA (2017) Nitric oxide signaling and its crosstalk with other plant growth regulators in plant responses to abiotic stress. Environ Sci Pollut Res 24:2273–2285. https://doi.org/10.1007/s11356-016-7947-8
Ashraf U, Mahmood MHR, Hussain S, Abbas F, Anjum SA, Tang X (2020) Lead (Pb) distribution and accumulation in different plant parts and its associations with grain Pb contents in fragrant rice. Chemosphere. https://doi.org/10.1016/j.chemosphere.2020.126003
Ashraf U, Kanu AS, Deng Q, Mo Z, Pan S, Tian H, Tang X (2017) Lead (Pb) toxicity; physio-biochemical mechanisms, grain yield, quality, and Pb distribution proportions in scented rice. Front Plant Sci 8:259. https://doi.org/10.3389/fpls.2017.00259
Azhar N, Ashraf MY, Hussain M, Ashraf M, Ahmed R (2009) EDTA-induced improvement in growth and water relations of sunflower (Helianthus annuus L.) plants grown in lead contaminated medium. Pak J Bot 41:3065–3074
Bai X, Dong Y, Wang Q, Xu L, Kong J, Liu S (2015) Effects of lead and nitric oxide on photosynthesis, antioxidative ability, and mineral element content of perennial ryegrass. Biol Plant 59:163–170. https://doi.org/10.1007/s10535-014-0476-8
Bali S, Jamwal VL, Kohli SK, Kaur P, Tejpal R, Bhalla V, Ohri P, Gandhi SG, Bhardwaj R et al (2019) Jasmonic acid application triggers detoxification of lead (Pb) toxicity in tomato through the modifications of secondary metabolites and gene expression. Chemosphere 235:734–748. https://doi.org/10.1016/j.chemosphere.2019.06.188
Beligni MV, Lamattina L (2000) Nitric oxide stimulates seed germination and de-etiolation, and inhibits hypocotyl elongation, three light-inducible responses in plants. Planta 210:215–221. https://doi.org/10.1007/PL00008128
Bharwana SA, Ali S, Farooq MA, Iqbal N, Hameed A, Abbas F, Ahmad MSA (2014) Glycine betaine-induced lead toxicity tolerance related to elevated photosynthesis, antioxidant enzymes suppressed lead uptake and oxidative stress in cotton. Turk J Bot 38:281–292. https://doi.org/10.3906/bot-1304-65
Bradford MM (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/10.1016/0003-2697(76)90527-3
Cakmak I, Horst WJ (1991) Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiol Plant 83:463–468. https://doi.org/10.1111/j.1399-3054.1991.tb00121.x
Cândido GS, Martins GC, Vasques IC, Lima FR, Pereira P, Engelhardt MM, Reis RH, Marques JJ (2020) Toxic effects of lead in plants grown in Brazilian soils. Ecotoxicology. https://doi.org/10.1007/s10646-020-02174-8
Corpas FJ, Del Río LA, Palma JM (2019) Plant peroxisomes at the crossroad of NO and H2O2 metabolism. J Integr Plant Biol 61:803–816. https://doi.org/10.1111/jipb.12772
Devi SS, Saha B, Awasthi JP, Regon P, Panda SK (2020) Redox status and oxalate exudation determines the differential tolerance of two contrasting varieties of ‘Assam tea’ [Camelia sinensis (L.) O. Kuntz] in response to aluminum toxicity. Horticult Environ Biotechnol. https://doi.org/10.1007/s13580-020-00241-x
Dey SK, Dey J, Patra S, Pothal D (2007) Changes in the antioxidative enzyme activities and lipid peroxidation in wheat seedlings exposed to cadmium and lead stress. Braz J Plant Physiol 19:53–60. https://doi.org/10.1590/S1677-04202007000100006
Dias MC, Mariz-Ponte N, Santos C (2019) Lead induces oxidative stress in Pisum sativum plants and changes the levels of phytohormones with antioxidant role. Plant Physiol Biochem 137:121–129. https://doi.org/10.1016/j.plaphy.2019.02.005
Doganlar ZB, Demir K, Basak H, Gul I (2010) Effects of salt stress on pigment and total soluble protein contents of three different tomato cultivars. Afr J Agric Res 5:2056–2065
El-Moshaty FB, Pike S, Novacky A, Sehgal O (1993) Lipid peroxidation and superoxide production in cowpea (Vigna unguiculata) leaves infected with tobacco ringspot virus or southern bean mosaic virus. Physiol Mol Plant Pathol 43:109–119. https://doi.org/10.1006/pmpp.1993.1044
Esim N, Atici O (2013) Nitric oxide alleviates boron toxicity by reducing oxidative damage and growth inhibition in maize seedlings (‘Zea mays L.). Aust J Crop Sci 7:1085. https://doi.org/10.18811/ijpen.v5i01.3
Fahr M, Laplaze L, Bendaou N, Hocher V, El Mzibri M, Bogusz D, Smouni A (2013) Effect of lead on root growth. Front Plant Sci. https://doi.org/10.3389/fpls.2013.00175
Fan H, Guo S, Jiao Y, Zhang R, Li J (2007) Effects of exogenous nitric oxide on growth, active oxygen species metabolism, and photosynthetic characteristics in cucumber seedlings under NaCl stress. Front Mech Eng China 1:308–314. https://doi.org/10.1007/s11703-007-0052-5
FAO UN (2010) Top production quantity in the world, Title 17. Top production on watermelons in 2010. 18 Apr. 2012.
Farag M, Najeeb U, Yang J, Hu Z, Fang ZM (2017) Nitric oxide protects carbon assimilation process of watermelon from boron-induced oxidative injury. Plant Physiol Biochem 111:166–173. https://doi.org/10.1016/j.plaphy.2016.11.024
Figlioli F, Sorrentino MC, Memoli V, Arena C, Maisto G, Giordano S, Capozzi F, Spagnuolo V (2019) Overall plant responses to Cd and Pb metal stress in maize: Growth pattern, ultrastructure, and photosynthetic activity. Environ Sci Pollut Res 26:1781–1790. https://doi.org/10.1007/s11356-018-3743-y
Filippou P, Bouchagier P, Skotti E, Fotopoulos V (2014) Proline and reactive oxygen/nitrogen species metabolism is involved in the tolerant response of the invasive plant species Ailanthus altissima to drought and salinity. Environ Exp Bot 97:1–10. https://doi.org/10.1016/j.envexpbot.2013.09.010
Gottesfeld P, Were FH, Adogame L, Gharbi S, San D, Nota MM, Kuepouo G (2018) Soil contamination from lead battery manufacturing and recycling in seven African countries. Environ Res 161:609–614. https://doi.org/10.1016/j.envres.2017.11.055
Hamid N, Bukhari N, Jawaid F (2010) Physiological responses of Phaseolus vulgaris to different lead concentrations. Pak J Bot 42:239–246
Hasanuzzaman M, Fujita M (2013) Exogenous sodium nitroprusside alleviates arsenic-induced oxidative stress in wheat (Triticum aestivum L.) seedlings by enhancing antioxidant defense and glyoxalase system. Ecotoxicology 22:584–596. https://doi.org/10.1007/s10646-013-1050-4
Hassan M, Mansoor S (2014) Oxidative stress and antioxidant defense mechanism in mung bean seedlings after lead and cadmium treatments. Turk J Agric for 38:55–61. https://doi.org/10.3906/tar-1212-4
Hatamzadeh A, Molaahmad Nalousi A, Ghasemnezhad M, Biglouei M (2015) The potential of nitric oxide for reducing oxidative damage induced by drought stress in two turfgrass species, creeping bentgrass and tall fescue. Grass Forage Sci 70:538–548. https://doi.org/10.1111/gfs.12135
Hattab S, Hattab S, Flores-Casseres ML, Boussetta H, Doumas P, Hernandez LE, Banni M (2016) Characterisation of lead-induced stress molecular biomarkers in Medicago sativa plants. Environ Exp Bot 123:1–12. https://doi.org/10.1016/j.envexpbot.2015.10.005
Hayat S, Hasan SA, Mori M, Fariduddin Q, Ahmad A (2010) Nitric oxide: chemistry, biosynthesis, and physiological role. Nitric Oxide Plant Physiol. https://doi.org/10.1002/9783527629138.ch1
He S, He Z, Wu Q, Wang L, Zhang X (2015) Effects of GA3 on plant physiological properties, extraction, subcellular distribution and chemical forms of Pb in Lolium perenne. Int J Phytorem 17:1153–1159. https://doi.org/10.1080/15226514.2015.1045124
Inoue H, Fukuoka D, Tatai Y, Kamachi H, Hayatsu M, Ono M, Suzuki S (2013) Properties of lead deposits in cell walls of radish (Raphanus sativus) roots. J Plant Res 126:51–61. https://doi.org/10.1007/s10265-012-0494-6
Islam E, Yang X, Li T, Liu D, Jin X, Meng F (2007) Effect of Pb toxicity on root morphology, physiology and ultrastructure in the two ecotypes of Elsholtzia argyi. J Hazard Mater 147:806–816. https://doi.org/10.1016/j.jhazmat.2007.01.117
Ismaiel MM, Said AA (2018) Tolerance of Pseudochlorella pringsheimii to Cd and Pb stress: role of antioxidants and biochemical contents in metal detoxification. Ecotoxicol Environ Saf 164:704–712. https://doi.org/10.1016/j.ecoenv.2018.08.088
Ismail GSM (2012) Protective role of nitric oxide against arsenic-induced damages in germinating mung bean seeds. Acta Physiol Plant 34:1303–1311. https://doi.org/10.1007/s11738-012-0927-9
Jafarnezhad-Moziraji Z, Saeidi-Sar S, Dehpour A, Masoudian N (2017) Protective effects of exogenous nitric oxide against lead toxicity in lemon balm (Melissa officinalis L.). Appl Ecol Environ Res 15:1605–1621. https://doi.org/10.15666/aeer/1504_16051621
Jayasri M, Suthindhiran K (2017) Effect of zinc and lead on the physiological and biochemical properties of aquatic plant Lemna minor: its potential role in phytoremediation. Appl Water Sci 7:1247–1253. https://doi.org/10.1007/s13201-015-0376-x
Jiang W, Liu D (2010) Pb-induced cellular defense system in the root meristematic cells of Allium sativum L. BMC Plant Biol 10:40. https://doi.org/10.1186/1471-2229-10-40
Kabir M, Iqbal MZ, Shafiq M, Farooqi Z (2008) Reduction in germination and seedling growth of Thespesia populnea L., caused by lead and cadmium treatments. Pak J Bot 40:2419–2426
Kausar F, Shahbaz M, Ashraf M (2013) Protective role of foliar-applied nitric oxide in Triticum aestivum under saline stress. Turk J Bot 37:1155–1165. https://doi.org/10.3906/bot-1301-17
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 Hortic 255:52–60. https://doi.org/10.1016/j.scienta.2019.05.029
Khan M, Khan MD, Ali B, Muhammad N, Zhu S-J (2014) Differential physiological and ultrastructural responses of cottonseeds under Pb toxicity. Polish J Environ Stud 23:2063–2070. https://doi.org/10.15244/pjoes/23798
Khan I, Iqbal M, Ashraf MY, Ashraf MA, Ali S (2016) Organic chelants-mediated enhanced lead (Pb) uptake and accumulation is associated with higher activity of enzymatic antioxidants in spinach (Spinacea oleracea L.). J Hazard Mater 317:352–361. https://doi.org/10.1016/j.jhazmat.2016.06.007
Khan J, Yang Y, Fu Q, Shao W, Wang J, Shen L, Huai Y, Malangisha GK, Ali A et al (2020) Screening of watermelon varieties for Lead tolerance at the seedling stage. HortScience 1:1–12. https://doi.org/10.21273/HORTSCI14855-20
Khator K, Saxena I, Shekhawat GS (2020) Nitric oxide induced Cd tolerance and phytoremediation potential of B. juncea by the modulation of antioxidant defense system and ROS detoxification. Biometals. https://doi.org/10.1007/s10534-020-00259-9
Kopittke PM, Asher CJ, Menzies NW (2007) Toxic effects of Ni2+ on growth of cowpea (Vigna unguiculata). Plant Soil 292:283–289. https://doi.org/10.1007/s11104-007-9226-4
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. https://doi.org/10.1016/j.plaphy.2003.09.003
Kotapati KV, Palaka BK, Ampasala DR (2017) Alleviation of nickel toxicity in finger millet (Eleusine coracana L.) germinating seedlings by exogenous application of salicylic acid and nitric oxide. Crop J 5:240–250. https://doi.org/10.1016/j.cj.2016.09.002
Lee HJ, Lee JH, Lee SG, An S, Lee HS, Choi CK, Kim SK (2019) Foliar application of biostimulants affects physiological responses and improves heat stress tolerance in Kimchi cabbage. Hortic Environ Biotechnol 60:841–851. https://doi.org/10.1007/s13580-019-00193-x
Li C, Li T, Zhang D, Jiang L, Shao Y (2013) Exogenous nitric oxide effect on fructan accumulation and FBEs expression in chilling-sensitive and chilling-resistant wheat. Environ Exp Bot 86:2–8. https://doi.org/10.1016/j.envexpbot.2011.12.032
Li Y, Zhou C, Huang M, Luo J, Hou X, Wu P, Ma X (2016) Lead tolerance mechanism in Conyza canadensis: subcellular distribution, ultrastructure, antioxidative defense system, and phytochelatins. J Plant Res 129:251–262. https://doi.org/10.1007/s10265-015-0776-x
Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Portland Press Limited. https://doi.org/10.1042/bst0110591
Ma L, Sun J, Yang Z, Wang L (2015) Heavy metal contamination of agricultural soils affected by mining activities around the Ganxi River in Chenzhou, Southern China. Environ Monit Assess 187:731. https://doi.org/10.1007/s10661-015-4966-8
Mahdavian K, Ghaderian SM, Schat H (2016) Pb accumulation, Pb tolerance, antioxidants, thiols, and organic acids in metallicolous and non-metallicolous Peganum harmala L. under Pb exposure. Environ Exp Bot 126:21–31. https://doi.org/10.1016/j.envexpbot.2016.01.010
Małkowski E, Kita A, Galas W, Karcz W, Kuperberg JM (2002) Lead distribution in corn seedlings (Zea mays L.) and its effect on growth and the concentrations of potassium and calcium. Plant Growth Regul 37:69–76. https://doi.org/10.1023/A:1020305400324
Misra A, Misra M, Singh R (2011) Nitric oxide ameliorates stress responses in plants. Plant Soil Environ 57:95–100. https://doi.org/10.17221/202/2010-pse
Mittova V, Guy M, Tal M, Volokita M (2002) Response of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii to salt-dependent oxidative stress: increased activities of antioxidant enzymes in root plastids. Free Radical Res 36:195–202. https://doi.org/10.1080/10715760290006402
Nabi RBS, Tayade R, Hussain A, Kulkarni KP, Imran QM, Mun B-G, Yun B-W (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
Nas F, Ali M (2018) The effect of lead on plants in terms of growing and biochemical parameters: a review. MOJ Eco Environ Sci 3:265–268. https://doi.org/10.15406/mojes.2018.03.00098
Natasha SM, Farooq ABU, Rabbani F, Khalid S, Dumat C (2020) Risk assessment and biophysiochemical responses of spinach to foliar application of lead oxide nanoparticles: a multivariate analysis. Chemosphere 245:125605. https://doi.org/10.1016/j.chemosphere.2019.125605
Nihad K, Berwal MK, Hebbar KB, Bhat R, Haris AA, Ramesh S (2019) Photochemical and biochemical responses of heliconia (Heliconia stricta ‘Iris’) to different light intensities in a humid coastal environment. Hortic Environ Biotechnol 60:799–808. https://doi.org/10.1007/s13580-019-00173-1
Okant M, Kaya C (2019) The role of endogenous nitric oxide in melatonin-improved tolerance to lead toxicity in maize plants. Environ Sci Pollut Res 26:11864–11874. https://doi.org/10.1007/s11356-019-04517-3
Phang C, Leung DW, Taylor HH, Burritt DJ (2011) The protective effect of sodium nitroprusside (SNP) treatment on Arabidopsis thaliana seedlings exposed to toxic level of Pb is not linked to avoidance of Pb uptake. Ecotoxicol Environ Saf 74:1310–1315. https://doi.org/10.1016/j.ecoenv.2011.02.006
Pidatala VR, Li K, Sarkar D, Wusirika R, Datta R (2018) Comparative metabolic profiling of vetiver (Chrysopogon zizanioides) and maize (Zea mays) under lead stress. Chemosphere 193:903–911. https://doi.org/10.1016/j.chemosphere.2017.11.087
Piotrowska A, Bajguz A, Godlewska-Żyłkiewicz B, Czerpak R, Kamińska M (2009) Jasmonic acid as modulator of lead toxicity in aquatic plant Wolffia arrhiza (Lemnaceae). Environ Exp Bot 66:507–513. https://doi.org/10.1016/j.envexpbot.2009.03.019
Plewa MJ, Smith SR, Wagner ED (1991) Diethyldithiocarbamate suppresses the plant activation of aromatic amines into mutagens by inhibiting tobacco cell peroxidase. Mutat Res Fundam Mol Mech Mutagenesis 247:57–64. https://doi.org/10.1016/0027-5107(91)90033-k
Pourrut B, Shahid M, Dumat C, Winterton P, Pinelli E (2011a) Lead uptake, toxicity, and detoxification in plants. In: RevEnviron Contam T 213, Vol 213. Springer, pp 113–136. https://doi.org/10.1007/978-1-4419-9860-6_4
Pourrut B, Shahid M, Dumat C, Winterton P, Pinelli E (2011b) Lead uptake, toxicity, and detoxification in plants. In: Reviews of environmental contamination and toxicology, vol 213. Springer, pp 113–136. https://doi.org/10.1007/978-1-4419-9860-6_4
Pourrut B, Shahid M, Douay F, Dumat C, Pinelli E (2013) Molecular mechanisms involved in lead uptake, toxicity and detoxification in higher plants. In: Heavy metal stress in plants. Springer, pp 121–147. https://doi.org/10.1007/978-3-642-38469-1_7
Sadeghipour O (2016) Pretreatment with nitric oxide reduces lead toxicity in cowpea (Vigna unguiculata [L.] walp.). Arch Biol Sci 68:165–175. https://doi.org/10.2298/ABS150325139S
Sadeghipour O (2017) Nitric oxide increases Pb tolerance by lowering Pb uptake and translocation as well as phytohormonal changes in cowpea (Vigna unguiculata (L.) Walp). Sains Malaysiana 46:189–195. https://doi.org/10.17576/jsm-2017-4602-02
Seregin IV, Shpigun LK, Ivanov VB (2004) Distribution and toxic effects of cadmium and lead on maize roots. Russ J Plant Physl 51:525–533. https://doi.org/10.1023/B:RUPP.0000035747.42399.84
Shahid M, Farooq ABU, Rabbani F, Khalid S, Dumat C (2020) Risk assessment and biophysiochemical responses of spinach to foliar application of lead oxide nanoparticles: a multivariate analysis. Chemosphere 245:125605. https://doi.org/10.1016/j.chemosphere.2019.125605
Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot. https://doi.org/10.1155/2012/217037
Sharma A, Soares C, Sousa B, Martins M, Kumar V, Shahzad B, Sidhu GP, Bali AS, Asgher M et al (2019) Nitric oxide-mediated regulation of oxidative stress in plants under metal stress: a review on molecular and biochemical aspects. Physiol Plant. https://doi.org/10.1111/ppl.13004
Sheng Y, Luan F, Zhang F, Davis AR (2012) Genetic diversity within Chinese watermelon ecotypes compared with germplasm from other countries. J Am Soc Hortic Sci 137:144–151. https://doi.org/10.21273/jashs.137.3.144
Shi X, Wang S, Wang D, Sun H, Chen Y, Liu J, Jiang Z (2019) Woody species Rhus chinensis Mill. seedlings tolerance to Pb: Physiological and biochemical response. J Environ Sci 78:63–73. https://doi.org/10.1016/j.jes.2018.07.003
Siddiqui MH, Al-Whaibi MH, Basalah MO (2011) Role of nitric oxide in tolerance of plants to abiotic stress. Protoplasma 248:447–455. https://doi.org/10.1007/s00709-010-0206-9
Singh R, Tripathi R, Dwivedi S, Kumar A, Trivedi P, Chakrabarty D (2010) Lead bioaccumulation potential of an aquatic macrophyte Najas indica are related to antioxidant system. Biores Technol 101:3025–3032. https://doi.org/10.1016/j.biortech.2009.12.031
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 8:562. https://doi.org/10.3390/plants8120562
Stoeva N, Berova M, Zlatev Z (2005) Effect of arsenic on some physiological parameters in bean plants. Biol Plant 49:293–296. https://doi.org/10.1007/s10535-005-3296-z
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. J Exp Bot 70:4477–4488. https://doi.org/10.1093/jxb/erz184
Tunc-Ozdemir M, Miller G, Song L, Kim J, Sodek A, Koussevitzky S, Misra AN, Mittler R, Shintani D (2009) Thiamin confers enhanced tolerance to oxidative stress in Arabidopsis. Plant Physiol 151:421–432. https://doi.org/10.1104/pp.109.140046
Venkatachalam P, Jayalakshmi N, Geetha N, Sahi SV, Sharma NC, Rene ER, Sarkar SK, Favas PJC (2017) Accumulation efficiency, genotoxicity and antioxidant defense mechanisms in medicinal plant Acalypha indica L. under lead stress. Chemosphere 171:544–553. https://doi.org/10.1016/j.chemosphere.2016.12.092
Wang X-Y, Shen W-B, Xu L-L (2004) Exogenous nitric oxide alleviates osmotic stress-induced membrane lipid peroxidation in wheat seedling leaves. J Plant Physiol Mol Biol 30:195–200
Wang Q, Liang X, Dong Y, Xu L, Zhang X, Hou J, Fan Z (2013) Effects of exogenous nitric oxide on cadmium toxicity, element contents and antioxidative system in perennial ryegrass. Plant Growth Regul 69:11–20. https://doi.org/10.4067/s0718-95162018005000601
Wang J, Chen J, Pan K (2013) Effect of exogenous abscisic acid on the level of antioxidants in Atractylodes macrocephala Koidz under lead stress. Environ Sci Pollut Res 20:1441–1449. https://doi.org/10.1007/s11356-012-1048-0
Wang Y-j, Dong Y-X, Wang J, Cui X-m (2016) Alleviating effects of exogenous NO on tomato seedlings under combined Cu and Cd stress. Environ Sci Pollut Res 23:4826–4836. https://doi.org/10.1007/s11356-015-5525-0
Wei B, Yang L (2010) A review of heavy metal contaminations in urban soils, urban road dusts and agricultural soils from China. Microchem J 94:99–107. https://doi.org/10.1016/j.microc.2009.09.014
Wei L, Zhang J, Wang C, Liao W (2019) Recent progress in the knowledge on the alleviating effect of nitric oxide on heavy metal stress in plants. Plant Physiol Biochem. https://doi.org/10.1016/j.plaphy.2019.12.021
Wei L, Zhang M, Wei S, Zhang J, Wang C, Liao W (2020) Roles of nitric oxide in heavy metal stress in plants: cross-talk with phytohormones and protein S-nitrosylation. Environ Pollut. https://doi.org/10.1016/j.envpol.2020.113943
Winska-Krysiak M, Koropacka K, Gawronski S (2015) Determination of the tolerance of sunflower to lead-induced stress. J Elementol. https://doi.org/10.5601/jelem.2014.19.4.721
Xiong J, An L, Lu H, Zhu C (2009) Exogenous nitric oxide enhances cadmium tolerance of rice by increasing pectin and hemicellulose contents in root cell wall. Planta 230:755–765. https://doi.org/10.1007/s00425-009-0984-5
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. https://doi.org/10.1007/s11104-009-0011-4
Zhang W, Zhang F, Raziuddin R, Gong H, Yang Z, Lu L, Ye Q, Zhou W (2008) Effects of 5-aminolevulinic acid on oilseed rape seedling growth under herbicide toxicity stress. J Plant Growth Regul 27:159–169. https://doi.org/10.1007/s00344-008-9042-y
Zhang Y, Han X, Chen X, Jin H, Cui X (2009) Exogenous nitric oxide on antioxidative system and ATPase activities from tomato seedlings under copper stress. Sci Hortic 123:217–223. https://doi.org/10.1016/j.scienta.2009.08.015
Zhao L, Li T, Yu H, Chen G, Zhang X, Zheng Z, Li J (2015) Changes in chemical forms, subcellular distribution, and thiol compounds involved in Pb accumulation and detoxification in Athyrium wardii (Hook.). Environ Sci Pollut Res Int 22:12676–12688. https://doi.org/10.1007/s11356-015-4464-0
Zhivotovsky OP, Kuzovkina JA, Schulthess CP, Morris T, Pettinelli D, Ge M (2011) Hydroponic screening of willows (Salix L.) for lead tolerance and accumulation. Int J Phytorem 13:75–94. https://doi.org/10.1080/15226511003671361
Zhong B, Chen J, Shafi M, Guo J, Wang Y, Wu J, Ye Z, He L, Liu D (2017) Effect of lead (Pb) on antioxidation system and accumulation ability of Moso bamboo (Phyllostachys pubescens). Ecotoxicol Environ Saf 138:71–77. https://doi.org/10.1016/j.ecoenv.2016.12.020
Zhou J, Zhang Z, Zhang Y, Wei Y, Jiang Z (2018) Effects of lead stress on the growth, physiology, and cellular structure of privet seedlings. PLoS ONE. https://doi.org/10.1371/journal.pone.0191139
Acknowledgements
The authors thank Engineer Dr. Afed Ullah Khan, School of Municipal and Environmental Engineering, Harbin Institute of Technology, China, and Mr. Raza Ullah Khan, Department of Chemistry, Institute for Computation in Molecular and Materials Science, Nanjing University of Science and Technology, Nanjing, China for technical comments that greatly improved the manuscript. This work was supported by the earmarked fund for Modern Agro-Industry Technology Research System of China (CARS-26-17), The National Key Research and Development Program of China (2018YFD0201300, 2019YFD1000300), National Natural Science Foundation of China (31501782, 31672175, and 31372077), Key Science and Technology Breeding Program of Agricultural New Variety of Zhejiang Province (2016C02051-4-1).
Author information
Authors and Affiliations
Contributions
Z.H. and M.Z. conceived and designed the study; J.K. conducted all experiments and write the manuscript; Z.H. and J.K. participated in results analysis; A.A., A.M. and G.K.M. helped perform parts of experiments; all authors reviewed the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Ethical approval
The work presented in this study does not involve any human participants or animal use which requires ethical approval.
Informed consent
There were no human participants and no consent was required.
Additional information
Communicated by Sung Kyeom Kim.
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
About this article
Cite this article
Khan, J., Malangisha, G.K., Ali, A. et al. Nitric oxide alleviates lead toxicity by inhibiting lead translocation and regulating root growth in watermelon seedlings. Hortic. Environ. Biotechnol. 62, 701–714 (2021). https://doi.org/10.1007/s13580-021-00346-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13580-021-00346-x