Enhancing antioxidant defense system of mung bean with a salicylic acid exogenous application to mitigate cadmium toxicity

  • Imran KHAN University of Agriculture Faisalabad, Department of Agronomy, Faisalabad, 38040 (PK)
  • Mahmoud F. SELEIMAN King Saud University, College of Food and Agriculture Sciences, Plant Production Department, P.O. Box 2460, Riyadh 11451; Menoufia University, Faculty of Agriculture, Department of Crop Sciences, Shibin El-kom 32514 (SA)
  • Muhammad U. CHATTHA University of Agriculture Faisalabad, Department of Agronomy, Faisalabad, 38040 (PK)
  • Rewaa S. JALAL University of Jeddah, College of Sciences, Department of Biology, Jeddah (SA)
  • Faisal MAHMOOD Government College University Faisalabad, Department of Environmental Sciences & Engineering, Faisalabad (PK)
  • Fahmy A. S. HASSAN Taif University, College of Science, Department of Biology, P.O. Box 11099, Taif 21944 (SA)
  • Warda IZZET University of Agriculture Faisalabad, Department of Botany, Faisalabad, 38040 (PK)
  • Bushra A. ALHAMMAD Prince Sattam Bin Abdulaziz University, College of Science and Humanity Studies, Biology Department, Al Kharj Box 292, Riyadh 11942 (SA)
  • Esmat F. ALI Taif University, College of Science, Department of Biology, P.O. Box 11099, Taif 21944 (SA)
  • Rana ROY Sylhet Agricultural University, Faculty of Agriculture, Department of Agroforestry & Environmental Science, Sylhet 3100 (BD)
  • Omer S. USLU University of Sutcu Imam, Faculty of Agriculture, Department of Field Crops (TR)
  • Muhammad U. HASSAN University of Agriculture Faisalabad, Department of Agronomy, Faisalabad, 38040 (PK)
Keywords: antioxidant machinery, heavy metal stress, mung bean, photosynthesis, reactive oxygen species, salicylic acid

Abstract

Cadmium (Cd) accumulation is an emerging environmental hazard and has detrimental effects on plant growth and development. Salicylic acid (SA) is a well-known plant growth regulator that can initiate various molecular pathways to ameliorate Cd toxicity. The experiment was executed to scrutinize the mediatory role of SA to accelerate the defensive mechanism of mung bean in response to Cd stress. Mung bean plants were exposed to 0, 5, 10 and 15 mg Cd kg-1 of soil. Exogenous application of SA 0, 10-6 and 10-3 M was added prior flowering. Results exhibited that Cd stress considerably reduced the growth-related attributes i.e. shoot length, root length, fresh and dry biomass, total soluble protein, total amino acids, relative water contents and photosynthetic pigments. Cadmium stress showed a significant increase in antioxidants levels such as peroxidase (POD), ascorbate peroxidase (APX), ascorbic acid (AsA), and catalase (CAT) and promoted the accumulation of hydrogen peroxide (H2O2) and malondialdehyde (MDA) contents. However, exogenously applied SA significantly improved plant biomass and photosynthetic pigments under Cd stress. Moreover, SA improved the defensive system by enhancing antioxidants’ activities under the increasing concentration of Cd stress. Furthermore, SA reduced the Cd uptake, membrane damage and, H2O2 and MDA accumulation. The study's findings concluded that exogenous-applied SA enhanced plant growth, promoted the antioxidant activities, and reduced the oxidative damage in mung bean seedlings under Cd stress.

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References

Abbas MS, Akmal M, Ullah S, Hassan MU, Farooq S (2017). Effectiveness of zinc and gypsum application against cadmium toxicity and accumulation in wheat (Triticum aestivum L.). Communications in Soil Science and Plant Analysis 48:1659-1668. https://doi.org/10.1080/00103624.2017.1373798

Acar O, Türkan I, Özdemir F (2001). Superoxide dismutase and peroxidase activities in drought sensitive and resistant barley (Hordeum vulgare L.) varieties. Acta Physiologiae Plantarum 23:351-356. https://link.springer.com/article/10.1007/s11738-001-0043-8

Akhtar J, Ahmad R, Ashraf MY, Tanveer A, Waraich EA, Oraby H (2013). Influence of exogenous application of salicylic acid on salt-stressed mungbean (Vigna radiata): growth and nitrogen metabolism. Pakistan Journal of Botany 45:119-125. https://www.pakbs.org/pjbot/PDFs/45(1)/15.pdf

Aamir M, Hassan MU, Li Z, A Ali, Su Q, Liu L, … Guaqin H (2018). Foliar application of glycinebetaine alleviates the cadmium toxicity in spinach through reducing Cd uptake and improving the activity of anti-oxidant system. Applied Ecology and Environmental Research 16(6):7575-7583. http://dx.doi.org/10.15666/aeer/1606_75757583

Al-Ashkar I, Alderfasi A, Ben Romdhane W, Seleiman MF, El-Said RA, Al-Doss A (2020). Morphological and genetic diversity within salt tolerance detection in eighteen wheat genotypes. Plants 9:287. https://doi.org/10.3390/plants9030287

Anjum NA, Umar S, Iqbal M, Khan NA (2011). Cadmium causes oxidative stress in mung bean by affecting the antioxidant enzyme system and ascorbate-glutathione cycle metabolism. Russian Journal of Plant Physiology 58:92-99. https://link.springer.com/article/10.1134/S1021443710061019

Arnon DI (1949). Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology 24:1-14. https://doi.org/10.1104/pp.24.1.1

Asada K (1987). Production and scavenging of active oxygen in photosynthesis. Photoinhibition 227-287.

Barceló J, Poschenrieder C (1990). Plant water relations as affected by heavy metal stress: a review. Journal of Plant Nutrition 13:1-37. https://doi.org/10.1080/01904169009364057

Bezrukova MV, Fatkhutdinova RA, Lubyanova AR, Murzabaev AR, Fedyaev VV, Shakirova FM (2011). Lectin involvement in the development of wheat tolerance to cadmium toxicity. Russian Journal of Plant Physiology 58:1048-1056. https://link.springer.com/article/10.1134/S1021443711060021

Bradford MM (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Annals of Biochemistry 72:248-254. https://doi.org/10.1006/abio.1976.9999

Cakmak I, Horst WJ (1991). Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiologia Plantarum 83:463-468. https://doi.org/10.1111/j.1399-3054.1991.tb00121.x

Ekmekçi Y, Tanyolac D, Ayhan B (2008). Effects of cadmium on antioxidant enzyme and photosynthetic activities in leaves of two maize cultivars. Journal of Plant Physiology 165:6000611. https://doi.org/10.1016/j.jplph.2007.01.017

Elahi NN, Mustafa S, Mirza JI (2004). Growth and nodulation of mungbean (Vigna radiata (L.) Wilczek) as affected by sodium chloride. Journal of Research and Science of Bahauddin Zakaria Univ Multan, Pakistan 15:139-143. https://www.bzu.edu.pk/jrscience/vol15no2/3.pdf

Gill RA, Zhang N, Ali B, Farooq MA, Xu J, Gill MB, … Zhou W (2016). Role of exogenous salicylic acid in regulating physio-morphic and molecular changes under chromium toxicity in black-and yellow-seeded Brassica napus L. Environmental Science and Pollution Research 23:20483-20496. https://doi.org/10.1007/s11356-016-7167-2

Goldberg AL (2003). Protein degradation and protection against misfolded or damaged proteins. Nature 426:895. https://doi.org/10.1038/nature02263

Guo Q, Meng L, Mao PC, Jia YQ, Shi YJ (2013). Role of exogenous salicylic acid in alleviating cadmium-induced toxicity in Kentucky bluegrass. Biochemical Systematices and Ecology 50:269-276. https://doi.org/10.1016/j.bse.2013.05.002

Hassan MU, Chattha MU, Khan I, Chattha MB, Aamer M, Nawaz M, … Khan TA (2019). Nickel toxicity in plants: reasons, toxic effects, tolerance mechanisms, and remediation possibilities-a review. Environmental Sciences and Pollution Research 26:12673-12688. https://doi.org/10.1007/s11356-019-04892-x

Hassan MU, Aamer M, Chattha MU, Haiying T, Shahzad B, Barbanti L, … Guoqin H (2020). The critical role of zinc in plants facing the drought stress. Agriculture 10(9):396. https://doi.org/10.3390/agriculture10090396

Hassan MU, Muhammad A, Chattha MU, Haiying T, Khan I, Seleiman MF, … Afzal A (2021). Sugarcane distillery spent wash (dsw) as a bio-nutrient supplement: a win-win option for sustainable crop production. Agronomy 11:183. https://doi.org/10.3390/agronomy11010183

Hafez EH, Seleiman MF (2017). Response of barley quality traits, yield and antioxidant enzymes to water-stress and chemical inducers. International Journal of Plant Production 11:477-490.

Hayat Q, Hayat S, Irfan M, Ahmad A (2010). Effect of exogenous salicylic acid under changing environment: a review. Environmental and Experimental Botany 68:14-25. https://doi.org/10.1016/j.envexpbot.2009.08.005

Hsu YT, Kao CH (2003). Role of abscisic acid in cadmium tolerance of rice (Oryza sativa L.) seedlings. Plant Cell and Environment 26:867-874. https://doi.org/10.1046/j.1365-3040.2003.01018.x

Klessig DF (2017). How does the multifaceted plant hormone salicylic acid combat disease in plants and are similar mechanisms utilized in humans? BMC Biology 15:1-23. https://doi.org/10.1186/s12915-017-0364-8

Krantev A, Yordanova R, Janda T, Szalai G, Popova L (2008). Treatment with salicylic acid decreases the effect of cadmium on photosynthesis in maize plants. Journal of Plant Physiology 165:920-931. https://doi.org/10.1016/j.jplph.2006.11.014

Laspina N V, Groppa MD, Tomaro ML, Benavides MP (2005). Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Science 169:323-330. https://doi.org/10.1016/j.plantsci.2005.02.007

Liu J, Qian M, Cai G, Yang J, Zhu Q (2007). Uptake and translocation of Cd in different rice cultivars and the relation with Cd accumulation in rice grain. Journal of Hazardous Materials 143:443-447. https://doi.org/10.1016/j.jhazmat.2006.09.057

Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004). Reactive oxygen gene network of plants. Trends in Plant Science 9:490-498. https://doi.org/10.1016/j.tplants.2004.08.009

Moore S, Stein WH (1954). A modified ninhydrin reagent for the photometric determination of amino acids and related compounds. Journal of biology and Chemistry 211:907-913. https://doi.org/10.1016/S0021-9258(18)71178-2

Mukherjee SP, Choudhuri MA (1983). Implications of water stress‐induced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in Vigna seedlings. Physiology of Plants 58:166-170. https://doi.org/10.1111/j.1399-3054.1983.tb04162.x

Nagamiya K, Motohashi T, Nakao K, Prodhan SH, Hattori E, Hirose S, … Takabe T (2007). Enhancement of salt tolerance in transgenic rice expressing an Escherichia coli catalase gene. Plant Biotechnology Reports 1:49-55. https://link.springer.com/article/10.1007/s11816-007-0007-6

Noriega G, Caggiano E, Lecube ML, Santa Cruz D, Batlle A, Tomaro M, Balestrasse KB (2012). The role of salicylic acid in the prevention of oxidative stress elicited by cadmium in soybean plants. Biometals 25:1155-1165. https://link.springer.com/article/10.1007/s10534-012-9577-z

Oweis T, Pala M, Ryan J (1999). Management alternatives for improved durum wheat production under supplemental irrigation in Syria. European Journal of Agronomy 11:255-266. https://doi.org/10.1016/S1161-0301(99)00036-2

Pietrini F, Iannelli MA, Pasqualini S, Massacci A (2003). Interaction of cadmium with glutathione and photosynthesis in developing leaves and chloroplasts of Phragmites australis (Cav.) Trin. ex Steudel. Plant Physiology 133:829-837. https://doi.org/10.1104/pp.103.026518

Rasheed A, Fahad S, Aamer M, Hassan MU, Tahir MM, Wu ZM (2020). Role of genetic factors in regulating cadmium uptake, transport and accumulation mechanisms and quantitative trait loci mapping in rice. Applied Ecology and Environmental Research 18(3):4005-4023. http://dx.doi.org/10.15666/aeer/1803_40054023

Salem HM, Abdel-Salam A, Abdel-Salam MA, Seleiman MF (2018). Phytoremediation of metal and metalloids from contaminated soil. In: Plants Under Metal and Metalloid Stress. Springer Nature Singapore Pte Ltd.: Singapore, pp 249-262.

Saleem MH, Ali S, Seleiman MF, Rizwan M, Rehman M, Aisha AN, … Mubushar M (2019). Assessing the Correlations between different traits in copper-sensitive and copper-resistant varieties of jute (Corchorus capsularis L.). Plants 8:545. https://doi.org/10.3390/plants8120545

Seleiman MF, Ali S, Refay Y, Rizwan M, Alhammad BA, El-Hendawy SE (2020a). Chromium resistant microbes and melatonin reduced Cr uptake and toxicity, improved physio-biochemical traits and yield of wheat in contaminated soil. Chemosphere 250:126239. https://doi.org/10.1016/j.chemosphere.2020.126239

Seleiman MF, Almutairi KF, Alotaibi M, Shami A, Alhammad BA, Battaglia ML (2021a). Nano-fertilization as an emerging fertilization technique: why can modern agriculture benefit from its use? Plants 10:2. https://doi.org/10.3390/plants10010002

Seleiman MF, Alotaibi MA, Alhammad BA, Alharbi BM, Refay Y, Badawy SA (2020c). Effects of ZnO nanoparticles and biochar of rice straw and cow manure on characteristics of contaminated soil and sunflower productivity, oil quality, and heavy metals uptake. Agronomy 10:790. https://doi.org/10.3390/agronomy10060790

Seleiman MF, Al-Suhaibani N, Ali N, Akmal M, Alotaibi M, Refay Y, … Battaglia ML (2021b) Drought stress impacts on plants and different approaches to alleviate its adverse effects. Plants 10:259. https://doi.org/10.3390/plants10020259.

Seleiman MF, Santanen A, Jaakkola S, Ekholm P, Hartikainen H, Stoddard FL, Mäkelä PS (2013). Biomass yield and quality of bioenergy crops grown with synthetic and organic fertilizers. Biomass Bioenergy 59:477-485.

Seleiman MF, Santanen A, Mäkelä PS (2020b). Recycling sludge on cropland as fertilizer-advantages and risks. Resource Conservation and Recycling 155:104647. https://doi.org/10.1016/j.resconrec.2019.104647

Seleiman MF, Santanen A, Stoddard FL, Mäkelä P (2012). Feedstock quality and growth of bioenergy crops fertilized with sewage sludge. Chemosphere 89:1211-1217. https://doi.org/10.1016/j.chemosphere.2012.07.031

Seleiman MF, Selim S, Jaakkola S, Mäkelä PS (2017) Chemical composition and in vitro digestibility of whole-crop maize fertilized with synthetic fertilizer or digestate and harvested at two maturity stages in Boreal growing conditions. Agricultural and Food Science 26:47-55.

Shakirova FM (2007). Role of hormonal system in the manifestation of growth promoting and antistress action of salicylic acid. In Salicylic acid: a plant hormone. Springer, Dordrecht, pp 69-89.

Shao X, Yang H, Ran K, Jiang Q, Sun X (2010). Effects of salicylic acid on plasma membrane ATPase and free radical of grape root under cadmium stress. Scientia Agricultura Sinica 43:1441-1447. https://doi.org/10.3864/j.issn.0578-1752.2010.07.015

Shi Q, Zhu Z (2008). Effects of exogenous salicylic acid on manganese toxicity, element contents and antioxidative system in cucumber. Environment and Experimental Botany 63:317-326. https://doi.org/10.1016/j.envexpbot.2007.11.003

Šimonová E, Henselová M, Masarovičová E, Kohanová J (2007). Comparison of tolerance of Brassica juncea and Vigna radiata to cadmium. Biology of Plants 51:488-492. https://link.springer.com/article/10.1007/s10535-007-0103-z

Singh PK, Gautam S (2013). Role of salicylic acid on physiological and biochemical mechanism of salinity stress tolerance in plants. Acta Physiologia Plantrum 35:2345-2353. https://link.springer.com/article/10.1007/s11738-013-1279-9

Sofy MR, Seleiman MF, Alhammad BA, Alharbi BM, Mohamed HI, (2020). Minimizing adverse effects of pb on maize plants by combined treatment with jasmonic, salicylic acids and proline. Agronomy 10:699. https://doi.org/10.3390/agronomy10050699

Souza JF, Dolder H, Cortelazzo AL (2005). Effect of excess cadmium and zinc ions on roots and shoots of maize seedlings. Journal of Plant Nutrition 28:1923-1931. https://doi.org/10.1080/01904160500310435

Türkan I, Bor M, Özdemir F, Koca H (2005). Differential responses of lipid peroxidation and antioxidants in the leaves of drought-tolerant P. acutifolius Gray and drought-sensitive P. vulgaris L. subjected to polyethylene glycol mediated water stress. Plant Science 168:223-231. https://doi.org/10.1016/j.plantsci.2004.07.032

Turner NC (1981). Techniques and experimental approaches for the measurement of plant water status. Plant Soil 58:339-366. https://link.springer.com/article/10.1007/BF02180062

Uslu OS, Babur E, Alma MH, Solaiman ZM (2020). Walnut shell biochar increases seed germination and early growth of seedlings of fodder crops. Agriculture 10:427. https://doi.org/10.3390/agriculture10100427

Vassilev A, Perez-Sanz A, Semane B, Carleer R, Vangronsveld J (2005). Cadmium accumulation and tolerance of two Salix genotypes hydroponically grown in presence of cadmium. Journal of Plant Nutrition 28:2159-2177.

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 Science 151:59-66. https://doi.org/10.1016/S0168-9452(99)00197-1

Wahid A, Ghani A, Javed F (2008). Effect of cadmium on photosynthesis, nutrition and growth of mungbean. Agronomy for Sustainable Development 28:273-280. https://link.springer.com/article/10.1051/agro:2008010

White PJ Brown PH (2010). Plant nutrition for sustainable development and global health. Annals of Botany 105:1073-1080. https://doi.org/10.1093/aob/mcq085

Xue Z-C, Gao H-Y, Zhang L-T (2013). Effects of cadmium on growth, photosynthetic rate and chlorophyll content in leaves of soybean seedlings. Biologia Plantarum 57:587-590. https://link.springer.com/article/10.1007/s10535-013-0318-0

Yan B, Dai Q, Liu X, Huang S, Wang Z (1996). Flooding-induced membrane damage, lipid oxidation and activated oxygen generation in corn leaves. Plant Soil 179:261-268. https://link.springer.com/article/10.1007/BF00009336

Yang QW, Lan CY, Wang HB, Zhuang P, Shu WS (2006). Cadmium in soil–rice system and health risk associated with the use of untreated mining wastewater for irrigation in Lechang, China. Agriculture and Water Management 84:147-152.

Yang XE, Long XX, Ye HB, He ZL, Calvert DV, Stoffella PJ (2004). Cadmium tolerance and hyperaccumulation in a new Zn-hyperaccumulating plant species (Sedum alfredii Hance). Plant and Soil 259:181-189. https://doi.org/10.1016/j.agwat.2006.01.005

Yang ZM, Wang J, Wang SH, Xu LL (2003). Salicylic acid-induced aluminum tolerance by modulation of citrate efflux from roots of Cassia tora L. Planta 217:168-174. https://link.springer.com/article/10.1007/s00425-003-0980-0

Published
2021-05-11
How to Cite
KHAN, I., SELEIMAN, M. F., CHATTHA, M. U., JALAL, R. S., MAHMOOD, F., HASSAN, F. A. S., IZZET, W., ALHAMMAD, B. A., ALI, E. F., ROY, R., USLU, O. S., & HASSAN, M. U. (2021). Enhancing antioxidant defense system of mung bean with a salicylic acid exogenous application to mitigate cadmium toxicity. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 49(2), 12303. https://doi.org/10.15835/nbha49212303
Section
Research Articles
CITATION
DOI: 10.15835/nbha49212303

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