Abstract
Cadmium (Cd) is a serious threat for environmental sustainability as it can be taken up quickly by plants and transported to the food chain of living organisms. It alters plants’ metabolic and physiological activities and causes yield loss, thereby, enhancing plant tolerance to Cd stress is of utmost essential. Therefore, an experiment was executed to investigate the potential role of Ascophyllum nodosum extract (ANE) and moringa (Moringa oleifera) leaf extract (MLE) to confer Cd tolerance in rice (Oryza sativa cv. BRRI dhan89). Thirty-five-day-old seedling was subjected to Cd stress (50 mg kg−1 CdCl2) alone and in a combination of ANE (0.25%) or MLE (0.5%) in a semi-controlled net house. Exposure to Cd resulted in accelerated production of reactive oxygen species, enhanced lipid peroxidation, and disrupted antioxidant defense and glyoxalase system, thus retarded plant growth, biomass production, and yield attributes of rice. On the contrary, the supplementation of ANE or MLE enhanced the contents of ascorbate and glutathione, and the activities of antioxidant enzymes such as ascorbate peroxidase, dehydroascorbate reductase, monodehydroascorbate reductase, glutathione reductase, glutathione peroxidase, and catalase. Moreover, supplementation of ANE and MLE enhanced the activities of glyoxalase I and glyoxalase II which prevented the overgeneration of methylglyoxal in Cd stressed rice plants. Thus, because of ANE and MLE addition Cd-induced rice plants showed a noticeable declination in membrane lipid peroxidation, hydrogen peroxide generation, and electrolyte leakage, whereas improved water balance. Furthermore, the growth and yield attributes of Cd-affected rice plants were improved with the supplementation of ANE and MLE. All the studied parameters indicates the potential role of ANE and MLE in mitigating Cd stress in rice plants through improving the physiological attributes, modulating antioxidant defense and glyoxalase system.
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References
Al-Taisan WA, Alabdallah NM, Almuqadam L (2022) Moringa leaf extract and green algae improve the growth and physiological attributes of Mentha species under salt stress. Sci Rep 12:14205. https://doi.org/10.1038/s41598-022-18481-5
Alyemeni MN, Ahanger MA, Wijaya L, Alam P, Bhardwaj R, Ahmad P (2018) Selenium mitigates cadmium-induced oxidative stress in tomato (Solanum lycopersicum L.) plants by modulating chlorophyll fluorescence, osmolyte accumulation, and antioxidant system. Protoplasma 255:459–469
Auesukaree C, Bussarakum J, Sirirakphaisarn S, Saengwilai PJ (2022) Effects of aqueous Moringa oleifera leaf extract on growth performance and accumulation of cadmium in a Thai jasmine rice—Khao Dawk Mali 105 variety. Environ Sci Pollut Res 29:46968–46976
Aziz R, Rafiq MT, Li T, Liu D, He Z, Stoffella PJ, Sun K, Xiaoe Y (2015) Uptake of cadmium by rice grown on contaminated soils and its bioavailability/toxicity in human cell lines (Caco-2/HL-7702). J Agric Food Chem 63:3599–3608
Azzam CR, S-nS Z, Bamagoos AA, Rady MM, Alharby HF (2022) Soaking maize seeds in zeatin-type cytokinin biostimulators improves salt tolerance by enhancing the antioxidant system and photosynthetic efficiency. Plants 11:1004. https://doi.org/10.3390/plants11081004
Barrs HD, Weatherley PE (1962) A re-examination of the relative turgidity technique for estimating water deficits in leaves. Aust J Biol Sci 15:413–428
Basu S, Prabhakar AA, Kumari S, Aabha, Kumar RR, Shekhar S, Prakash K, Singh JP, Singh GP, Prasad R, Kumar G (2022) Micronutrient and redox homeostasis contribute to Moringa oleifera-regulated drought tolerance in wheat. Plant Growth Regul 2022. https://doi.org/10.1007/s10725-022-00795-z
Bates LS, Waldren RP, Teari D (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207
Battacharyya D, Babgohari MZ, Rathor P, Prithiviraj B (2015) Seaweed extracts as biostimulants in horticulture. Sci Hortic 196:39–48
Bonomelli C, Celis V, Lombardi G, Mártiz J (2018) Salt stress effects on avocado (Persea Americana mill.) plants with and without seaweed extract (Ascophyllum nodosum) application. Agronomy 8:64. https://doi.org/10.3390/agronomy8050064
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
BRRI (Bangladesh Rice Research Institute) (2020) Adhunik Dhaner Chash (in Bengali). Joydebpur, Dhaka- 1701. p.106
Campobenedetto C, Agliassa C, Mannino G, Vigliante I, Contartese V, Secchi F, Bertea CM (2021) A biostimulant based on seaweed (Ascophyllum nodosum and Laminaria digitata) and yeast extracts mitigates water stress effects on tomato (Solanum lycopersicum L.). Agriculture 11:557. https://doi.org/10.3390/agriculture11060557
Carrasco-Gil S, Hernandez-Apaolaza L, Lucena JJ (2018) Effect of several commercial seaweed extracts in the mitigation of iron chlorosis of tomato plants (Solanum lycopersicum L.). Plant Growth Regul 86:401–411
Chen D, Chen D, Xue R, Long J, Lin X, Lin Y, Jia L, Zeng R, Song Y (2019) Effects of boron, silicon and their interactions on cadmium accumulation and toxicity in rice plants. J Hazard Mater 367:447–455
CoStat (2008) CoStat- Statistics Software Version 6.400. CoHort Software, 798 Lighthouse Ave. PMB 320. Monterey, CA, 93940, USA
Craigie JS (2011) Seaweed extract stimuli in plant science and agriculture. J Appl Phycol 23:371–393
DalCorso G, Manara A, Furini A (2013) An overview of heavy metal challenge in plants: from roots to shoots. Metallomics 5:1117–1132
Di Stasio E, Van Oosten MJ, Silletti S, Raimondi G, Carillo P, Maggio A (2018) Ascophyllum nodosum-based algal extracts act as enhancers of growth, fruit quality, and adaptation to stress in salinized tomato plants. J Appl Phycol 30:2675–2686
Di Stasio E, Cirillo V, Raimondi G, Giordano M, Esposito M, Maggio A (2020) Osmo-priming with seaweed extracts enhances yield of salt-stressed tomato plants. Agronomy 10:1559. https://doi.org/10.3390/agronomy10101559
Dionisio-Sese ML, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Sci 135:1–9. https://doi.org/10.1016/s0168-9452(98)00025-9
El-Hack ME, Alagawany M, Elrys AS, Desoky E-SM, Tolba HMN, Elnahal ASM, Elnesr SS, Swelum AA (2018) Effect of forage Moringa oleifera L. on animal health and nutrition and its beneficial applications in soil, plants and water purification. Agriculture 8:145. https://doi.org/10.3390/agriculture8090145
Elia AC, Galarini R, Taticchi MI, Dorr AJM, Mantilacci L (2003) Antioxidant responses and bioaccumulation in Ictalurus melas under mercury exposure. Ecotoxicol Environ Saf 55:162–167
El-Mageed TAA, Semida WM, Rady MM (2017) Moringa leaf extract as biostimulant improves water use efficiency, physio-biochemical attributes of squash plants under deficit irrigation. Agril Water Manag 193:46–54
Fan D, Hodges DM, Zhang J, Kirby CW, Ji X, Locke SJ, Critchley AT, Prithiviraj B (2011) Commercial extract of the brown seaweed Ascophyllum nodosum enhances phenolic antioxidant content of spinach (Spinacia oleracea L.) which protects Caenorhabditis elegans against oxidative and thermal stress. Food Chem 124:195–202
Ferńandez R, Bertrand A, Reis R, Mourato MP, Martins LL, Gonźalez A (2013) Growth and physiological responses to cadmium stress of two populations of Dittrichia viscosa (L.) Greuter. J Hazard Mater 244–245:555–562
Forlani G, Bertazzini M, Cagnano G (2019) Stress-driven increase in proline levels, and not proline levels themselves, correlates with the ability to withstand excess salt in a group of 17 Italian rice genotypes. Plant Biol 21:336–342
Frioni T, Sabbatini P, Tombesi S, Norrie J, Poni S, Gatti M, Palliotti A (2018) Effects of a biostimulant derived from the brown seaweed Ascophyllum nodosum on ripening dynamics and fruit quality of grapevines. Sci Hortic 232:97–106
Garai S, Bhowal B, Kaur C, Singla-Pareek SL, Sopory SK (2021) What signals the glyoxalase pathway in plants? Physiol Mol Biol Plants 27:2407–2420
Gill SS, Anjum NA, Hasanuzzaman M, Gill R, Trived DK, Ahmad I, Pereira E, Tuteja N (2013) Glutathione reductase and glutathione: a boon in disguise for plant abiotic stress defense operations. Plant Physiol Biochem 70:204–212
Gratao PL, Pompeu GB, Capaldi FR, Vitorello VA, Lea PJ, Azevedo RA (2008) Antioxidant response of Nicotiana tabacum cv. Bright Yellow 2 cells to cadmium and nickel stress. Plant Cell Tiss Organ Cult 94:73. https://doi.org/10.1007/s11240-008-9389-6
Habiba U, Ali S, Rizwan M, Ibrahim M, Hussain A, Shahid MR, Alamri SA, Alyemeni MN, Ahmad P (2019) Alleviative role of exogenously applied mannitol in maize cultivars differing in chromium stress tolerance. Environ Sci Pollut Res 26:5111–5121
Hafeez A, Tipu MI, Saleem MH, Al-Ashkar I, Saneoka H, El Sabagh A (2022) Foliar application of moringa leaf extract (MLE) enhanced antioxidant system, growth, and biomass related attributes in safflower plants. S Afr J Bot 150:1087–1095
Han Y, Wu M, Hao L, Yi H (2018) Sulfur dioxide derivatives alleviate cadmium toxicity by enhancing antioxidant defence and reducing Cd2+ uptake and translocation in foxtail millet seedlings. Ecotoxicol Environ Saf 157:207–215
Hasanuzzaman M, Nahar K, Anee TI, Khan MIR, Fujita M (2018) Silicon-mediated regulation of antioxidant defense and glyoxalase systems confers drought stress tolerance in Brassica napus L. S Afr J Bot 115:50–57
Hasanuzzaman M, Bhuyan MHMB, Anee TI, Parvin K, Nahar K, Mahmud JA, Fujita M (2019) Regulation of ascorbate-glutathione pathway in mitigating oxidative damage in plants under abiotic stress. Antioxidants 8:384. https://doi.org/10.3390/antiox8090384
Hasanuzzaman M, Parvin K, Bardhan K, Nahar K, Anee TI, Masud AAC, Fotopoulos V (2021a) Biostimulants for the regulation of reactive oxygen species metabolism in plants under abiotic stress. Cells 10:2537. https://doi.org/10.3390/cells10102537
Hasanuzzaman M, Raihan MRH, Khojah E, Samra BN, Fujita M, Nahar K (2021b) Biochar and chitosan regulate antioxidant defense and methylglyoxal detoxification systems and enhance salt tolerance in jute (Corchorus olitorius L.). Antioxidants 10:2017. https://doi.org/10.3390/antiox10122017
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplast. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198
Hossain MA, Nakano Y, Asada K (1984) Monodehydroascorbate reductase in spinach chloroplasts and its participation in the regeneration of ascorbate for scavenging hydrogen peroxide. Plant Cell Physiol 25:385–395
Huang C, He W, Guo J, Chang X, Su P, Zhang L (2005) Increased sensitivity to salt stress in ascorbate-deficient Arabidopsis mutant. J Exp Bot 56:3041–3049
IRRI (International Rice Research Institute) (2022) http://www.knowledgebank.irri.org. accessed on October 6, 2022
Karalija E, Selović A (2018) The effect of hydro and proline seed priming on growth, proline and sugar content, and antioxidant activity of maize under cadmium stress. Environ Sci Pollut Res 25:33370–33380
Karthiga D, Chozhavendhan S, Gandhiraj V, Aniskumar M (2022) The effects of Moringa oleifera leaf extract as an organic biostimulants for the growth of various plants: review. Biocatal Agric Biotechnol 43:102446
Kaya C, Ashraf M, Alyemeni MN, Ahmad P (2020) The role of nitrate reductase in brassinosteroid induced endogenous nitric oxide generation to improve cadmium stress tolerance of pepper plants by upregulating the ascorbate-glutathione cycle. Ecotoxicol Environ Saf 196:110483
Khan W, Rayirath UP, Subramanian S, Jithesh MN, Rayorath P, Hodges DM, Critchley AT, Craigie JS, Norrie J, Prithiviraj B (2009) Seaweed extracts as biostimulants of plant growth and development. J Plant Growth Regul 28:386–399
Khan S, Ibrar D, Bashir S, Rashid N, Hasnain Z, Nawaz M, Al-Ghamdi AA, Elshikh MS, Dvořáčková H, Dvořáček J (2022) Application of moringa leaf extract as a seed priming agent enhances growth and physiological attributes of rice seedlings cultivated under water deficit regime. Plants 11:261. https://doi.org/10.3390/plants11030261
Layek J, Das A, Idapuganti RG, Sarkar D, Ghosh A, Zodape ST, Lal R, Yadav GS, Panwar AS, Ngachan S, Meena RS (2018) Seaweed extract as organic bio-stimulant improves productivity and quality of rice in eastern Himalayas. J Appl Phycol 30:547–558
Li S, Yang W, Yang T, Chen Y, Ni W (2015) Effects of cadmium stress on leaf chlorophyll fluorescence and photosynthesis of Elsholtzia argyi—a cadmium accumulating plant. Int J Phytoremediat 17:85–92
Li J, Wang X, Lin X, Yan G, Liu L, Zheng H, Zhao B, Tang J, Guo Y-D (2018) Alginate-derived oligosaccharides promote water stress tolerance in cucumber (Cucumis sativus L.). Plant Physiol Biochem 130:80–88
Li N, Feng A, Liu N, Jiang Z, Wei S (2020) Silicon application improved the yield and nutritional quality while reduced cadmium concentration in rice. Environ Sci Pollut Res 27:20370–20379
MacKinnon SA, Craft CA, Hiltz D, Ugarte R (2010) Improved methods of analysis for betaines in Ascophyllum nodosum and its commercial seaweed extracts. J Appl Phycol 22:489–494
Mahmud JA, Bhuyan MHMB, Anee TI, Nahar K, Fujita M, Hasanuzzaman M (2019) Reactive oxygen species metabolism and antioxidant defense in plants under metal/metalloid stress. In: Hasanuzzaman M, Hakeem KR, Nahar K, Alharby H (eds) Plant abiotic stress tolerance. Springer, Cham, pp 221–257
Moyo B, Oyedemi S, Masika PJ, Muchenje V (2012) Polyphenolic content and antioxidant properties of Moringa oleifera leaf extracts and enzymatic activity of liver from goats supplemented with Moringa oleifera leaves/sunflower seed cake. Meat Sci 91:441–447
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Oddo E, Inzerillo S, La Bella F, Grisafi F, Salleo S, Nardini A (2011) Short-term effects of potassium fertilization on the hydraulic conductance of Laurus nobilis L. Tree Physiol 31:131–138
Ozfidan-Konakci C, Yildiztugay E, Bahtiyar M, Kucukoduk M (2018) The humic acid-induced changes in the water status, chlorophyll fluorescence and antioxidant defense systems of wheat leaves with cadmium stress. Ecotoxicol Environ Saf 155:66–75
Principato GB, Rosi G, Talesa V, Govannini E, Uolila L (1987) Purification and characterization of two forms of glyoxalase II from rat liver and brain of Wistar rats. Biochim Biophys Acta 911:349–355
Rady MM, Varma CB, Howladar SM (2013) Common bean (Phaseolus vulgaris L.) seedlings overcome NaCl stress as a result of presoaking in Moringa oleifera leaf extract. Sci Hortic 162:63–70
Raihan MRH, Rahman M, Mahmud NU, Adak MK, Islam T, Fujita M, Hasanuzzaman M (2022) Application of rhizobacteria, Paraburkholderia fungorum and Delftia sp. confer cadmium tolerance in rapeseed (Brassica campestris) through modulating antioxidant defense and glyoxalase systems. Plants 11:2738. https://doi.org/10.3390/plants11202738
Ramzan M, Ayub F, Shah AA, Naz G, Shah AN, Malik A, Sardar R, Telesiński A, Kalaji HM, Dessoky ES, Elgawad HA (2022) Synergistic effect of zinc oxide nanoparticles and Moringa oleifera leaf extract alleviates cadmium toxicity in Linum usitatissimum: antioxidants and physiochemical studies. Front Plant Sci 13:900347. https://doi.org/10.3389/fpls.2022.900347
Rayorath P, Benkel B, Hodges DM, Allan-Wojtas P, MacKinnon S, Critchley AT, Prithiviraj B (2009) Lipophilic components of the brown seaweed, Ascophyllum nodosum, enhance freezing tolerance in Arabidopsis thaliana. Planta 230:135–147
Santner A, Estelle M (2009) Recent advances and emerging trends in plant hormone signaling. Nature 459:1071–1078
Seifikalhor M, Hassani SB, Aliniaeifard S (2020) Seed priming by cyanobacteria (Spirulina platensis) and salep gum enhances tolerance of maize plant against cadmium toxicity. J Plant Growth Regul 39:1009–1021
Shivani GSK, Gill RK, Virk HK, Bhardwaj RD (2022) Methylglyoxal detoxification pathway-explored first time for imazethapyr tolerance in lentil (Lens culinaris L.). Plant Physiol Biochem 177:10–22
Silva AJ, Nascimento CWA, Gouveia-Neto AS (2017) Assessment of cadmium phytotoxicity alleviation by silicon using chlorophyll a fluorescence. Photosynthetica 55:648–654
Sofo A, Scopa A, Nuzzaci M, Vitti A (2015) Ascorbate peroxidase and catalase activities and their genetic regulation in plants subjected to drought and salinity stresses. Int J Mol Sci 16:13561–13578
Sreelatha S, Jeyachitra A, Padma PR (2011) Antiproliferation and induction of apoptosis by Moringa oleifera leaf extract on human cancer cells. Food Chem Toxicol 49:1270–1275
Trivedi K, Anand KGV, Vaghela P, Ghosh A (2018) Differential growth, yield and biochemical responses of maize to the exogenous application of Kappaphycus alvarezii seaweed extract, at grain-filling stage under normal and drought conditions. Algal Res 35:236–244
Vardhan KH, Kumar PS, Panda RC (2019) A review on heavy metal pollution, toxicity and remedial measures: current trends and future perspectives. J Mol Liq 290:111197. https://doi.org/10.1016/j.molliq.2019.111197
Xue D, Chen M, Zhang G (2009) Mapping of QTLs associated with cadmium tolerance and accumulation during seedling stage in rice (Oryza sativa L.). Euphytica 165:587–596
Ye W, Wu F, Zhang G, Fang Q, Lu H, Hu H (2020) Calcium decreases cadmium concentration in root but facilitates cadmium translocation from root to shoot in rice. J Plant Growth Regul 39:422–429
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 14:7405–7432
Zaid A, Mohammad F, Wani SH, Siddique KM (2019) Salicylic acid enhances nickel stress tolerance by up-regulating antioxidant defense and glyoxalase systems in mustard plants. Ecotoxicol Environ Saf 180:575–587
Zhang K, Wang G, Bao M, Wang L, Xie X (2019) Exogenous application of ascorbic acid mitigates cadmium toxicity and uptake in Maize (Zea mays L.). Environ Sci Pollut Res Int 26:19261–19271
Zhao C, Zhang H, Song C, Zhu JK, Shabala S (2020) Mechanisms of plant responses and adaptation to soil salinity. Innovation 1:100017
Acknowledgements
We cordially acknowledge Md. Mahabub Alam for his generous help during the biochemical analysis. We are thankful to Khussboo Rahman, Mira Rahman, Naznin Ahmed, and Khadeja Sultana Sathi for their assistance during the fieldwork. We also thankful to Ayesha Siddika for her critical review of the manuscript.
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M.H. and K.N. conceived and designed the experiments. M.R.H.R., F.N., and K.N. conducted the experiments. M.H. provided the methodologies and supervised the experiments. M.H. analyzed the data and prepared the illustration. M.H., M.R.H.R, and F.N. wrote the manuscript draft. M.H. and K.N. revised, edited, and formatted the manuscript. All authors read and approved the manuscript.
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Hasanuzzaman, M., Raihan, M.R.H., Nowroz, F. et al. Insight into the physiological and biochemical mechanisms of biostimulating effect of Ascophyllum nodosum and Moringa oleifera extracts to minimize cadmium-induced oxidative stress in rice. Environ Sci Pollut Res 30, 55298–55313 (2023). https://doi.org/10.1007/s11356-023-26251-7
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DOI: https://doi.org/10.1007/s11356-023-26251-7