Ameliorative role of salicylic acid on morpho-anatomy and physiology of rapeseed (Brassica napus L.) under lead stress

Anbreen SULTAN; Abdul HASEEB; Daji LI; Iqra LATIF; Abdul GHAFOOR

doi:10.15835/nbha53314703

Authors

Anbreen SULTAN The Islamia University of Bahawalpur, Department of Botany, Bahawalnagar Campus, 62300 (PK)
Abdul HASEEB The Islamia University of Bahawalpur, Department of Botany, Bahawalnagar Campus, 62300 (PK)
Daji LI Baicheng Normal University, School of Life Science, Baicheng, Jilin, 137000 (CN)
Iqra LATIF The Islamia University of Bahawalpur, Department of Botany, Bahawalnagar Campus, 62300 (PK)
Abdul GHAFOOR King Faisal University, Water and Environmental Studies Center, Al-Ahsa, 31982 (SA)

DOI:

https://doi.org/10.15835/nbha53314703

Keywords:

anatomy, Brassica, heavy metals, lead, morphology, salicylic acid

Abstract

Heavy metals, due to their pervasiveness is serious threat to crop productivity. Lead (Pb) is an incredibly toxic and unnecessary heavy metal that makes its entry into the plants via contaminated soil. Salicylic acid (SA), a plant-derived hormone has the ability to assist pants to strengthen their immune system against toxic metals like lead (Pb). This research intends to investigate the alleviating impact of salicylic acid on the morphology, anatomy and physiology of B. napus (rapeseed) plants during the toxicity of lead (Pb). The plants were treated with 3 levels of lead (lead nitrate) i.e. 1 mM, 2 mM, and 4 mM along with salicylic acid and without salicylic acid. Two levels of salicylic acid i.e. 0.5 mM and 1 mM were used in the form of foliar spray. The results indicated that Pb induced damage is alleviated by SA and the morphological traits were improved i.e root length (58%), shoot length (16%), root fresh weight (73%), shoot fresh weight (79%) and dry weight of root (66%) and shoot (74%), number of leaves (87%), leaf area (61%), and yield (78%) as compared to Pb stress. Similarly, the anatomical features i.e. epidermal thickness (46-63%), vascular tissue area (42-54%), cellular thickness (27-59%) of the plant also improved with SA treatment in comparison to Pb stress. The physiological parameter i.e chlorophyll pigments (chlorophyll a, b and total chlorophyll) were also increased by 2-4% with SA as compared to Pb toxicity. However, the higher level of SA (1 mM) proved less beneficial as compared to the lower level (0.5 mM) in mitigating the effects caused by stress. According to these outcomes, SA could serve as a helpful approach for enhancing the tolerance of B. napus to withstand stressed conditions, hence improving crop resilience in Pb-containing soils.

References

Agnihotri A, Gupta P, Dwivedi A, Seth CS (2018). Counteractive mechanism(s) of salicylic acid in response to lead toxicity in Brassica juncea (L.) Czern. cv. Varuna. Planta 248:49- 68. https://doi.org/10.1007/s00425-018-2867-0

Ahmed S, Khan M, Sardar R (2023). Glutathione primed seed improved lead-stress tolerance in Brassica rapa L. through modulation of physio-biochemical attributes and nutrient uptake. International Journal of Phytoremediation 25(12):1614 -1624. https://doi.org/10.1080/15226514.2023.2178380

Akbar F, Begum KN (2020). A comparative anatomical investigation of three taxa of Brassica L. from Bangladesh. Bangladesh Journal of Plant Taxonomy 27(1):15-26. https://doi.org/10.3329/bjpt.v27i1.47566

Alamri SA, Siddiqui MH, Al-Khaishany MY, Khan MN, Ali HM, Alaraidh IA, Alsahli AA, Al-Rabiah H, Mateen M (2018). Ascorbic acid improves the tolerance of wheat plants to lead toxicity. Journal of Plant Interactions 13(1):409-419. https://doi.org/10.1080/17429145.2018.1491067

Ali B, Gill RA, Yang S, Gill MB, Farooq MA, Liu D, … Zhou W (2015). Regulation of cadmium-induced proteomic and metabolic changes by 5-aminolevulinic acid in leaves of Brassica napus L. PLoS One 10(4):e0123328. https://doi.org/10.1371/journal.pone.0123328

Arif H, Aggarwal S (2018). Salicylic Acid (Aspirin). In: StatPearls. StatPearls Publishing.

Arnon DI (1949). Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta Vulgaris. Plant Physiology 24(1):1-15. https://doi.org/10.1104/pp.24.1.1

Arshad T, Maqbool N, Javed F, Arshad MU (2017). Enhancing the defensive mechanism of lead affected barley (Hordeum vulgare L.) genotypes by exogenously applied salicylic acid. Journal of Agricultural Science 9(2):139. https://doi.org/10.5539/jas.v9n2p139

Ashraf U, Tang X (2017). Yield and quality responses, plant metabolism and metal distribution pattern in aromatic rice under lead (Pb) toxicity. Chemosphere 176:141-155. https://doi.org/10.1016/j.chemosphere.2017.02.103

Borges CE, Von dos Santos Veloso R, Da Conceição CA, Mendes DS, Ramirez-Cabral NY, Shabani F, ... DaSilva RS (2023). Forecasting Brassica napus production under climate change with a mechanisticspecies distribution model. Scientific Reports 13(1):12656. https://doi.org/10.1038/s41598-023 -38910-3

Chaudhari J, Patel K, Patel V (2016). Exploring the toxic effects of Pb & Ni on stem anatomy of Pisum sativum L. International Journal of Chemical, Environmental & Biological Sciences (IJCEBS) 4(1):28-32.

Dalyan E, Yüzbaşıoğlu E, Akpınar I (2018). Effect of 24-Epibrassinolide on antioxidative defence system against lead-induced oxidative stress in the roots of Brassica juncea L. seedlings. Russian Journal of Plant Physiology 65(4):570-578. https://doi.org/10.1134/s1021443718040118

Dalyan E, Yüzbaşıoğlu E, Akpınar I (2020). Physiological and biochemical changes in plant growth and different plant enzymes in response to lead stress. In: Gupta D, Chatterjee S, Walther C (Eds). In: Radionuclides and Heavy Metals in Environment , pp. 129-147. https://doi.org/10.1007/978-3-030-21638-2_8

de Freitas-Silva L, De Araújo TO, Da Silva LC, De Oliveira JA, De Araujo JM (2016). Arsenic accumulation in Brassicaceae seedlings and its effects on growth and plant anatomy. Ecotoxicology and Environmental Safety 124:1-9. https://doi.org/10.1016/j.ecoenv.2015.09.028

Ding Y, Jian H, Wang T, Di F, Wang J, Li J, Liu L (2018). Screening of candidate gene responses to cadmium stress by RNA sequencing in oilseed rape (Brassica napus L.). Environmental Science and Pollution Research 25(32):32433-32446. https://doi.org/10.1007/s11356-018-3227-0

Ejaz U, Khan SM, Khalid N, Ahmad Z, Jehangir S, Fatima Rizvi Z, ... Raposo A (2023). Detoxifying the heavy metals: a multipronged study of tolerance strategies against heavy metals toxicity in plants. Frontiers in Plant Science 14:1154571. https://doi.org/10.3389/fpls.2023.1154571

Elings A (2000). Estimation of leaf area in tropical maize. Agronomy Journal 92(3):436-444. https://doi.org/10.2134/agronj2000.923436x

Emamverdian A, Ding Y, Mokhberdoran F (2020). The role of salicylic acid and gibberellin signaling in plant responses to abiotic stress with an emphasis on heavy metals. Plant Signaling & Behavior 15(7):1777372. https://doi.org/10.1080/15592324.2020.1777372

Ghani A, Khan I, Ahmed I, Mustafa I, Abd-Ur-Rehman, Muhammad Net al. (2015). Amelioration of lead toxicity in Pisum sativum (L.) by foliar application of salicylic acid. Journal of Environmental and Analytical Toxicology 5(292). https://doi.org/10.4172/2161-0525.1000292

Ghori N, Ghori T, Hayat MQ, Imadi SR, Gul A, Altay V, Ozturk M (2019). Heavy metal stress and responses in plants. International Journal of Environmental Science and Technology 16(3):1807-1828. https://doi.org/10.1007/s13762-019-02215-8

Gill RA, Zang L, Ali B, Farooq MA, Cui P, Yang S, Zhou W (2015). Chromium-induced physio-chemical and ultrastructural changes in four cultivars of Brassica napus L. Chemosphere 120:154-164. https://doi.org/10.1016/j.chemosphere.2014.06.0290

Gondor OK, Pál M, Darkó É, Janda T, Szalai G (2016). Salicylic acid and sodium salicylate alleviate cadmium toxicity to different extents in maize (Zea mays L.). PLoS OneNE 11(8):e0160157. https://doi.org/10.1371/journal.pone.0160157

Guo Z, Gao Y, Yuan X, Yuan M, Huang L, Wang S, ... Duan C (2023). Effects of heavy metals on stomata in plants: A review. International Journal of Molecular Sciences 24(11):9302. https://doi.org/10.3390/ijms24119302

Hadi F, Aziz T (2015). A mini review on lead (Pb) toxicity in plants. Journal of Biology and Life Science 6(2):91-–101. https://doi.org/10.5296/jbls.v6i2.7152

Hasanuzzaman M, Matin MA, Fardus J, Hasanuzzaman M, Hossain MS, Parvin K (2019). Foliar application of salicylic acid improves growth and yield attributes by upregulating the antioxidant defense system in Brassica campestris plants grown in lead-amended soils. Acta Agrobotanica 72(2):1756. https://doi.org/10.5586/aa.1765

Hattab S, Hattab S, Flores-Casseres ML, Boussetta H, Doumas P, Hernandez LE, Banni M (2016). Characterisation of lead-induced stress molecular biomarkers in Medicago sativa plants. Environmental and Experimental Botany 123:1-12. https://doi.org/10.1016/j.envexpbot.2015.10.005

Hou X, Han H, Cai L, Liu A, Ma X, Zhou C, Wang G, Meng F (2018). Pb stress effects on leaf chlorophyll fluorescence, antioxidative enzyme activities, and organic acid contents of Pogonatherum crinitum seedlings. Flora 240:82-88. https://doi.org/10.1016/j.flora.2018.01.006

Jayasri MA, Suthindhiran K (2016). Effect of zinc and lead on the physiological and biochemical properties of aquatic plant Lemna minor: its potential role in phytoremediation. Applied Water Science 7(3):1247-1253. https://doi.org/10.1007/s13201-015-0376-x

Kaur L (2018). Accumulation potential of Indian mustard (Brassica juncea var. arawali) and fenugreek (Trigonella foenum-graecum L.) planted on lead and nickel contaminated soil. Tropical Plant Research 5(2):217-223. https://doi.org/10.22271/tpr.2018.v5.i2.027

Khan MM, Islam E, Irem S, Akhtar K, Ashraf MY, Iqbal J, Liu D (2018b). Pb-induced phytotoxicity in para grass (Brachiaria mutica) and castorbean (Ricinus communis L.): Antioxidant and ultrastructural studies. Chemosphere 200:257-265. https://doi.org/10.1016/j.chemosphere.2018.02.101

Khare S, Singh N, Niharika N, Singh A, Amist N, Azim Z, Yadav RK (2022). Phytochemicals mitigation of Brassica napus by IAA grown under Cd and Pb toxicity and its impact on growth responses of Anagallis arvensis. Journal of Biotechnology 343:83-95. https://doi.org/10.1016/j.jbiotec.2021.12.001

Kohli SK, Handa N, Sharma A, Gautam V, Arora S, Bhardwaj R, Wijaya L, Alyemeni MN, Ahmad P (2018). Interaction of 24-epibrassinolide and salicylic acid regulates pigment contents, antioxidative defense responses, and gene expression in Brassica juncea L. seedlings under Pb stress. Environmental Science and Pollution Research 25(15):15159-15173. https://doi.org/10.1007/s11356-018-1742-7

Kumar A, Pal L, Agrawal V (2017). Glutathione and citric acid modulates lead- and arsenic-induced phytotoxicity and genotoxicity responses in two cultivars of Solanum lycopersicum L. Acta Physiologiae Plantarum 39:(151). https://doi.org/10.1007/s11738-017-2448-z

Piršelová B, Kubová V, Boleček P, Hegedűsová A (2021). Impact of cadmium toxicity on leaf area and stomatal characteristics in Faba bean. Journal of Microbiology, Biotechnology and Food Sciences 11(2):e3718-e3718. https://doi.org/10.15414/jmbfs.3718

Pratima H, Pratima M (2016). Lead-induced oxidative stress and metabolic alteration in seedlings of Brassica juncea L. International Research Journal of Environmental Sciences 5(3):37-41. URL: http://www.isca.in/IJENS/Archive/v5/i3/5.ISCA-IRJEVS-2015-263.php

Raboanatahiry N, Li H, Yu L, Li M (2021). Rapeseed (Brassica napus): Processing, utilization, and genetic improvement. Agronomy 11(9):1776. https://doi.org/10.3390/agronomy11091776

Rai GK, Bhat BA, Mushtaq M, Tariq L, Rai PK, Basu U, ... Bhat JA (2021). Insights into decontamination of soils by phytoremediation: A detailed account on heavy metal toxicity and mitigation strategies. Physiologia Plantarum 173(1):287-304. https://doi.org/10.1111/ppl.13433

Riyazuddin R, Nisha N, Ejaz B, Khan MIR, Kumar M, Ramteke PW, Gupta R (2022). A comprehensive review on the heavy metal toxicity and sequestration in plants. Biomolecules 12(1):43. https://doi.org/10.3390/biom12010043

Rizwan M, Ali S, Rehman MZU, Javed MR, Bashir A (2018). Lead toxicity in cereals and its management strategies: A critical review. Water Air & Soil Pollution 229(6):1-14. https://doi.org/10.1007/s11270-018-3865-3

Romero-Freire A, Peinado FM, Van Gestel CAM (2015). Effect of soil properties on the toxicity of Pb: Assessment of the appropriateness of guideline values. Journal of Hazardous Materials 289:46-53. https://doi.org/10.1016/j.jhazmat.2015.02.034

Saman RU, Shahbaz M, Maqsood MF, Lili N, Zulfiqar U, Haider FU, ... Shahzad B (2022). Foliar application of ethylenediamine tetraacetic acid (EDTA) improves the growth and yield of brown mustard (Brassica juncea) by modulating photosynthetic pigments, antioxidant defense, and osmolyte production under lead (Pb) stress. Plants 12(1):115. https://doi.org/10.3390/plants12010115

Sanders JL, Brown DA (1976). Effect of variations in the shoot: root ratio upon the chemical composition and growth of soybeans. Agronomy Journal 68(5):713-717. https://doi.org/10.2134/agronj1976.00021962006800050006x

Seneviratne M, Rajakaruna N, Rizwan M, Madawala HMSP, Ok YS, Vithanage M (2017). Heavy metal-induced oxidative stress on seed germination and seedling development: A critical review. Environmental Geochemistry and Health 41(4):1813-1831. https://doi.org/10.1007/s10653-017-0005-8

Sharma A, Sidhu GPS, Araniti F, Bali AS, Shahzad B, Tripathi DK, ... Landi M (2020). The role of salicylic acid in plants exposed to heavy metals. Molecules 25(3):540. https://doi.org/10.3390/molecules25030540

Sheetal KR, Singh SD, Anand A, Prasad S (2016). Heavy metal accumulation and effects on growth, biomass and physiological processes in mustard. Indian Journal of Plant Physiology 21:219-–223. https://doi.org/10.1007/s40502-016-0221-8

Shehzad J, Mustafa G, Arshad H, Ali A, Naveed NH, Riaz Z, Khan I (2023). Morphophysiological and biochemical responses of Brassica species toward lead (Pb) stress. Acta Physiologiae Plantarum 45(1):8. https://doi.org/10.1007/s11738-022-03493-5

Sidhu GPS, Singh HP, Batish DR, Kohli RK (2016). Effect of lead on oxidative status, antioxidative response and metal accumulation in Coronopus didymus. Plant Physiology and Biochemistry 105:290-296. https://doi.org/10.1016/j.plaphy.2016.05.019

Sidhu GPS, Singh HP, Batish DR, Kohli RK (2017). Alterations in photosynthetic pigments, protein, and carbohydrate metabolism in a wild plant Coronopus didymus L. (Brassicaceae) under lead stress. Acta Physiologiae Plantarum 39:(176). https://doi.org/10.1007/s11738-017-2476-8

Silva S, Silva P, Oliveira H, Gaivão I, Matos M, Pinto-Carnide O, Santos C (2016). Pb low doses induced genotoxicity in Lactuca sativa plants. Plant Physiology and Biochemistry 112:109-116. https://doi.org/10.1016/j.plaphy.2016.12.026

Thien SJ (1979). A flow diagram for teaching texture‐by‐feel analysis. Journal of Agronomic Education 8(1):54-55. https://doi.org/10.2134/jae.1979.0054

Tupan CI, Azrianingsih R (2016). Accumulation and deposition of lead heavy metal in the tissues of roots, rhizomes and leaves of seagrass Thalassia hemprichii (Monocotyledoneae, Hydrocharitaceae). Aquaculture, Aquarium, Conservation & Legislation 9(3):580-589. http://www.bioflux.com.ro/docs/2016.580-589.pdf

Venkatachalam P, Jayalakshmi N, Geetha N, Sahi SV, Sharma NC, Rene ER, Sarkar SK, Favas PJ (2017). Accumulation efficiency, genotoxicity and antioxidant defense mechanisms in medicinal plant Acalypha indica L. under lead stress. Chemosphere 171:544-553. https://doi.org/10.1016/j.chemosphere.2016.12.092

Wafee C, Khan AS, Siddiqi MR (2018). Phytoremediation potential of Catharanthus roseus L. and effects of lead (Pb) toxicity on its morpho-anatomical features. Pakistan Journal of Botany 50(4):1323-1326. https://www.pakbs.org/pjbot_01-02-23/papers/1524638221.pdf

Wang Y, Zhang L, Wang J, Lv J (2020). Identifying quantitative sources and spatial distributions of potentially toxic elements in soils by using three receptor models and sequential indicator simulation. Chemosphere 242:125266. https://doi.org/10.1016/j.chemosphere.2019.125266

Wani AB, Chadar H, Wani AH, Singh S, Upadhyay N (2017). Salicylic acid to decrease plant stress. Environmental Chemistry Letters 15(1):101-123. https://doi.org/10.1007/s10311-016-0584-0

Yadav V, Arif N, Kováč J, Singh VP, Tripathi DK, Chauhan DK, Vaculík M (2021). Structural modifications of plant organs and tissues by metals and metalloids in the environment: a review. Plant Physiology and Biochemistry 159:100-112. https://doi.org/10.1016/j.plaphy.2020.11.047

Zanganeh R, Jamei R, Rahmani F (2021). Response of maize plant to sodium hydrosulfide pretreatment under lead stress conditions at early stages of growth. Cereal Research Communications 49(2):267-276. https://doi.org/10.1007/s42976-020-00095-0

Zengin F (2015). Effects of exogenous salicylic acid on growth characteristics and biochemical content of wheat seeds under arsenic stress. Journal of Environmental Biology 36(1):249-256. http://www.jeb.co.in/journal_issues/201501_jan15/paper_10.pdf

Zhang Y, Deng B, Li Z (2018). Inhibition of NADPH oxidase increases defense enzyme activities and improves maize seed germination under Pb stress. Ecotoxicology and Environmental Safety 158:187-192. https://doi.org/10.1016/j.ecoenv.2018.04.028

Zhang Y, Xu S, Yang S, Chen Y (2015). Salicylic acid alleviates cadmium-induced inhibition of growth and photosynthesis through upregulating antioxidant defense system in two melon cultivars (Cucumis melo L.). Protoplasma 252(3):911-924. https://doi.org/10.1007/s00709-014-0732-y

Zunaidi AA, Lim LH, Metali F (2024). Heavy metal tolerance and accumulation in the Brassica species (Brassica chinensis var. parachinensis and Brassica rapa L.): a pot experiment. Heliyon 10(8):e29528. https://doi.org/10.1016/j.heliyon.2024.e29528