Abstract
Nitric oxide (NO), a signaling molecule with diverse physiological functions, improves immunity of the plant against different environmental stresses. Heavy metal stress-induced structural and functional damages in cells are common consequences. Seed germination and seedlings development are crucial phases in the life cycle of a plant. The present experiment was designed to investigate how NO suppresses hexavalent chromium Cr(VI)-provoked impairment in the key processes during seed germination and seedlings development of tomato. This study reports that Cr(VI) stress significantly impaired seed germination attributes and the activity of hydrolyzing enzymes, such as α-amylase (α-A) and protease (Pr). However, exogenous NO donor sodium nitroprusside substantially improved seed germination parameters and upregulation of α-A and Pr. Furthermore, NO improved the content of nitrogen (N), NO, and proline (Pro), and modulated the activity of enzymes involved in Pro and N-assimilation. Under Cr(VI) toxicity conditions, NO improved the content of metal ligation compounds (non-protein thiols and total thiols), ascorbate and glutathione (GSH), and maintained higher content of GSH in glutathione pool (GSH:GSSG) and suppressed the formation of 4-hydroxy-2-nonenal and protein carbonylation, and electrolyte leakage. It may be concluded that NO improved the activity of hydrolyzing and Pro and N-metabolism enzymes. Application of NO also enhanced non-enzymatic antioxidants, and 2,2-diphenyl-1-picrylhydrazyl radical scavenging activity under Cr(VI) toxicity conditions, thereby improved enhanced seed germination and seedlings vigor.
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References
Adrees M, Ali S, Iqbal M, Aslam Bharwana S, Siddiqi Z, Farid M, Ali Q, Saeed R, Rizwan M (2015) Mannitol alleviates chromium toxicity in wheat plants in relation to growth, yield, stimulation of anti-oxidative enzymes, oxidative stress and Cr uptake in sand and soil media. Ecotoxicol Environ Saf 122:1–8. https://doi.org/10.1016/j.ecoenv.2015.07.003
Ahmad R, Ali S, Rizwan M, Dawood M, Farid M, Hussain A, Wijaya L, Alyemeni MN, Ahmad P (2020) Hydrogen sulfide alleviates chromium stress on cauliflower by restricting its uptake and enhancing antioxidative system. Physiol Plant 168(2):289–300. https://doi.org/10.1111/ppl.13001
Akram NA, Shafiq F, Ashraf M (2017) Ascorbic acid—a potential oxidant scavenger and its role in plant development and abiotic stress tolerance. Front Plant Sci 8:613. https://doi.org/10.3389/fpls.2017.00613
Alamri S, Ali HM, Khan MIR, Singh VP, Siddiqui MH (2020) Exogenous nitric oxide requires endogenous hydrogen sulfide to induced the resilience through sulfur assimilation in tomato seedlings under hexavalent chromium toxicity. Plant Physiol Biochem 155:20–34
Alamri SA, Siddiqui MH, Al-Khaishany MY, Khan MN, Ali HM, Alakeel KA (2019) Nitric oxide-mediated cross-talk of proline and heat shock proteins induce thermotolerance in Vicia faba L. Environ Exp Bot 161:290–302. https://doi.org/10.1016/j.envexpbot.2018.06.012
Ali-Rachedi S, Bouinot D, Wagner MH, Bonnet M, Sotta B, Grappin P, Jullien M (2004) Changes in endogenous abscisic acid levels during dormancy release and maintenance of mature seeds: studies with the Cape Verde Islands ecotype, the dormant model of Arabidopsis thaliana. Planta 219(3):479–488. https://doi.org/10.1007/s00425-004-1251-4
Amin H, Ahmed Arain B, Abbasi MS, Amin F, Jahangir TM, Soomro NU (2019) Evaluation of chromium phyto-toxicity, phyto-tolerance, and phyto-accumulation using biofuel plants for effective phytoremediation. Int J Phytoremediation 21(4):352–363. https://doi.org/10.1080/15226514.2018.1524837
Arc E, Galland M, Godin B, Cueff G, Rajjou L (2013) Nitric oxide implication in the control of seed dormancy and germination. Front Plant Sci 4:346. https://doi.org/10.3389/fpls.2013.00346
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 Int 24(3):2273–2285. https://doi.org/10.1007/s11356-016-7947-8
Ashraf A, Bibi I, Niazi NK, Ok YS, Murtaza G, Shahid M, Kunhikrishnan A, Li D, Mahmood T (2017) Chromium(VI) sorption efficiency of acid-activated banana peel over organo-montmorillonite in aqueous solutions. Int J Phytoremediation 19(7):605–613. https://doi.org/10.1080/15226514.2016.1256372
Bali S, Jamwal VL, Kohli SK, Kaur P, Tejpal R, Bhalla V, Ohri P, Gandhi SG, Bhardwaj R, Al-Huqail AA, Siddiqui MH, Ali HM, Ahmad P (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
Bates LS, Waldren RP, Teare ID (1972) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207
Beligni MV, Lamattina L (2001) Nitric oxide: a non-traditional regulator of plant growth. Trends Plant Sci 6(11):508–509. https://doi.org/10.1016/s1360-1385(01)02156-2
Bethke PC, Libourel IG, Jones RL (2006) Nitric oxide reduces seed dormancy in Arabidopsis. J Exp Bot 57(3):517–526. https://doi.org/10.1093/jxb/erj060
Bhalerao SA, Sharma AS (2015) Chromium: as an environmental pollutant. Int J Curr Microbiol Appl Sci 4(4):732–746
Bishnoi NR, Dua A, Gupta VK, Sawhney SK (1993) Effect of chromium on seed germination, seedling growth and yield of peas. Agric Ecosyst Environ 47:47–57
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/10.1006/abio.1976.9999
Brasili E, Bavasso I, Petruccelli V, Vilardi G, Valletta A, Bosco CD, Gentili A, Pasqua G, Palma LD (2020) Remediation of hexavalent chromium contaminated water through zero-valent iron nanoparticles and effects on tomato plant growth performance. Sci Rep 10:1920. https://doi.org/10.1038/s41598-020-58639-7
Buet A, Galatro A, Ramos-Artuso F, Simontacchi M (2019) Nitric oxide and plant mineral nutrition: current knowledge. J Exp Bot 70(17):4461–4476. https://doi.org/10.1093/jxb/erz129
Castro-Ruiz JE, Rojas-Molina A, Luna-Vazquez FJ, Rivero-Cruz F, Garcia-Gasca T, Ibarra-Alvarado C (2017) Affinin (spilanthol), isolated from Heliopsis longipes, induces vasodilation via activation of gasotransmitters and prostacyclin signaling pathways. Int J Mol Sci 18(1):218. https://doi.org/10.3390/ijms18010218
Chandrakar V, Dubey A, Keshavkant S (2018) Modulation of arsenic-induced oxidative stress and protein metabolism by diphenyleneiodonium, 24-epibrassinolide and proline in Glycine max L. Acta Botanica Croatica 77(1):51–61
Chandrakar V, Naithani SC, Keshavkant S (2016) Arsenic-induced metabolic disturbances and their mitigation mechanisms in crop plants: a review. Biologia 71:367–377
Charest C, Phan CT (1990) Cold acclimation of wheat (Triticum aestivum): properties of enzymes involved in proline metabolism. Physiol Plant 80(2):159–168
Corradi MG, Bianchi A, Albasini A (1993) Chromium toxicity in Salvia sclarea—I. Effects of hexavalent chromium on seed germination and seedling development. Environ Exp Bot 33(3):405–413
Danish S, Kiran S, Fahad S, Ahmad N, Ali MA, Tahir FA, Rasheed MK, Shahzad K, Li X, Wang D, Mubeen M, Abbas S, Munir TM, Hashmi MZ, Adnan M, Saeed B, Saud S, Khan MN, Ullah A, Nasim W (2019) Alleviation of chromium toxicity in maize by Fe fortification and chromium tolerant ACC deaminase producing plant growth promoting rhizobacteria. Ecotoxicol Environ Saf 185:109706. https://doi.org/10.1016/j.ecoenv.2019.109706
Davies FT, Puryear JD, Newton RJ, Egilla JN, Grossi JAS (2002) Mycorrhizal fungi increase chromium uptake by sunflower plants: influence on tissue mineral concentration, growth, and gas exchange. J Plant Nutr 25:2389–2407
Ding AH, Nathan CF, Stuehr DJ (1988) Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. J Immunol 141(7):2407–2412
Dua A, Sawhney SK (1991) Effect of chromium on activities of hydrolytic enzymes in germinating pea seeds. Environ Exp Bot 31(2):133–139
Eastin EF (1978) Total nitrogen determination of plant materialcontaining nitrate. Anal Biochem 85:591–594
Ferreira IC, Baptista P, Vilas-Boas M, Barros L (2007) Free-radical scavenging capacity and reducing power of wild edible mushrooms from northeast Portugal: individual cap and stipe activity. Food Chem 100(4):1511–1516
Garcia-Mata C, Lamattina L (2013) Gasotransmitters are emerging as new guard cell signaling molecules and regulators of leaf gas exchange. Plant Sci 201–202:66–73. https://doi.org/10.1016/j.plantsci.2012.11.007
He H, Li Y, He LF (2019) Role of nitric oxide and hydrogen sulfide in plant aluminum tolerance. Biometals 32(1):1–9. https://doi.org/10.1007/s10534-018-0156-9
Hendricks SB, Taylorson RB (1974) Promotion of seed germination by nitrate, nitrite, hydroxylamine, and ammonium salts. Plant Physiol 54(3):304–309. https://doi.org/10.1104/pp.54.3.304
Henriques FS (2010) Changes in biomass and photosynthetic parameters of tomato plants exposed to trivalent and hexavalent chromium. Biol Plant 54:583–586
Hourmant A, Pradet A (1981) Oxidative phosphorylation in germinating lettuce seeds (Lactuca sativa) during the first hours of imbibition. Plant Physiol 68(3):631–635. https://doi.org/10.1104/pp.68.3.631
Hu S, Gu H, Cui C, Ji R (2016) Toxicity of combined chromium(VI) and phenanthrene pollution on the seed germination, stem lengths, and fresh weights of higher plants. Environ Sci Pollut Res Int 23(15):15227–15235. https://doi.org/10.1007/s11356-016-6701-6
Hu XY, Neill SJ, Cai WM, Tang ZC (2003) NO-mediated hypersensitive responses of rice suspension cultures induced by incompatible elicitor. Chin Sci Bull 48:358–363
Israr M, Sahi S, Datta R, Sarkar D (2006) Bioaccumulation and physiological effects of mercury in Sesbania drummondii. Chemosphere 65(4):591–598. https://doi.org/10.1016/j.chemosphere.2006.02.016
Jaworski EG (1971) Nitrate reductase assay in intact plant tissues. Biochem Biophys Res Commun 43(6):1274–1279. https://doi.org/10.1016/s0006-291x(71)80010-4
Joshi R (2018) Role of enzymes in seed germination. Int J Creat Res Thoughts (2320–2882) 6:1481–1485
Kalemba EM, Pukacka S (2014) Carbonylated proteins accumulated as vitality decreases during long-term storage of beech (Fagus sylvatica L.) seeds. Trees 28:503–515
Kandziora-Ciupa M, Ciepal R, Nadgorska-Socha A, Barczyk G (2016) Accumulation of heavy metals and antioxidant responses in Pinus sylvestris L. needles in polluted and non-polluted sites. Ecotoxicology 25(5):970–981. https://doi.org/10.1007/s10646-016-1654-6
Kaneko M, Itoh H, Ueguchi-Tanaka M, Ashikari M, Matsuoka M (2002) The α-amylase induction in endosperm during rice seed germination is caused by gibberellin synthesized in epithelium. Plant Physiol 128(4):1264–1270. https://doi.org/10.1104/pp.010785
Khan AG, Kuek C, Chaudhry TM, Khoo CS, Hayes WJ (2000) Role of plants, mycorrhizae and phytochelators in heavy metal contaminated land remediation. Chemosphere 41(1–2):197–207. https://doi.org/10.1016/s0045-6535(99)00412-9
Khan MN, AlSolami MA, Basahi RA, Siddiqui MH, Al-Huqail AA, Abbas ZK, Siddiqui ZH, Ali HM, Khan F (2020) Nitric oxide is involved in nano-titanium dioxide-induced activation of antioxidant defense system and accumulation of osmolytes under water-deficit stress in Vicia faba L. Ecotoxicol Environ Saf 190:110152. https://doi.org/10.1016/j.ecoenv.2019.110152
Khan MN, Mobin M, Abbas ZK, Siddiqui MH (2017) Nitric oxide-induced synthesis of hydrogen sulfide alleviates osmotic stress in wheat seedlings through sustaining antioxidant enzymes, osmolyte accumulation and cysteine homeostasis. Nitric Oxide 68:91–102. https://doi.org/10.1016/j.niox.2017.01.001
Khan MN, Siddiqui MH, Mohammad F, Naeem M (2012) Interactive role of nitric oxide and calcium chloride in enhancing tolerance to salt stress. Nitric Oxide 27(4):210–218. https://doi.org/10.1016/j.niox.2012.07.005
Kolbert Z, Feigl G, Freschi L, Poor P (2019) Gasotransmitters in action: nitric oxide-ethylene crosstalk during plant growth and abiotic stress responses. Antioxidants (Basel) 8(6):167. https://doi.org/10.3390/antiox8060167
Kumar S, Sharma JG, Chakrabarti R (2000) Quantitative estimation of proteolytic enzyme and ultrastructural study of anterior part of intestine of Indian major carp (Catla catla) larvae during ontogenesis. Curr Sci 79:1007–1011
Kuriakose SV, Prasad MNV (2008) Cadmium stress affects seed germination and seedling growth in Sorghum bicolor (L.) Moench by changing the activities of hydrolyzing enzymes. Plant Growth Regul 54:143–156
Levine A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79(4):583–593. https://doi.org/10.1016/0092-8674(94)90544-4
Libourel IG, Bethke PC, De Michele R, Jones RL (2006) Nitric oxide gas stimulates germination of dormant Arabidopsis seeds: use of a flow-through apparatus for delivery of nitric oxide. Planta 223(4):813–820. https://doi.org/10.1007/s00425-005-0117-8
Lindner RC (1944) Rapid analytical methods for some of the more common inorganic constituents of plant tissue. Plant Physiol 19:76–89
Liu L, Zhang X, Zhong T (2016) Pollution and health risk assessment of heavy metals in urban soil in China. Hum Ecol Risk Assess 22:424–434
Lutts S, Kinet JM, Bouharmont J (1995) Changes in plant response to NaCl during development of rice (Oryza sativa L.) varieties differing in salinity resistance. J Exp Bot 46:1843–1852. https://doi.org/10.1093/jxb/46.12.1843
Matysik J, Alia BB, Mohanty P (2002) Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Curr Sci India 82(5):525–532
Metwally A, Finkemeier I, Georgi M, Dietz KJ (2003) Salicylic acid alleviates the cadmium toxicity in barley seedlings. Plant Physiol 132(1):272–281. https://doi.org/10.1104/pp.102.018457
Mishra S, Bharagava RN (2016) Toxic and genotoxic effects of hexavalent chromium in environment and its bioremediation strategies. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 34(1):1–32. https://doi.org/10.1080/10590501.2015.1096883
Misra N, Dwivedi UN (1990) Nitrogen assimilation in germinating Phaseolus aureus seeds under saline stress. J Plant Physiol 135(6):719–724
Nagalakshmi N, Prasad MN (2001) Responses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scenedesmus bijugatus. Plant Sci 160(2):291–299. https://doi.org/10.1016/s0168-9452(00)00392-7
Osuna D, Prieto P, Aguilar M (2015) Control of seed germination and plant development by carbon and nitrogen availability. Front Plant Sci 6:1023. https://doi.org/10.3389/fpls.2015.01023
Paradiso A, Berardino R, de Pinto MC, Sanita di Toppi L, Storelli MM, Tommasi F, De Gara L (2008) Increase in ascorbate-glutathione metabolism as local and precocious systemic responses induced by cadmium in durum wheat plants. Plant Cell Physiol 49:362–374
Radin JW (1974) Distribution and development of nitrate reductase activity in germinating cotton seedlings. Plant Physiol 53(3):458–463. https://doi.org/10.1104/pp.53.3.458
Ray S, Roy K, Sengupta C (2007) Evaluation of protective effect of water extract of Spirulina platensis (blue green algae) on cisplatin-induced lipid peroxidation. Indian J Pharm Sci 3:378–382
Rowbotham AL, Levy LS, Shuker LK (2000) Chromium in the environment: an evaluation of exposure of the UK general population and possible adverse health effects. J Toxicol Environ Health B Crit Rev 3(3):145–178. https://doi.org/10.1080/10937400050045255
Sawhney SK, Naik MS (1973) Effect of chloramphenicol and cycloheximide on the synthesis of nitrate reductase and nitrite reductase in rice leaves. Biochem Biophys Res Commun 51:67–73
Sethy SK, Ghosh S (2013) Effect of heavy metals on germination of seeds. J Nat Sci Biol Med 4(2):272–275. https://doi.org/10.4103/0976-9668.116964
Shanker AK, Cervantes C, Loza-Tavera H, Avudainayagam S (2005) Chromium toxicity in plants. Environ Int 31(5):739–753. https://doi.org/10.1016/j.envint.2005.02.003
Sharma A, Kapoor D, Wang J, Shahzad B, Kumar V, Bali AS, Jasrotia S, Zheng B, Yuan H, Yan D (2020) Chromium bioaccumulation and its impacts on plants: an overview. Plants (Basel) 9(1):100. https://doi.org/10.3390/plants9010100
Shaw JF, Lin FP, Chen SC, Chen CC (1995) Purification and properties of an extracellular α-amylase from Thermus sp. Bot Bull Acad Sin 36:195–200
Shekar CHC, Sammaiah D, Ujjwala D, Shasthree T, Reddy KJ (2013) Chromium toxicity in tomato (Lycopersicon esculenum Mill.). Int J Univers Pharm Life Sci 3(3):115–121
Siddiqui MH, Al-Whaibi MH (2014) Role of nano-SiO2 in germination of tomato (Lycopersicum esculentum seeds Mill.). Saudi J Biol Sci 21(1):13–17. https://doi.org/10.1016/j.sjbs.2013.04.005
Siddiqui MH, Al-Whaibi MH, Basalah MO (2011) Role of nitric oxide in tolerance of plants to abiotic stress. Protoplasma 248(3):447–455. https://doi.org/10.1007/s00709-010-0206-9
Siddiqui MH, Alamri S, Al-Khaishany MY, Khan MN, Al-Amri A, Ali HM, Alaraidh IA, Alsahli AA (2019) Exogenous melatonin counteracts NaCl-induced damage by regulating the antioxidant system, proline and carbohydrates metabolism in tomato seedlings. Int J Mol Sci 20(2):353. https://doi.org/10.3390/ijms20020353
Siddiqui MH, Alamri S, Alsubaie QD, Ali HM, Khan MN, Al-Ghamdi A, Ibrahim AA, Alsadon A (2020) Exogenous nitric oxide alleviates sulfur deficiency-induced oxidative damage in tomato seedlings. Nitric Oxide 94:95–107. https://doi.org/10.1016/j.niox.2019.11.002
Siddiqui MH, Alamri SA, Al-Khaishany MY, Al-Qutami MA, Ali HM, AL-Rabiah H, Kalaji HM (2017a) Exogenous application of nitric oxide and spermidine reduces the negative effects of salt stress on tomato. Hortic Environ Biotechnol 58:537–547
Siddiqui MH, Alamri SA, Al-Khaishany MYY, Al-Qutami MA, Ali HM, Khan MN (2017b) Sodium nitroprusside and indole acetic acid improve the tolerance of tomato plants to heat stress by protecting against DNA damage. J Plant Interact 12(1):177–186
Signorelli S, Considine MJ (2018) Corrigendum: Nitric oxide enables germination by a four-pronged attack on ABA-induced seed dormancy. Front Plant Sci 9:654. https://doi.org/10.3389/fpls.2018.00654
Signorelli S, Imparatta C, Rodriguez-Ruiz M, Borsani O, Corpas FJ, Monza J (2016) In vivo and in vitro approaches demonstrate proline is not directly involved in the protection against superoxide, nitric oxide, nitrogen dioxide and peroxynitrite. Funct Plant Biol 43(9):870–879. https://doi.org/10.1071/Fp16060
Singh VP, Tripathi DK, Fotopoulos V (2020) Hydrogen sulfide and nitric oxide signal integration and plant development under stressed/non-stressed conditions. Physiol Plant 168(2):239–240. https://doi.org/10.1111/ppl.13066
Sirova J, Sedlarova M, Piterkova J, Luhova L, Petrivalsky M (2011) The role of nitric oxide in the germination of plant seeds and pollen. Plant Sci 181(5):560–572. https://doi.org/10.1016/j.plantsci.2011.03.014
Smith BW, Roe JH (1949) A photometric method for the determination of a-amylase in blood and urine with the use of the starch-iodine color. J Biol Chem 179:53–59
Sumithra K, Jutur PP, Carmel BD, Reddy AR (2006) Salinity-induced changes in two cultivars of Vigna radiata: responses of antioxidative and proline metabolism. Plant Growth Regul 50:11–22
Takahama U, Oniki T (1992) Regulation of peroxidase-dependent oxidation of phenolics in the apoplast of spinach leaves by ascorbate. Plant Cell Physiol 33:379–387
Tao KL, Zheng GH (1990) Seed vigour. Science Press, Beijing
Tommasi F, Paciolla C, de Pinto MC, De Gara L (2001) A comparative study of glutathione and ascorbate metabolism during germination of Pinus pinea L. seeds. J Exp Bot 52(361):1647–1654
Turcsányi E, Lyons T, Plochl M, Barnes J (2000) Does ascorbate in the mesophyll cell walls form the first line of defence against ozone? Testing the concept using broad bean (Vicia faba L.). J Exp Bot 51:901–910
Vajpayee P, Khatoon I, Patel CB, Singh G, Gupta KC, Shanker R (2011) Adverse effects of chromium oxide nano-particles on seed germination and growth in Triticum aestivum L. J Biomed Nanotechnol 7(1):205–206. https://doi.org/10.1166/jbn.2011.1270
Vashisth A, Nagarajan S (2010) Effect on germination and early growth characteristics in sunflower (Helianthus annuus) seeds exposed to static magnetic field. J Plant Physiol 167(2):149–156. https://doi.org/10.1016/j.jplph.2009.08.011
Yadu S, Dewangan TL, Chandrakar V, Keshavkant S (2017) Imperative roles of salicylic acid and nitric oxide in improving salinity tolerance in Pisum sativum L. Physiol Mol Biol Plants 23(1):43–58. https://doi.org/10.1007/s12298-016-0394-7
Yamasaki S, Fujii N, Takahashi H (2005) Hormonal regulation of sex expression in plants. Vitam Horm 72:79–110. https://doi.org/10.1016/S0083-6729(05)72003-3
Yu CW, Murphy TM, Lin CH (2003) Hydrogen peroxide-induced chilling tolerance in mung beans mediated through ABA-independent glutathione accumulation. Funct Plant Biol 30:955–963
Zagorchev L, Seal CE, Kranner I, Odjakova M (2013) A central role for thiols in plant tolerance to abiotic stress. Int J Mol Sci 14(4):7405–7432. https://doi.org/10.3390/ijms14047405
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The authors extend their appreciation to the Deanship of Scientific Research at King Saud University for funding this work through Research Group No. RG-1439-041.
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MNK and SA, MHS: Conceptualization, Methodology, Data curation, Formal analysis, Investigation, Writing. VPS, and MHS: Conceptualization, Data curation, Writing—review & editing. BA and HMA Software, Validation. AAA and QDA Methodology, Formal analysis, Investigation.
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Khan, M.N., Alamri, S., Al-Amri, A.A. et al. Effect of Nitric Oxide on Seed Germination and Seedling Development of Tomato Under Chromium Toxicity. J Plant Growth Regul 40, 2358–2370 (2021). https://doi.org/10.1007/s00344-020-10212-2
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DOI: https://doi.org/10.1007/s00344-020-10212-2