Salicylic acid and biochar improve drought tolerance in Borago officinalis L. by enhancing antioxidant enzymes, leaf proline and soluble sugars

Document Type : Original Article

Authors

1 Department of Agronomy and Plant Breeding, Faculty of Agriculture, Shahrood University of Technology, Shahrood, Iran

2 Crop and Horticultural Science Research Department of Semnan (Shahrood), Agricultural and Natural Resources Research Center, AREEO, Shahrood, Iran

Abstract

Water scarcity has become an increasingly important factor contributing to crop yield decline in arid regions. Soil amendments and certain growth regulators are some strategies used to mitigate the negative effects of drought stress. This study aimed to investigate the effects of biochar and salicylic acid on some physiological and biochemical properties of Borago officinalis L. under water deficit conditions. This experiment was conducted as a split-plot factorial experiment based on a randomized complete block design with four replicates. The factors were irrigation regimes according to the percentage of water requirement (100% WR, 75% WR, and 50% WR) in the main plots, biochar application (0, 5, and 10 ton ha-1) and foliar application of salicylic acid (0, 0.5 mM) in the subplots. This study was conducted in the research field of Shahrood University of Technology, Shahrood, Iran, in two cropping years, 2017 and 2018. The results showed that the total amount of soluble sugars decreased with an increase in the irrigation regime; however, the leaf antioxidant enzymes (SOD, CAT, and POX) and leaf proline concentration significantly increased in the 75% WR irrigation regime and slightly decreased in the 50% WR irrigation regime in both years. Applying salicylic acid (0.5 mM) significantly increased the leaf proline by 50% and 55% in irrigation regimes of 100% WR and 75% WR, respectively, in both years. It also modified the total amount of soluble sugars in both years. In addition, salicylic acid also stimulated leaf antioxidant enzymes under 100%WR under 75% WR and 50% WR irrigation regimes in both years. Biochar application reduced leaf proline concentration by 27% and 28% (10 ton ha-1) under 100% WR and 75% WR irrigation regimes, respectively. An improvement of all antioxidant enzymes via biochar application was found in both years. Application of 5 ton ha -1 biochar mitigated relative water content in 75% WR. Our results clearly indicated that applying exogenous salicylic acid in combination with biochar could be a promising approach to improve plant stress tolerance mechanisms under water deficit conditions.

Keywords


Aebi, H. (1984). Catalase in Vitro. Methods in Enzymology. 105, 121–126. https://doi.org/10.1016/S0076-6879(84)05016-3
Abdelli, M., Moghrani, H., Aboun, A. & Maachi, R. (2016). Algerian Mentha pulegium L. leaves essential oil: Chemical composition, antimicrobial, insecticidal and antioxidant activities. Industrial Crops and Products. 94, 197–205. https://doi.org/10.1016/j.indcrop.2016.08.042
Abideen, Z., Koyro, H.W., Huchzermeyer, B., Ansari, R., Zulfiqar, F. & Gul, B. (2020). Ameliorating effects of biochar on photosynthetic efficiency and antioxidant defence of Phragmites karka under drought stress. Plant Biology. 22, 259–266. https://doi.org/10.1111/plb.13054
Adejumo, S.A., Arowo, D.O., Ogundiran, M.B. & Srivastava, P. (2020). Biochar in combination with compost reduced Pb uptake and enhanced the growth of maize in lead (Pb)-contaminated soil exposed to drought stress. Journal of Crop Science and Biotechnology. 23, 273–288. https://doi.org/10.1007/s12892-020-00035-8
Aebi, H. (1984). Catalase in Vitro. Methods in Enzymology. 105, 121–126. https://doi.org/10.1016/S0076-6879(84)05016-3
Akhtar, S.S., Li, G., Andersen, M.N. & Liu, F. (2014). Biochar enhances yield and quality of tomato under reduced irrigation. Agriculture and Water Management. 138, 37–44. https://doi.org/10.1016/j.agwat.2014.02.016
Askari, E. & Ehsanzadeh, P. (2015). Drought stress mitigation by foliar application of salicylic acid and their interactive effects on physiological characteristics of fennel (Foeniculum vulgare Mill.) genotypes. Acta Physiologiae Plantarum. 37. https://doi.org/10.1007/s11738-014-1762-y
Bahadori, M. & Tofighi, H. (2016). A Modified Walkley-Black Method Based on Spectrophotometric Procedure. Communication in Soil Science and Plant Analysis. 47, 213–220. https://doi.org/10.1080/00103624.2015.1118118
Baronti, S., Vaccari, F.P., Miglietta, F., Calzolari, C., Lugato, E., Orlandini, S., Pini, R., Zulian, C. & Genesio, L. (2014). Impact of biochar application on plant water relations in Vitis vinifera (L.). European Journal of Agronomy. 53, 38–44. https://doi.org/10.1016/j.eja.2013.11.003
Barrs, H.D. & Weatherley, P.E. (1962) A Re-Examination of the Relative Turgidity Techniques for Estimating Water Deficits in Leaves. Australian Journal of Biological Sciences. 15, 413 - 428.
http://dx.doi.org/10.1071/BI9620413.
Bates, L.S., Waldren, R.P. & Teare, I.D. (1973). Rapid determination of free proline for water-stress studies. Plant and Soil. 39205–207.  https://doi.org/10.1007/BF00018060
Batool, A., Taj, S., Rashid, A., Khalid, A., Qadeer, S., Saleem, A.R. & Ghufran, M.A. (2015). Potential of soil amendments (Biochar and gypsum) in increasing water use efficiency of abelmoschus esculentus L. Moench. Frontiers in Plant Science. 6, 1–13. https://doi.org/10.3389/fpls.2015.00733
Beauchamp, C. & Fridovich, I. (1971). Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels. Analals of Biochemistry. 44, 276–287. https://doi.org/10.1016/0003-2697(71)90370-8
Borchard, N., Schirrmann, M., Cayuela, M.L., Kammann, C., Wrage-Mönnig, N., Estavillo, J.M., Fuertes-Mendizábal, T., Sigua, G., Spokas, K., Ippolito, J.A. & Novak, J. (2019). Biochar, soil and land-use interactions that reduce nitrate leaching and N2O emissions: A meta-analysis. Science of The Total Environment. 651, 2354–2364. https://doi.org/10.1016/j.scitotenv.2018.10.060
Cao, Y., Luo, Q., Tian, Y. & Meng, F. (2017). Physiological and proteomic analyses of the drought stress response in Amygdalus Mira (Koehne) roots. Plant Biolology. 17, 1–16. https://doi.org/10.1186/s12870-017-1000-z
Chance, B. & Maehly, A.C. (1955). [136] Assay of catalases and peroxidases. {black small square}. Methods in Enzymology. 2, 764–775. https://doi.org/10.1016/S0076-6879(55)02300-8
Chavoushi, M., Najafi, F., Salimi, A. & Angaji, S.A. (2020). Effect of salicylic acid and sodium nitroprusside on growth parameters, photosynthetic pigments and secondary metabolites of safflower under drought stress. Scientia Horticulturae. (Amsterdam). 259. https://doi.org/10.1016/j.scienta.2019.108823
Chen, L., Liu, M., Ali, A., Zhou, Q., Zhan, S., Chen, Y., Pan, X. & Zeng, Y. (2020). Effects of Biochar on Paddy Soil Fertility Under Different Water Management Modes. Journal of Soil Science and Plant Nutrition. 20, 1810–1818. https://doi.org/10.1007/s42729-020-00252-8
Cheng, W. & Kuzyakov, Y. (2015). Root effects on soil organic matter decomposition. Roots Soil Manag. Interact. between Roots Soil. 48, 119–143. https://doi.org/10.2134/agronmonogr48.c7
Chow, P.S. & Landhäusser, S.M. (2004). A method for routine measurements of total sugar and starch content in woody plant tissues. Tree Physiology. 24, 1129–1136. https://doi.org/10.1093/treephys/24.10.1129
Dapanage, M. & Bhat, S. (2018). Physiological responses of commercial sugarcane (Saccharum spp. hybrids) varieties to moisture deficit stress tolerance. Indian Journal of Plant Physiology. 23, 40–47. https://doi.org/10.1007/s40502-017-0328-6
Dong, C.J., Liu, X.Y., Xie, L.L., Wang, L.L. & Shang, Q.M. (2020). Salicylic acid regulates adventitious root formation via competitive inhibition of the auxin conjugation enzyme CsGH3.5 in cucumber hypocotyls. Planta. 252, 1–15. https://doi.org/10.1007/s00425-020-03467-2
Darvizheh, H., Zahedi, M., Abbaszadeh, B. & Razmjoo, J. (2019). Changes in some antioxidant enzymes and physiological indices of purple coneflower (Echinacea purpurea L.) in response to water deficit and foliar application of salicylic acid and spermine under field condition. Scientia Horticulturae. (Amsterdam). 247, 390–399. https://doi.org/10.1016/j.scienta.2018.12.037
Diatta, A.A., Fike, J.H., Battaglia, M.L., Galbraith, J.M. & Baig, M.B. (2020). Effects of biochar on soil fertility and crop productivity in arid regions: a review. Arabian Journal of Geosciences. 13, 595. https://doi.org/10.1007/s12517-020-05586-2
Du, C., Shen, F., Li, Y., Zhao, Z., Xu, X., Jiang, J. & Li, J. (2021). Effects of salicylic acid, jasmonic acid and reactive oxygen species on the resistance of Solanum peruvianum to Meloidogyne incognita. Scientia Horticulturae. (Amsterdam). 275, 109649. https://doi.org/10.1016/j.scienta.2020.109649
Estaji, A. & Niknam, F. (2020). Foliar salicylic acid spraying effect’ on growth, seed oil content, and physiology of drought-stressed Silybum marianum L. plant. Agriculture and Water Management. 234, 106116. https://doi.org/10.1016/j.agwat.2020.106116
Farhangi-Abriz, S. & Torabian, S. (2017). Antioxidant enzyme and osmotic adjustment changes in bean seedlings as affected by biochar under salt stress.
Ecotoxicology and Environmental Safety.  137, 64–70. https://doi.org/10.1016/j.ecoenv.2016.11.029
Farhadi, N. & Ghassemi-Golezani, K. (2020). Physiological changes of Mentha pulegium in response to exogenous salicylic acid under salinity. Scientia Horticulturae. (Amsterdam). 267, 109325. https://doi.org/10.1016/j.scienta.2020.109325
Friedman, S.P. (2005). Soil properties influencing apparent electrical conductivity: A review. Computer and Electronic in Agriculture. 46, 45–70. https://doi.org/10.1016/j.compag.2004.11.001
Gacnik, S., Veberic, R., Marinovic, S., Halbwirth, H. & Mikulic-Petkovsek, M. (2021). Effect of pre-harvest treatments with salicylic and methyl salicylic acid on the chemical profile and activity of some phenylpropanoid pathway related enzymes in apple leaves. Scientia Horticulturae. (Amsterdam). 277, 109794. https://doi.org/10.1016/j.scienta.2020.109794
Gao, S., Wang, Y., Yu, S., Huang, Y., Liu, H., Chen, W. & He, X. (2020). Effects of drought stress on growth, physiology and secondary metabolites of Two Adonis species in Northeast China. Scientia Horticulturae. (Amsterdam). 259, 108795. https://doi.org/10.1016/j.scienta.2019.108795
Ghaffari, H., Tadayon, M.R., Nadeem, M., Cheema, M. & Razmjoo, J. (2019). Proline-mediated changes in antioxidant enzymatic activities and the physiology of sugar beet under drought stress. Acta Physiologiae Plantarum. 41, 23. https://doi.org/10.1007/s11738-019-2815-z
Ghassemi-Golezani, K. & Farhangi-Abriz, S. (2018). Changes in Oil Accumulation and Fatty Acid Composition of Soybean Seeds under Salt Stress in Response to Salicylic Acid and Jasmonic Acid. Russian Journal of  Plant Physiology. 65, 229–236. https://doi.org/10.1134/S1021443718020115
Ghassemi, S., Ghassemi-Golezani, K. & Salmasi, S.Z. (2019). Changes in antioxidant enzymes activities and physiological traits of ajowan in response to water stress and hormonal application. Scientia Horticulturae. (Amsterdam). 246, 957–964. https://doi.org/10.1016/j.scienta.2018.11.086
Gorni, P.H., Pacheco, A.C., Moro, A.L., Silva, J.F.A., Moreli, R.R., de Miranda, G.R., Pelegrini, J.M., Spera, K.D., Bronzel, J.L. & da Silva, R.M.G. (2020). Salicylic acid foliar application increases biomass, nutrient assimilation, primary metabolites and essential oil content in Achillea millefolium L. Scientia Horticulturae. (Amsterdam). 270, 109436. https://doi.org/10.1016/j.scienta.2020.109436
Gong Z, Li P, Guo S, Jing X, Wang X, Zhang H. (2001).Bioslurry remediation of soil contaminated with polycyclic aromatic hydrocarbons. Sep;22(5):112-6. Chinese. PMID: 11769215.
Guo, L., Bornø, M.L., Niu, W. & Liu, F. (2021). Biochar amendment improves shoot biomass of tomato seedlings and sustains water relations and leaf gas exchange rates under different irrigation and nitrogen regimes. Agriculture and Water Management. 245. https://doi.org/10.1016/j.agwat.2020.106580
Han, M., Sun, L., Gan, D., Fu, L. & Zhu, B. (2020). Root functional traits are key determinants of the rhizosphere effect on soil organic matter decomposition across 14 temperate hardwood species. Soil Biology and Biochemistry. 151, 108019. https://doi.org/10.1016/j.soilbio.2020.108019
Hossain, M.Z., Bahar, M.M., Sarkar, B., Donne, S.W., Ok, Y.S., Palansooriya, K.N., Kirkham, M.B., Chowdhury, S. & Bolan, N. (2020). Biochar and its importance on nutrient dynamics in soil and plant, Biochar. 2, 379-420. https://doi.org/10.1007/s42773-020-00065-z
Huang, L., Li, M., Zhou, K., Sun, T., Hu, L., Li, C. & Ma, F. (2018). Uptake and metabolism of ammonium and nitrate in response to drought stress in Malus prunifolia. Plant Physiology and Biochemistry. 127, 185–193. https://doi.org/10.1016/j.plaphy.2018.03.031
Huang, Y.T., Cai, S.Y., Ruan, X.L., Chen, S.Y., Mei, G.F., Ruan, G.H. & Cao, D.D. (2021). Salicylic acid enhances sunflower seed germination under Zn2+ stress via involvement in Zn2+ metabolic balance and phytohormone interactions. Scientia Horticultura. (Amsterdam). 275, 109702. https://doi.org/10.1016/j.scienta.2020.109702
Hussain, M., Farooq, S., Hasan, W., Ul-Allah, S., Tanveer, M., Farooq, M. & Nawaz, A. (2018). Drought stress in sunflower: Physiological effects and its management through breeding and agronomic alternatives. Agriculture and Water Management. 201, 152–166. https://doi.org/10.1016/j.agwat.2018.01.028
Idrees, M., Khan, M.M.A., Aftab, T., Naeem, M. & Hashmi, N. (2010). Salicylic acid-induced physiological and biochemical changes in lemongrass varieties under water stress. Journal of Plant Interaction. 5, 293–303. https://doi.org/10.1080/17429145.2010.508566
Ilyas, N., Gull, R., Mazhar, R., Saeed, M., Kanwal, S., Shabir, S. & Bibi, F. (2017). Influence of Salicylic Acid and Jasmonic Acid on Wheat Under Drought Stress. Communication in Soil Science and Plant Analysis. 48, 2715–2723. https://doi.org/10.1080/00103624.2017.1418370
Jovanovic, N., Pereira, L.S., Paredes, P., Pôças, I., Cantore, V. &Todorovic, M. (2020). A review of strategies, methods and technologies to reduce non-beneficial consumptive water use on farms considering the FAO56 methods. Agriculture and Water Management. 239, 106267. https://doi.org/10.1016/j.agwat.2020.106267
Kadioglu, A., Saruhan, N., Sağlam, A., Terzi, R., Acet, T., 2011. Exogenous Salicylic acid alleviates effects of long term drought stress and delays leaf rolling by inducing antioxidant system. Plant Growth Regulation. 64, 27–37. https://doi.org/10.1007/s10725-010-9532-3v
Karimi, A., Moezzi, A., Chorom, M. & Enayatizamir, N. (2020). Application of Biochar Changed the Status of Nutrients and Biological Activity in a Calcareous Soil. Journal of Soil Science and Plant Nutrition. 20, 450–459. https://doi.org/10.1007/s42729-019-00129-5
Karimi, E., Oskoueian, E., Karimi, A., Noura, R. & Ebrahimi, M. (2018). Borago officinalis L. flower: a comprehensive study on bioactive compounds and its health-promoting properties. Journal of Food Measurement and Characterization. 12, 826–838. https://doi.org/10.1007/s11694-017-9697-9
Kambo, H.S. & Dutta, A. (2015). A comparative review of biochar and hydrochar in terms of production, physico-chemical properties and applications. Renewable and Sustainable Energy Reviews. 45, 359–378. https://doi.org/10.1016/j.rser.2015.01.050
Kordi, S., Saidi, M. & Ghanbari, F. (2013). Induction of Drought Tolerance in Sweet Basil (Ocimum basilicum L) by Salicylic Acid. International Journal of Agricultural Food Research. 2, 18–26. https://doi.org/10.24102/ijafr.v2i2.149
La, V.H., Lee, B.R., Zhang, Q., Park, S.H., Islam, M.T. & Kim, T.H. (2019). Salicylic acid improves drought-stress tolerance by regulating the redox status and proline metabolism in Brassica rapa. Horticulture, Environment and Biotechnology. 60, 31–40. https://doi.org/10.1007/s13580-018-0099-7
Lehmann, J., Rillig, M.C., Thies, J., Masiello, C.A., Hockaday, W.C. & Crowley, D. (2011). Biochar effects on soil biota - A review. Soil Biology and Biochemistry. 43, 1812–1836. https://doi.org/10.1016/j.soilbio.2011.04.022
Lorenz, K. & Lal, R. (2014). Biochar application to soil for climate change mitigation by soil organic carbon sequestration. Journal of Plant Nutrition and Soil Science. 177, 651–670. https://doi.org/10.1002/jpln.201400058
Loutfy, N., El-Tayeb, M.A., Hassanen, A.M., Moustafa, M.F.M., Sakuma, Y. & Inouhe, M. (2012). Changes in the water status and osmotic solute contents in response to drought and salicylic acid treatments in four different cultivars of wheat (Triticum aestivum). Journal of Plant Research. 125, 173–184. https://doi.org/10.1007/s10265-011-0419-9
Lugojan, C. & Ciulca, S. (2011). Evaluation of relative water content in winter wheat. Journal of Horticulture, Forestry and Biotechnol. 15(2), 173–177.
Lyu, S., Du, G., Liu, Z., Zhao, L. & Lyu, D. (2016). Effects of biochar on photosystem function and activities of protective enzymes in Pyrus ussuriensis Maxim. under drought stress. Acta Physiologiae Plantarum. 38. https://doi.org/10.1007/s11738-016-2236-1.
Malamos, N., Barouchas, P.E., Tsirogiannis, I.L., Liopa-Tsakalidi, A. & Koromilas, T.H. (2015). Estimation of monthly FAO Penman-Monteith evapotranspiration in GIS environment, through a geometry independent algorithm. Agriculture and Agricultural Science Procedia. 4, 290-299.
Rayment, G.E. & Higginson, F.R. (1992). Australian Laboratory Handbook of Soil and Water Chemical Methods. Melbourne, Inkafa Press. Australian Soil and Lab Survey Handbooks, 3.
Safahani Langeroodi, A.R., Campiglia, E., Mancinelli, R. & Radicetti, E. (2019). Can biochar improve pumpkin productivity and its physiological characteristics under reduced irrigation regimes? Scientia Horticulturae. (Amsterdam). 247, 195–204. https://doi.org/10.1016/j.scienta.2018.11.059
Shah Jahan, M., Wang, Y., Shu, S., Zhong, M., Chen, Z., Wu, J., Sun, J. & Guo, S. (2019). Exogenous salicylic acid increases the heat tolerance in Tomato (Solanum lycopersicum L) by enhancing photosynthesis efficiency and improving antioxidant defense system through scavenging of reactive oxygen species. Scientia. Horticulturae. (Amsterdam). 247, 421–429. https://doi.org/10.1016/j.scienta.2018.12.047
Shahbazi, Z., Salehi, A., Hazrati, S. & Dehnavi, M.M. (2019). Enhancing the Quality and Yield of European Borage (Borago officinalis) by Simultaneous Application of Granulated Compost, Vermicompost and Mycorrhiza. International Journal of Horticultural Science and Technology. 6, 283–298. https://doi.org/10.22059/ijhst.2019.274604.281
Shawon, R.A., Kang, B.S., Lee, S.G., Kim, S.K., Ju Lee, H., Katrich, E., Gorinstein, S. & Ku, Y.G. (2020). Influence of drought stress on bioactive compounds, antioxidant enzymes and glucosinolate contents of Chinese cabbage (Brassica rapa). Food Chemistry. 308, 125657. https://doi.org/10.1016/j.foodchem.2019.125657
Verheijen, F., Jeffery, S., Bastos, A.C., Van Der Velde, M. & Diafas, I. (2010). Biochar Application to Soils: A Critical Scientific Review of Effects on Soil Properties, Processes and Functions. European Communities Publication, pp.164.
Wang, Yanfang, Pan, F., Wang, G., Zhang, G., Wang, Yanling, Chen, X. & Mao, Z. (2014). Effects of biochar on photosynthesis and antioxidative system of Malus hupehensis Rehd. seedlings under replant conditions. Scientia Horticulturae. (Amsterdam). 175, 9–15. https://doi.org/10.1016/j.scienta.2014.05.029
Yin, H., Wheeler, E. & Phillips, R.P. (2014). Root-induced changes in nutrient cycling in forests depend on exudation rates. Soil Biology and Biochemistry. 78, 213–221. https://doi.org/10.1016/j.soilbio.2014.07.022
Zamani, S., Naderi, M.R., Soleymani, A., Nasiri, B.M., Miransari, M., 2020. Sunflower (Helianthus annuus L.) biochemical properties and seed components affected by potassium fertilization under drought conditions. Ecotoxicology and Environmental Safety. 190, 110017. https://doi.org/10.1016/j.ecoenv.2019.110017
Zhang, C., Li, X., Yan, H., Ullah, I., Zuo, Z., Li, L. & Yu, J. (2020). Effects of irrigation quantity and biochar on soil physical properties, growth characteristics, yield and quality of greenhouse tomato. Agriculture and Water Management. 241, 106263. https://doi.org/10.1016/j.agwat.2020.106263
 Zhang, X., Qu, J., Li, H., La, S., Tian, Y. & Gao, L. (2020). Biochar addition combined with daily fertigation improves overall soil quality and enhances water-fertilizer productivity of cucumber in alkaline soils of a semi-arid region. Geoderma. 363, 114170.