Mitigating Arsenic-Induced Stress in Tomato through Boron Priming: Enhancing Plant Resilience and Antioxidant Defence Systems

Abstract

Apart from single and combined effect studies, priming stands out as a strategy that alleviates the effects of primary stress by inducing a mild oxidative stress through the administration of a priming agent prior to the actual stress. Arsenic (As) has a high potential to be found in agricultural lands, especially in irrigation water. In this study, tomato seedlings primed with different concentrations of boron (B) were subjected to 25 micromolar As application. At the end of the study, malondialdehyde (MDA) content, chlorophyll content, As accumulation, and the activities of antioxidant enzymes such as superoxide dismutase (SOD), catalase (CAT), and ascorbate peroxidase (APx) were analysed. The results showed that compared to the group treated with As alone, the groups treated with As+B significantly reduced the effects of stress up to a certain concentration. One of the significant findings was that arsenic accumulation decreased in all primed concentrations. This study demonstrates that boron priming at an appropriate concentration can be useful for cultivating plants resistant to environmental conditions, especially in arsenic-contaminated agricultural areas.

Keywords

• Priming
• Boron
• Antioxidant system
• Reactive Oxygen Species
• Arsenic

References

1. [1]. Liu,B, Asseng,S, Müller,C, Ewert,F, Elliott,J, Lobell,DB, Martre,P, Ruane,AC, Wallach,D, Jones,JW, Rosenzweig,C, Aggarwal,PK, Alderman,PD, Anothai,J, Basso,B, Biernath,C, Cammarano,D, Challinor,A, Deryng,D, Sanctis,GD. 2016. Similar estimates of temperature impacts on global wheat yield by three independent methods. Nature Climate Change 6: 1130–1136.
2. [2]. Rezaei EE, Webber,H, Asseng,S, Boote,K, Durand,JL, Ewert,F, Martre,P, MacCarthy,DS. 2023. Climate change impacts on crop yields. Nature Reviews Earth & Environment 4: 831–846.
3. [3]. Tuomisto,H, Scheelbeek,PFD, Chalabi,Z, Green,R, Smith,RD, Haines,A, Dangour,AD. 2017. Effects of environmental change on population nutrition and health: A comprehensive framework with a focus on fruits and vegetables. Wellcome Open Research 2: 21.
4. [4]. Forti,C, Shankar,A, Singh,A, Balestrazzi,A, Prasad,V, Macovei,A. 2020. Hydropriming and Biopriming Improve Medicago truncatula Seed Germination and Upregulate DNA Repair and Antioxidant Genes. Genes 11:.
5. [5]. Khan,MA, Durga,DP, Khan,FA, Khan,A, Belal,BA, Astha,A. 2024. Seed priming: An overview of techniques, mechanisms, and applications. Plant Science Today.
6. [6]. Carvalho,A, Reis,S, Pavia,I, Lima-Brito,JE. 2019. Influence of seed priming with iron and/or zinc in the nucleolar activity and protein content of bread wheat. Protoplasma 256: 763–775.
7. [7]. Ajouri,A, Asgedom,H, Becker,M. 2004. Seed priming enhances germination and seedling growth of barley under conditions of P and Zn deficiency. Journal of Plant Nutrition and Soil Science 167: 630–636.
8. [8]. Nouri,M, Haddioui,A. 2021. Improving seed germination and seedling growth of Lepidium sativum with different priming methods under arsenic stress. Acta Ecologica Sinica 41: 64–71.

9. [9]. Mondal,S, Bose,B. 2019. Impact of micronutrient seed priming on germination, growth, development, nutritional status and yield aspects of plants. Journal of Plant Nutrition 42: 2577–2599.
10. [10]. Brown PH, Bellaloui,N, Wimmer,MA, Bassil,ES, Ruiz,J, Hu,H, Pfeffer,H, Dannel,F, Römheld,V. 2002. Boron in plant biology. Plant Biology 4: 205–223.
11. [11]. Riaz,M, Wu,X, Yan,L, Hussain,S, Aziz,O, Shah,A, Jiang,C. 2018. Boron supply alleviates al-induced inhibition of root elongation and physiological characteristics in rapeseed (Brassica napus L). Journal of Plant Interactions 13: 270–276.
12. [12]. Chakraborty,P, Dwivedi,P, Aydin,M, Tombuloglu,G, Sakcali,MS, Hakeem,KR, Tombuloglu,H, Riaz,M, Kamran,M, Rizwan,M, Ali,S, Zhou,Y, Núñez-Delgado,A, Wang,X, Shireen,F, Nawaz,MA, Lu,J, Xiong,M, Kaleem,M, Huang,Y. 2021. Boron mitigates cadmium toxicity to rapeseed (Brassica napus) shoots by relieving oxidative stress and enhancing cadmium chelation onto cell walls. Ecotoxicology and Environmental Safety 19: 112828.
13. [13]. Meharg,AA, Macnair,MR. 1992. Suppression of the High Affinity Phosphate Uptake System: A Mechanism of Arsenate Tolerance in Holcus lanatus L. Journal of Experimental Botany 43: 519–524.
14. [14]. Asgher,M, Ahmed,S, Sehar,Z, Gautam,H, Gandhi,SG, Khan,NA. 2021. Hydrogen peroxide modulates activity and expression of antioxidant enzymes and protects photosynthetic activity from arsenic damage in rice (Oryza sativa L). Journal of Hazardous Materials 401: 123365.
15. [15]. Gupta,A, Dubey,P, Kumar,M, Roy,A, Sharma,D, Khan,MM, Bajpai,AB, Shukla,RP, Pathak,N, Hasanuzzaman,M. 2022. Consequences of Arsenic Contamination on Plants and Mycoremediation-Mediated Arsenic Stress Tolerance for Sustainable Agriculture. Plants (Basel, Switzerland) 11:.
16. [16]. Sandhi,A, Yu,C, Rahman,MM, Amin,MN. 2022. Arsenic in the water and agricultural crop production system: Bangladesh perspectives. Environmental Science and Pollution Research International 29: 51354–51366.
17. [17]. Raja,V, Majeed,U, Kang,H, Andrabi,KI, John,R. 2017. Abiotic stress: Interplay between ROS, hormones and MAPKs. Environmental and Experimental Botany 137: 142–157.
18. [18]. Shireen F, Nawaz,MA, Lu,J, Xiong,M, Kaleem,M, Huang,Y, Bie,Z. 2021. Application of boron reduces vanadium toxicity by altering the subcellular distribution of vanadium, enhancing boron uptake and enhancing the antioxidant defense system of watermelon. Ecotoxicology and Environmental Safety 226: 112828.
19. [19]. Witham,FH, Blaydes,DF, Devlin,RM. 1973. Experiments in plant physiology, New York, .
20. [20]. Heath,RL, Packer,L. 1968. Photoperoxidation in isolated chloroplasts I Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 125: 189–198.
21. [21]. Chen,T, Zhang,B. 2016. Measurements of Proline and Malondialdehyde Content and Antioxidant Enzyme Activities in Leaves of Drought Stressed Cotton. BIO-PROTOCOL 6: 1–14.
22. [22]. Duman,F, Urey,E, Temizgul,R, Bozok,F. 2010. Biological responses of a non-target aquatic plant (Nasturtium officinale) to the herbicide, tribenuron-methyl. Weed Biology and Management 10: 81–90.
23. [23]. Sen,A, Puthur,JT. 2020. Influence of different seed priming techniques on oxidative and antioxidative responses during the germination of Oryza sativa varieties. Physiology and Molecular Biology of Plants 26: 551–565.
24. [24]. Çatav,ŞS, Genç,TO, Kesik,Oktay,M, Kkakyüz,K. 2018. Effect of Boron Toxicity on Oxidative Stress and Genotoxicity in Wheat (Triticum aestivum L). Bulletin of Environmental Contamination and Toxicology 100: 502–508.
25. [25]. Kar,M, Gökpınar,G, Doğan,Ö. 2024. Hidrojen Peroksit Prımıng Yoluyla Domates Bitkilerinde Tuz Stresinin Azaltılması: Antioksidan Enzim Aktivitelerinin Ve Gen İfadesinde Meydana Gelen Değişimler. Eskişehir Teknik Üniversitesi Bilim ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji 13: 118–132.
26. [26]. Günay,E, Teker,Yıldız,M, Acar,O. 2022. Effects of Different Priming Treatments on Germination and Seedling Growth of Wheat under Drought Stress TT - Kuraklık Stresi Altında Farklı Priming Uygulamalarının Buğdayda Çimlenme ve Fide Büyümesi Üzerine Etkileri. ÇOMÜ Ziraat Fakültesi Dergisi 10: 303–311.
27. [27]. Poomani,S, Yadav,S, Choudhary,R, Singh,D, Dahuja,A, Yadav,SK. 2023. Seed priming with humic acid modifies seedling vigor and biochemical response of lentilunder heat stress conditions. Turkish Journal of Agriculture and Forestry 47: 1043–1057.
28. [28]. Aksakal,O, Esim,N. 2015. Evaluation of arsenic trioxide genotoxicity in wheat seedlings using oxidative system and RAPD assays. Environmental Science and Pollution Research 22: 7120–7128.
29. [29]. Chakrabarty,D, Trivedi,PK, Misra,P, Tiwari,M, Shri,M, Shukla,D, Kumar,S, Rai,A, Pandey,A, Nigam,D, Tripathi,RD, Tuli,R. 2009. Comparative transcriptome analysis of arsenate and arsenite stresses in rice seedlings. Chemosphere 74: 688–702.
30. [30]. Wiszniewska,A. 2021. Priming strategies for benefiting plant performance under toxic trace metal exposure. Plants 10:.
31. [31]. Jiang,Y, Gao,Z, Zhang,X, Nikolic,M, Liang,Y. 2023. Effects of exogenous salicylic acid on alleviation of arsenic-induced oxidative damages in rice. Journal of Plant Nutrition 46: 2811–2826.
32. [32]. Tombuloglu,H, Semizoglu,N, Sakcali,S, Kekec,G. 2012. Boron induced expression of some stress-related genes in tomato. Chemosphere 86: 433–438.
33. [33]. Abbas,G, Murtaza,B, Bibi,I, Shahid,M, Niazi,NK, Khan,MI, Amjad,M, Hussain,M. 2018. Arsenic Uptake, Toxicity, Detoxification, and Speciation in Plants: Physiological, Biochemical, and Molecular Aspects. International Journal of Environmental Research and Public Health 15:.
34. [34]. Zulfiqar,F, Nafees,M, Chen,J, Darras,A, Ferrante,A, Hancock,JT, Ashraf,M, Zaid,A, Latif,N, Corpas,FJ, Altaf,MA, Siddique,KHM. 2022. Chemical priming enhances plant tolerance to salt stress. Frontiers in Plant Science 13: 1–22.
35. [35]. Kerchev,P, van der Meer,T, Sujeeth,N, Verlee,A, Stevens,C,V, Van,Breusegem,F, Gechev,T. 2020. Molecular priming as an approach to induce tolerance against abiotic and oxidative stresses in crop plants. Biotechnology Advances 40: 107503.
36. [36]. ElSayed,AI, Rafudeen,MS, Ganie,SA, Hossain,MS, Gomaa,AM. 2022. Seed priming with cypress leaf extract enhances photosynthesis and antioxidative defense in zucchini seedlings under salt stress. Scientia Horticulturae 293: 110707.
37. [37]. Kar,M. 2018. Determination of the expression level of stress-related genes in Cicer arietinum root cell under Cd stress and the relationship to H 2 O 2 concentrations. Ecotoxicology 27: 1087–1094.
38. [38]. Ruiz,JM, Rivero,RM, Romero,L. 2006. Boron Increases Synthesis of Glutathione in Sunflower Plants Subjected to Aluminum Stress. Plant and Soil 279: 25–30.
39. [39]. Riaz,M, Kamran,M, Rizwan,M, Ali,S, Zhou,Y, Núñez-Delgado,A, Wang,X. 2021. Boron application mitigates Cd toxicity in leaves of rice by subcellular distribution, cell wall adsorption and antioxidant system. Ecotoxicology and Environmental Safety 222:.
40. [40]. Brdar-Jokanović,M. 2020. Boron Toxicity and Deficiency in Agricultural Plants. International Journal of Molecular Sciences 21:.
41. [41]. Chen,XF, Hua,D, Zheng,ZC, Zhang,J, Huang,WT, Chen,HH, Huang,ZR, Yang,LT, Ye,X, Chen,LS. 2022. Boron-mediated amelioration of copper-toxicity in sweet orange [Citrus sinensis (L) Osbeck cv Xuegan] seedlings involved reduced damage to roots and improved nutrition and water status. Ecotoxicology and Environmental Safety 234: 113423.