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Melatonin and nitric oxide enhance cadmium tolerance and phytoremediation efficiency in Catharanthus roseus (L.) G. Don

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In this study, a pot experiment was performed to evaluate the effects of foliar spray with sodium nitroprusside (200 μM SNP) and melatonin (100 μM) singly and in combination on tolerance and accumulation of cadmium (Cd) in Catharanthus roseus (L.) G. Don plants exposed to different levels of cadmium (0, 50, 100, and 200 mg Cd kg−1 soil). The results showed that 50 mg kg−1 Cd had no significant effect on the fresh and dry weight of roots and shoots and content of chlorophyll (Chl) a and b, but the higher levels of Cd (100 and 200 mg kg−1) significantly reduced these attributes and induced an increase in the level of leaf electrolyte leakage and disrupted nutrient homeostasis. The activities of catalase (CAT) and peroxidase (POD) in leaves were increased under lower Cd concentrations (50 and 100 mg kg−1) but decreased under 200 mg kg−1 Cd. However, foliar spray with melatonin and/or SNP increased shoot biomass and the content of Chl a and b, augmented activities of POD and CAT, lowered electrolyte leakage (EL), and improved essential cations homeostasis in leaves. Cadmium content in shoots of C. roseus was less than roots and TF (transfer factor) was < 1. Interestingly, foliar spray with SNP and/or melatonin increased Cd accumulation and bioconcentration factor (BCF) in both roots and shoots and elevated the Cd transport from roots to shoot, as TF values increased in these treatments. The co-application of melatonin and SNP further than their separate usage augmented Cd tolerance through increasing activities of antioxidant enzymes and regulating mineral homeostasis in C. roseus. Furthermore, co-treatment of SNP and melatonin increased Cd phytoremediation efficiency in C. roseus through increasing biomass and elevating uptake and translocation of Cd from root to shoot.

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  1. Amooaghaie R, Mardani Korrani F (2018) Bacillus subtilis and vermicompost suppress damping-off disease in psyllium through nitric oxide-dependent signaling system. Russ J Plant Physiol 65(3):435–445

  2. Amooaghaie R, Roohollahi S (2017) Effect of sodium nitroprusside on responses of Melissa officinalis to bicarbonate exposure and direct Fe deficiency stress. Photosynthetica 55:158–163

  3. Amooaghaie R, Zangene-Madar F, 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

  4. Amooaghaie R, Tabatabaei F, Ahadi AM (2018) Alterations in HO-1 expression, heme oxygenase activity and endogenous NO homeostasis modulate antioxidant responses of Brassica nigra against nano silver toxicity. J Plant Physiol 228:75–84. https://doi.org/10.1016/j.jplph.2018.01.012

  5. Arasimowicz-Jelonek J, Floryszak-Wieczorek E, Gwozdz A (2011) The message of nitric oxide in cadmium challenged plants. Plant Sci 181:612–620

  6. Arnao MB, Hernández-Ruiz J (2013) Growth conditions determine different melatonin levels in Lupinus albus L. J Pineal Res 55:149–155

  7. Arnao MB, Hernández-Ruiz J (2019a) Melatonin and reactive oxygen and nitrogen species: a model for the plant redox network. Melatonin Res 2:152–168

  8. Arnao MB, Hernández-Ruiz J (2019b) Melatonin: a new plant hormone and/or a plant master regulator? Trends Plant Sci 24:38–48

  9. Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements—a review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126

  10. Begara-Morales JC, Sanchez-Calvo B, Chaki M, Valderrama R, Mata-Perez C, Padilla MN, Corpas FJ, Barroso JB (2016) Antioxidant systems are regulated by nitric oxide-mediated post-translational modifications (NO-PTMs). Front Plant Sci 7:152

  11. Besson-Bard A, Gravot A, Richaud P, Auroy P, Duc C, Gaymard F et al (2009) Nitric oxide contributes to cadmium toxicity in Arabidopsis by promoting cadmium accumulation in roots and by up-regulating genes related to iron uptake. Plant Physiol 149:1302–1315

  12. Cai SY, Zhang Y, Xu YP, Qi ZY, Li MQ, Ahammed GJ, Xia XJ, Shi K, Zhou YH, Reiter RJ et al (2017) HsfA1a upregulates melatonin biosynthesis to confer cadmium tolerance in tomato plants. J Pineal Res 62:12387

  13. Cao YY, Qi CD, Li S, Wang Z, Wang X, Wang J, Ren S, Li X, Zhang N, Guo YD (2019) Melatonin alleviates copper toxicity via improving copper sequestration and ROS scavenging in cucumber. Plant Cell Physiol 60(3):562–574. https://doi.org/10.1093/pcp/pcy226

  14. Chen YH, Kao CH (2012) Calcium is involved in nitric oxide- and auxin-induced lateral root formation in rice. Protoplasma 249(1):187–195

  15. Chen Q, Wu K, Tang Z, Guo QX, Guo X, Wan H (2017) Exogenous ethylene enhanced the cadmium resistance and changed the alkaloid biosynthesis in Catharanthus roseus seedlings. Acta Physiol Plant 39:267

  16. Chen Q, Lu X, Guo X, Pan Y, Yu B, Tang Z, Guo Q (2018a) Differential responses to Cd stress induced by exogenous application of Cu, Zn or Ca in the medicinal plant Catharanthus roseus. Ecotoxicol Environ Saf 157:266–275

  17. Chen W, Dong Y, Hu G, Bai X (2018b) Effects of exogenous nitric oxide on cadmium toxicity and antioxidative system in perennial ryegrass. J Soil Sci Plant Nutr 18(1):129–143

  18. Dionisio-Sese ML, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Sci 135:1–9

  19. Elviri L, Speroni F, Careri M, Mangia A, Toppi LS, Zottini M (2010) Identification of in vivo nitrosylated phytochelatins in A. thaliana cells by liquid chromatography-direct electrospray linear ion trap-mass spectrometry. J Chromatography A 1217:4120–4126

  20. Grant CA (2011) Influence of phosphate fertilizer on cadmium in agricultural soils and crops. Pdeologist 54(35):143–155

  21. Graziano M, Lamattina L (2005) Nitric oxide and iron in plants: an emerging and converging story. Trends Plant Sci 10(1):4–8

  22. Gu Q, Chen Z, Yu X, Cui W, Pan J, Zhao G, Xu S, Wang R, Shen W (2017) Melatonin confers plant tolerance against cadmium stress via the decrease of cadmium accumulation and reestablishment of microRNA-mediated redox homeostasis. Plant Sci. https://doi.org/10.1016/j.plantsci.2017.05.001

  23. Hasan MK, Ahammed GJ, Yin L, Shi K, Xia X, Zhou Y (2015) Melatonin mitigates cadmium phytotoxicity through modulation of phytochelatins biosynthesis, vacuolar sequestration, and antioxidant potential in Solanum lycopersicum L. Front Plant Sci 6:601

  24. Hu Y, Lu L, Tian S, Li S, Liu X, Gao X, Zhou W, Lin X (2018) Cadmium-induced nitric oxide burst enhances Cd tolerance at early stage in roots of a hyperaccumulator Sedum alfredii partially by altering glutathione metabolism. Sci Total Environ 650(2):2761–2770

  25. Huang JJ, Lin LJ, Chen FB, Wei ZL, Wen J (2017) Effects of spraying melatonin on growth and cadmium accumulation of radish. J Sichuan Agric Univ 35(3):375–380

  26. 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 sativum) roots. PLoS One 10:138713

  27. Kaya C, Higgs D, Ashraf M, Alyemeni M, Ahmad P (2019a) Integrative roles of nitric oxide and hydrogen sulfide in melatonin-induced tolerance of pepper (Capsicum annuum L.) plants to iron deficiency and salt stress alone or in combination. Physiol Plant. https://doi.org/10.1111/ppl.12976

  28. Kaya C, Okant M, Ugurlar F, Alyemeni MN, Ashraf M, Ahmad P (2019b) Melatonin-mediated nitric oxide improves tolerance to cadmium toxicity by reducing oxidative stress in wheat plants. Chemosphere 225:627–638

  29. Khairy AIH, Jeong MI, Seung O, Lee M, Kim D, Roh KS (2016) Nitric oxide overcomes Cd and Cu toxicity in in vitro-grown tobacco plants through increasing contents and activities of Rubisco and Rubisco activase. Biochim Open 2:41–51

  30. Khan WU, Ahmad SR, Yasin NA, Ali A, Ahmad A (2017) Effect of Pseudomonas fluorescens RB4 and Bacillus subtilis 189 on the phytoremediation potential of Catharanthus roseus (L.) in Cu and Pb-contaminated soils. Int J Phytorem 19(6):514–521

  31. Khan WU, Yasin NA, Ahmad SR, Ali A, Ahmad A, Akram W, Faisal M (2018) Role of Burkholderia cepacia CS8 in Cd-stress alleviation and phytoremediation by Catharanthus roseus. Int J Phytorem 20(6):581–592

  32. Kobylinska A, Posmyk M (2016) Melatonin restricts Pb-induced PCD by enhancing BI-1 expression in tobacco suspension cells. Biomet 29:1059–1074

  33. Kováčik J, Babula P, Klejdus B, Hedbavny J, Jarošová M (2014) Unexpected behavior of some nitric oxide modulators under cadmium excess in plant tissue. PLoS One 9(3):e91685. https://doi.org/10.1371/journal.pone.0091685

  34. Kumar S, Varman P, Ranjitha Kumari BD (2011) Cadmium stress response in Catharanthus roseus leaves through proteomic approach. 2010 Int Conf on Biol, Environ and Chem IPCBEE 1.

  35. Kumari A, Sheokand S, Swaraj K (2010) Nitric oxide induced alleviation of toxic effects of short term and long term Cd stress on growth, oxidative metabolism and Cd accumulation in chickpea. Braz J Plant Physiol 22(4):271–284

  36. Lee HY, Back K (2017) Melatonin is required for H2O2- and NO-mediated defense signaling through MAPKKK3 and OXI1 in Arabidopsis thaliana. J Pineal Res 62:12379–11242

  37. Lee K, Choi GH, Back K (2017) Cadmium-induced melatonin synthesis in rice requires light, hydrogen peroxide, and nitric oxide: key regulatory roles for tryptophan decarboxylase and caffeic acid O-methyltransferase. J Pineal Res 63:e12441

  38. Leitenmaier B, Küpper H (2013) Compartmentation and complexation of metals in hyperaccumulator plants. Front Plant Sci 4:1–13

  39. Li MQ, Hasan MK, Li CX, Ahammed GJ, Xia XJ, Shi K, Zhou YH, Reiter RJ, Yu JQ, Xu MX, Zhou J (2016) Melatonin mediates selenium-induced tolerance to cadmium stress in tomato plants. J Pineal Res 61(3):291–302

  40. Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. Curr Protoc Food Anal Chem F F4:3

  41. Lin L, Li J, Chen F, Liao M, Tang Y, Liang D, Xia H, Lai Y, Wang X, Chen C, Ren W (2018) Effects of melatonin on the growth and cadmium characteristics of Cyphomandra betacea seedlings. Environ Monit Assess 190:119

  42. Liu F, Guo FQ (2013) Nitric oxide deficiency accelerates chlorophyll breakdown and stability loss of thylakoid membranes during dark-induced leaf senescence in Arabidopsis. J Pone 8(2):e56345

  43. Liu S, Yang R, Pan Y, Wang L (2013) Effects of exogenous nitric oxide on lipid peroxidation and ATPase activity of plasma membrane and photosynthetic characteristics in Catharanthus roseus under cadmium stress. J Integr Agric 32(12):2360–2368

  44. Liu N, Gong B, Jin Z, Wang X, Wei M, Yang F, Li Y, Shi Q (2015a) Sodic alkaline stress mitigation by exogenous melatonin in tomato needs nitric oxide as a downstream signal. J Plant Physiol 186–187:68–77

  45. Liu SL, Yang RJ, Ma MD, Dan F, Zhao Y, Jiang P, Wang MH (2015b) Effects of exogenous NO on the growth, mineral nutrient content, antioxidant system, and ATPase activities of Trifolium repens L. plants under cadmium stress. Acta Physiol Plant 37:1721–1738

  46. Liu SL, Huang YZ, Luo ZJ, Huang YC, Yang XW (2017) Effects of exogenous melatonin on accumulation and chemical form of Cd in rice. Chin J Appl Ecol 28(5):1588–1594

  47. Liu L, Li W, Song W, Guo M (2018) Remediation techniques for heavy metal-contaminated soils: principles and applicability. Sci The Total Environ 633:206–219

  48. Mihailovic N, Drazic G (2011) Incomplete alleviation of nickel toxicity in bean by nitric oxide supplementation. Plant Soil Environ 57(8):396–401

  49. Milner MJ, Kochian LV (2008) Investigating heavy-metal hyperaccumulation using Thlaspi caerulescens as a model system. Ann Bot 102:3–13

  50. Misra AN, Misra M, Singh R (2011) Nitric oxide ameliorates stress responses in plants. Plant Soil Environ 57(3):95–100

  51. Nabaei M, Amooaghaie R (2019a) Interactive effect of melatonin and sodium nitroprusside on seed germination and seedling growth of Catharanthus roseus under cadmium stress. Russ J Plant Physiol 66(1)

  52. Nabaei M, Amooaghaie R (2019b) Nitric oxide is involved in the regulation of melatonin-induced antioxidant responses in Catharanthus roseus roots under cadmium stress. Botany. https://doi.org/10.1139/cjb-2019-0107

  53. Nawaz MA, Huang Y, Bie Z, Ahmed W, Reiter RJ, Niu M, Hameed S (2016) Melatonin: current status and future perspectives in plant science. Front Plant Sci 6:1–13. https://doi.org/10.3389/fpls.2015.01230

  54. Ni J, Wang Q, Shah F, Liu W, Wang D, Huang S, Fu S, Wu L (2018) Exogenous melatonin confers cadmium tolerance by counterbalancing the hydrogen peroxide homeostasis in wheat seedlings. Molecules 23:799

  55. 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

  56. Oz MT, Eyidogan F, Yucel M, Oktem HA (2015) Functional role of nitric oxide under abiotic stress condition. In: Khan M, Mobin M, Mohammad F, Corpas F (eds) Nitric oxide action in abiotic stress responses in plants. Springer, Cham, pp 21–41. https://doi.org/10.1007/978-3-319-17804-2_2

  57. Parmar P, Kumari N, Sharma V (2013) Structural and functional alterations in photosynthetic apparatus of plants under cadmium stress. Bot Stud 54:45

  58. Ren S, Qun-xian Deng QX, Peng JW, Lin LJ, Zhang HF (2018) Effects of exogenous melatonin on growth and cadmium content of Zizyphus acidojujuba seedlings. IOP Conf Ser Earth Environ Sci 199:042006. https://doi.org/10.1088/1755-1315/199/4/042006

  59. Sahay S, Gupta M (2017) An update on nitric oxide and its benign role in plant responses under metal stress. Nitric Oxide 67:39–52

  60. Sekabira K, Oryem-Origa H, Mutumba G, Kakudidi E, Basamba TA (2011) Heavy metal phytoremediation by Commelina benghalensis (L) and Cynodon dactylon (L) growing in urban stream sediments. Int J Plant Physiol Biochem 3(8):133–142

  61. Singh P, Shah (2014) Evidences for reduced metal-uptake and membrane injury upon application of nitric oxide donor in cadmium stressed rice seedlings. Plant Physiol Biochem 83:180–184

  62. Singh P, Indoliya Y, Chauhan A, Singh SP, Singh AP et al (2017) Nitric oxide mediated transcriptional modulation enhances plant adaptive responses to arsenic stress. Sci Report 7:3592

  63. Souri Z, Karimi N (2017) Enhanced phytoextraction by As hyperaccumulator Isatis cappadocica spiked with sodium nitroprusside. Soil Sediment Contam Int J

  64. Subhashini V, Swamy AVVS (2013) Phytoremediation of Pb and Ni contaminated soils using Catharanthus roseus (L.). Univers J Environ Res Technol 3:465–472

  65. Subhashini V, Swamy AVVS (2015) Phytoremediation of lead, cadmium and chromium contaminated soils using selected weed plants. Acta Biol Indica 4(2):205–212

  66. Tang Y, Lin L, Xie Y, Liu J, Sun G, Li H, Liao M, Wang Z, Liang D, Xia H, Wang X, Zhang J, Liu Z, Huang Z, He Z, Tu L (2017) Melatonin affects the growth and cadmium accumulation of Malachium aquaticum and Galinsoga parviflora. Int J Phytorem 20(4):295–300

  67. Tran TA, Popova LP (2013) Functions and toxicity of cadmium in plants: recent advances and future prospects. A review article. Turk J Bot 37:1–13

  68. Umapathi M, Kalarani MK, Udhaya Bharathi M, Kalaiselvi P (2018) Cadmium induced stress mitigation in tomato by exogenous melatonin. Int J Pure Appl Biosci 6(1):903–909

  69. Weeda S, Zhang N, Zhao X, Ndip G, Guo Y, Buck GA, Fu C, Ren S (2014) Arabidopsis transcriptome analysis reveals key roles of melatonin in plant defense systems. PLoS One 9:93462

  70. Wen D, Gong B, Sun S, Liu S, Wang X, Wei M, Yang F, Li Y, Shi Q (2016) Promoting roles of melatonin in adventitious root development of Solanum lycopersicum L. by regulating auxin and nitric oxide signaling. Front. Plant Sci 7:718

  71. Xiang G, Lin L, Liao M, Tang Y, Liang D, Xia H, Wang J, Wang X, Sun G, Zhang H, Zou Y, Ren W (2019) Effects of melatonin on cadmium accumulation in the accumulator plant Perilla frutescens. Chem Ecol 35(6):553–562. https://doi.org/10.1080/02757540.2019.1600683

  72. Xiong J, An L, Lu H, Yhu C (2009) Exogenous nitric oxide enhances cadmium tolerance of rice by increasing pectin and hemicellulose contents in root cell wall. Planta 230:755–765

  73. Xu L, Dong Y, Kong J, Liu S (2014) Effects of root and foliar applications of exogenous NO on alleviating cadmium toxicity in lettuce seedlings. Plant Growth Regul 72:39–50

  74. Yang Y, Ge Y, Zeng H, Zhou X, Peng L, Zeng Q (2017) Phytoextraction of cadmium contaminated soil and potential of regenerated tobacco biomass for recovery of cadmium. Sci Rep 7:7210. https://doi.org/10.1038/s41598-017-05834-8

  75. Yoon J, Cao X, Zhou QL, Ma Q (2006) Accumulation of Pb, Cu, and Zn in native plants growing on a contaminated Florida site. Sci Total Environ 368:456–464

  76. Yu Q, Sun L, Jin H, Chen Q, Chen Z, Xu M (2012) Lead-induced nitric oxide generation plays a critical role in lead uptake by Pogonatherum crinitum root cells. Plant Cell Physiol 53:1728–1736

  77. Zhang N, Sun Q, Zhang H, Cao Y, Weeda S, Ren S, Guo YD (2015) Roles of melatonin in abiotic stress resistance in plants. J Exp Bot 66(3):647–656

  78. Zhang J, Li D, Wei J, Ma W, Kong X, Rengel Z, Chen Q (2019) Melatonin alleviates aluminum-induced root growth inhibition by interfering with nitric oxide production in Arabidopsis. Environ Exp Bot 161:157–165

  79. 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 Regul 78:243–251

  80. Zhao D, Wang R, Meng J, Li Z, Wu Y (2017) Ameliorative effects of melatonin on dark-induced leaf senescence in gardenia (Gardenia jasminoides Ellis): leaf morphology, anatomy, physiology and transcriptome. Sci Rep 7:1–19

  81. Zhou C, Liu Z, Zhu L, Ma Z, Wang J, Zhu J (2016) Exogenous melatonin improves plant iron deficiency tolerance via increased accumulation of polyamine-mediated nitric oxide. Int J Mol Sci 17:1777. https://doi.org/10.3390/ijms17111777

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Nabaei, M., Amooaghaie, R. Melatonin and nitric oxide enhance cadmium tolerance and phytoremediation efficiency in Catharanthus roseus (L.) G. Don. Environ Sci Pollut Res (2019). https://doi.org/10.1007/s11356-019-07283-4

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  • C. roseus
  • Phytoremediation
  • Nitric oxide
  • Melatonin
  • Cd tolerance