Abstract
Edible amaranth (Amaranthus tricolor L.) is used as a food-medicine or ornamental plant, and despite its importance, there are few reports associated with cadmium (Cd) stress. This study aimed to appraise the crosstalk between sodium nitroprusside (SNP), as a source of nitric oxide (NO), and cadmium toxicity on growth and physiological traits in edible amaranth by using different multivariate statistical methods. The results showed that growth-related traits of A. tricolor were significantly reduced under Cd stress. Contrarily, Cd treatments increased lipid peroxidation and reduced total protein content. Delving on the results of SNP application showed the suitability of its medium level (100 µM) on increasing the growth-related traits and also plant tolerance to Cd stress via lowering the lipid peroxidation and radical molecules production due to the higher activities of superoxide dismutase and catalase. Increasing the amount of Cd in roots and shoots, as the result of Cd treatment, reduced the growth and production of A. tricolor plants by high rates (over 50% in 60 mg kg−1 Cd level), indicating its susceptibility to high Cd toxicity. Contrarily, treating plants with SNP showed no effect on shoot Cd content, while it significantly increased Cd allocation in the root, which might be attributable to the protective effect of NO on Cd toxicity by trapping Cd in the root. Subsequently, the application of a medium level of SNP (around 100 µM) is recommendable for A. tricolor plant to overcome the negative impacts of Cd toxicity. Moreover, according to the results of heatmap and biplot, under no application of Cd, the application of 100 µM SNP showed a great association with growth-related traits indicating the effectiveness of SNP on the productivity of this species even under no stress situations.
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Abbreviations
- Cd-soil:
-
Cadmium content in soil
- Cd-rt:
-
Cadmium content in shoot
- TF:
-
Translocation factors
- T-phen:
-
Total phenol
- Cart:
-
Carotenoid content
- Rl:
-
Root length
- Shl:
-
Shoot length
- RDW:
-
Root dry weight
- SDW:
-
Shoot dry weight
- H2O2 :
-
Hydrogen peroxidase
- MDA:
-
Malondialdehyd
- SOD:
-
Superoxide dismutase
- CAT:
-
Catalyze
- POD:
-
Peroxidase
- SNP:
-
Sodium nitroprusside
References
Adegbeye MJ, Ravi Kanth Reddy P, Obaisi AI, Elghandour MMMY, Oyebamiji KJ, Salem AZM, Morakinyo-Fasipe OT, Cipriano-Salazar M, Camacho-Díaz LM (2020) Sustainable agriculture options for production, greenhouse gasses and pollution alleviation, and nutrient recycling in emerging and transitional nations – an overview. J Clean Prod 242:118319. https://doi.org/10.1016/j.jclepro.2019.118319
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. https://doi.org/10.1016/S0076-6879(84)05016-3
Alamri S, Kushwaha BK, Singh VP, Siddiqui MH (2020) Dose dependent differential effects of toxic metal cadmium in tomato roots: role of endogenous hydrogen sulfide. Ecotoxicol Environ Saf 203:110978. https://doi.org/10.1016/j.ecoenv.2020.110978
Alamri S, Alsubaie QD, Al-Amri AA, Al-Munqedi B, Ali HM, Kushwaha BK, Singh VP, Siddiqui MH (2021) Priming of tomato seedlings with 2-oxoglutarate induces arsenic toxicity alleviatory responses by involving endogenous nitric oxide. Physiol Plant 173:45–47. https://doi.org/10.1111/ppl.13168
Alamri S, Siddiqui MH, Mukherjee S, Kumar R, Kalaji HM, Irfan M, Minkina T, Rajput VD (2022) Molybdenum-induced endogenous nitric oxide (NO) signaling coordinately enhances resilience through chlorophyll metabolism, osmolyte accumulation and antioxidant system in arsenate stressed-wheat (Triticum aestivum L.) seedlings. Environ Pollut 292:118268. https://doi.org/10.1016/j.envpol.2021.118268
Arnon DI (1949) Copper enzymes in isolated chloroplasts Polyphenoloxidase in Beta Vulgaris. Plant Physiol 24:1–15. https://doi.org/10.1104/pp.24.1.1
Assaad N, Fadel D, Argyraki A, Kypritidou Z, Bakir A, Awad E (2020) Heavy metals accumulation in the edible vegetables of Lebanese Tabbouli salad. J Agric Sci. https://doi.org/10.5539/jas.v12n7p155
Baek SA, Han T, Ahn SK, Kang H, Cho MR, Lee SC, Im KH (2012) Effects of heavy metals on plant growths and pigment contents in Arabidopsis Thaliana. Plant Pathol J 28:446–452. https://doi.org/10.5423/PPJ.NT.01.2012.0006
Bali AS, Sidhu GPS, Kumar V, Bhardwaj R (2019) Mitigating cadmium toxicity in plants by phytohormones. In: Hasanuzzaman M, Prasad MNV, Fujita M (eds) Cadmium toxicity and tolerance in plants. Academic Press, pp 375–396. https://doi.org/10.1016/B978-0-12-814864-8.00015-2
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
Chi K, Zou R, Wang L, Huo W, Fan H (2019) Cellular distribution of cadmium in two amaranth (Amaranthus mangostanus L.) cultivars differing in cadmium accumulation. Environ Sci Pollut Res 26:22147–22158. https://doi.org/10.1007/s11356-019-05390-w
Dhindsa RS, Plumb-Dhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101. https://doi.org/10.1093/jxb/32.1.93
Fadel D, Assaad N, Hachem A, Argyraki A, Kypritidou Z (2020) Heavy metals interaction in soil-plant system of carmagnola cannabis strain. J Agric Sci. https://doi.org/10.5539/jas.v12n7p163
Fancy NN, Bahlmann AK, Loake GJ (2017) Nitric oxide function in plant abiotic stress. Plant Cell Environ 40:462–472. https://doi.org/10.1111/pce.12707
Folin O, Ciocalteu V (1927) On tyrosine and tryptophane determinations in proteins. J Biol Chem 73:627–650. https://doi.org/10.1016/S0021-9258(18)84277-6
Genchi G, Carocci A, Lauria G, Sinicropi MS, Catalano A (2020) Nickel: human health and environmental toxicology. Int j Environ Res Public Health 17(3):679. https://doi.org/10.3390/ijerph17030679
He S, Yang X, He Z, Baligar VC (2017) Morphological and physiological responses of plants to cadmium toxicity: a review. Pedosphere 27:421–438. https://doi.org/10.1016/S1002-0160(17)60339-4
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198. https://doi.org/10.1016/0003-9861(68)90654-1
Hemeda HM, Klein BP (1990) Effects of naturally occurring antioxidants on peroxidase activity of vegetable extracts. J Food Sci 55:184–185. https://doi.org/10.1111/j.1365-2621.1990.tb06048.x
Hossain MA, Bhattacharjee S, Armin S-M, Qian P, Xin W, Li H-Y, Burritt DJ, Fujita M, Tran LSP (2015) Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Front Plant Sci. https://doi.org/10.3389/fpls.2015.00420
Huang Y, Xi Y, Gan L, Johnson D, Wu Y, Ren D, Liu H (2019) Effects of lead and cadmium on photosynthesis in Amaranthus spinosus and assessment of phytoremediation potential. Int J Phytromedetion 21:1041–1049. https://doi.org/10.1080/15226514.2019.1594686
Ismael MA, Elyamine AM, Moussa MG, Cai M, Zhao X, Hu C (2019) Cadmium in plants: uptake, toxicity, and its interactions with selenium fertilizers. Metallomics 11:255–277. https://doi.org/10.1039/c8mt00247a
Kabata-Pendias A, Mukherjee AB (2007) Trace elements from soil to human. Springer.https://doi.org/10.1007/978-3-540-32714-1
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
Kaya C, Ashraf M, Alyemeni MN, Ahmad P (2020) Responses of nitric oxide and hydrogen sulfide in regulating oxidative defence system in wheat plants grown under cadmium stress. Physiol Plant 168:345–360. https://doi.org/10.1111/ppl.13012
Khan MN, Siddiqui MH, AlSolami MA, Alamri S, Hu Y, Ali HM, Al-Amri AA, Alsubaie QD, Al-Munqedhi BMA, Al-Ghamdi A (2020) Crosstalk of hydrogen sulfide and nitric oxide requires calcium to mitigate impaired photosynthesis under cadmium stress by activating defense mechanisms in Vigna radiate. Plant Physiol Biochem 156:278–290. https://doi.org/10.1016/j.plaphy.2020.09.017
Kumar S, Prasad S, Yadav KK, Shrivastava M, Gupta N, Nagar S, Bach Q-V, Kamyab H, Khan SA, Yadav S, Malav LC (2019) Hazardous heavy metals contamination of vegetables and food chain: role of sustainable remediation approaches – a review. Environ Res 179:108792. https://doi.org/10.1016/j.envres.2019.108792
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382. https://doi.org/10.1016/0076-6879(87)48036-1
Lindsay WL, Norvell WA (1987) Development of DTPA soil test for zinc, iron, manganese and copper. Soil Sci Soc Am J 42:421–428. https://doi.org/10.2136/sssaj1978.03615995004200030009x
Marques DN, Carvalho MEA, Piotto FA, Batagin-Piotto KD, Nogueira ML, Gaziola SA, Azevedo RA (2019) Antioxidant defense response in plants to cadmium stress. In: Hasanuzzaman M, Prasad MNV, Nahar K (eds) Cadmium tolerance in plants. Academic Press, pp 423–461. https://doi.org/10.1016/B978-0-12-815794-7.00016-3
Munawar A, Akram NA, Ahmad A, Ashraf M (2019) Nitric oxide regulates oxidative defense system, key metabolites and growth of broccoli (Brassica oleracea L.) plants under water limited conditions. Sci Hortic 254:7–13. https://doi.org/10.1016/j.scienta.2019.04.072
Nahar K, Hasanuzzaman M, Alam MM, Rahman A, Suzuki T, Fujita M (2016) Polyamine and nitric oxide crosstalk: antagonistic effects on cadmium toxicity in mung bean plants through upregulating the metal detoxification, antioxidant defense and methylglyoxal detoxification systems. Ecotoxicol Environ Saf 126:245–255. https://doi.org/10.1016/j.ecoenv.2015.12.026
Prakash V, Singh VP, Tripathi DK, Sharma S, Corpas FJ (2019) Crosstalk between nitric oxide (NO) and abscisic acid (ABA) signalling molecules in higher plants. Environ Exp Bot 161:41–49. https://doi.org/10.1016/j.envexpbot.2018.10.033
Qian H, Li J, Sun L, Chen W, Sheng GD, Liu W, Fu Z (2009) Combined effect of copper and cadmium on Chlorella vulgaris growth and photosynthesis-related gene transcription. Aquat Toxico l 94:56–61. https://doi.org/10.1016/j.aquatox.2009.05.014
Rai PK, Lee SS, Zhang M, Tsang YF, Kim K (2019) Heavy metals in food crops: health risks, fate, mechanisms, and management. Environ Int 125:365–385. https://doi.org/10.1016/j.envint.2019.01.067
Riasat M, Kiani S, Saed-Mouchehsi A, Pessarakli M (2019) Oxidant related biochemical traits are significant indices in triticale grain yield under drought stress condition. J Plant Nutr 42:111–126. https://doi.org/10.1080/01904167.2018.1549675
Riaz S, Iqbal M, Hussain I, Rasheed R, Ashraf MA, Mahmood S (2014) Chronic cadmium induced oxidative stress not the DNA fragmentation modulates growth in spring wheat (Triticum aestivum). Int J Agric Biol 16:789–794
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. https://doi.org/10.1016/j.chemosphere.2017.09.068
Saed-Moucheshi A, Pakniyat H, Pirasteh-Anosheh H, Azooz MM (2014) Role of ROS as signaling molecules in plants. In: Ahmad P (ed) Oxidative damage to plants. Academic Press pp 585–620. https://doi.org/10.1016/B978-0-12-799963-0.00020-4
Shanmugaraj BM, Malla A, Ramalingam S (2019) Cadmium stress and toxicity in plants: an overview. In: Hasanuzzaman M, Prasad MNV, Fujita M (eds) Cadmium toxicity and tolerance in plants. Academic Press pp 1–17. https://doi.org/10.1016/B978-0-12-814864-8.00001-2
Sharma A, Soares C, Sousa B, Martins M, Kumar V, Shahzad B, Sidhu GPS, Bali AS, Asgher M, Bhardwaj R (2020) Nitric oxide-mediated regulation of oxidative stress in plants under metal stress: a review on molecular and biochemical aspects. Physiol Plant 168:318–344. https://doi.org/10.1111/ppl.13004
Shu X, Yin LY, Zhang QF, Wang WB (2012) Effect of Pb toxicity on leaf growth, antioxidant enzyme activities, and photosynthesis in cuttings and seedlings of Jatropha curcas L. Environ Sci Pollut Res 19:893–902. https://doi.org/10.1007/s11356-011-0625-y
Siddiqui MH, Alamri SA, Al-Khaishany MY, Al-Qutami MA, Ali HM, Khan MN (2017) Sodium nitroprusside and indole acetic acid improve the tolerance of tomato plants to heat stress by protecting against DNA damage. J Plant Interact 12:177–186. https://doi.org/10.1080/17429145.2017.1310941
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
Subiramani S, Sundararajan S, Sivakumar HP, Rajendran V, Ramalingam S (2019) Sodium nitroprusside enhances callus induction and shoot regeneration in high value medicinal plant Canscora diffusa. Plant Cell Tissue Organ Cult 139:65–75. https://doi.org/10.1007/s11240-019-01663-x
Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Sci 151:59–66. https://doi.org/10.1016/S0168-9452(99)00197-1
Villafort Carvalho MT, Amaral DC, Guilherme LRG, Aarts MGM (2013) Gomphrena claussenii, the first South-American metallophyte species with indicator-like Zn and Cd accumulation and extreme metal tolerance. Front Plant Sci. https://doi.org/10.3389/fpls.2013.00180
Watanabe T, Murata Y, Osaki M (2009) Amaranthus tricolor has the potential for phytoremediation of cadmium-contaminated soils. Commun Soil Sci Plant Anal 40:3158–3169. https://doi.org/10.1080/00103620903261676
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. https://doi.org/10.1007/s10725-015-0089-z
Zhong Q, Ma C, Chu J, Wang X, Liu X, Ouyang W, Lin C, He M (2020) Toxicity and bioavailability of antimony in edible amaranth (Amaranthus tricolor Linn.) cultivated in two agricultural soil types. Environ Pollut 257:113642. https://doi.org/10.1016/j.envpol.2019.113642
Zhu H, Ai H, Hu Z, Du D, Sun J, Chen K, Chen L (2020) Comparative transcriptome combined with metabolome analyses revealed key factors involved in nitric oxide (NO)-regulated cadmium stress adaptation in tall fescue. BMC Genomics 21:601. https://doi.org/10.1186/s12864-020-07017-8
Zou R, Wang L, Li YC, Tong Z, Huo W, Chi K, Fan H (2020) Cadmium absorption and translocation of amaranth (Amaranthus mangostanus L.) affected by iron deficiency. Environ Pollut 256:113410. https://doi.org/10.1016/j.envpol.2019.113410
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In this manuscript, FB carried out the experiment and performed the main parts in the data gathering, analyzing, and writing the manuscript. MA cooperated in performing the experiment and data gathering along with the manuscript writing. VRS and MM edited the manuscript scientifically. The grammatical corrections and structural editing of the final manuscript were carried out by FB and VRS.
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Baniasadi, F., Arghavani, M., Saffari, V.R. et al. Multivariate analysis of morpho-physiological traits in Amaranthus tricolor as affected by nitric oxide and cadmium stress. Environ Sci Pollut Res 29, 49092–49104 (2022). https://doi.org/10.1007/s11356-022-19430-5
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DOI: https://doi.org/10.1007/s11356-022-19430-5