Plant Productions

Plant Productions

Evaluation of physiological and biochemical responses of apple (Malus domestica Borkh) rootstocks to different levels of boron

Document Type : Research Paper - Horticulture

Authors
Ghasem Hasani 1
Jamal Ahmadaali 2
Aziz Majidi 3
Mehdi Taheri 4
Ghader Ghasemi 1
Mashhid Henareh-Eshgehsou 1
1 Horticulture Crops Research Department, West Azerbaijan Agricultural and Natural Resources Research and Education Centre, AREEO, Urmia, Iran
2 Agricultural Engineering Research Department, West Azerbaijan Agricultural and Natural Resources Research and Education Centre, AREEO, Urmia, Iran
3 Soil and Water Research Department, West Azerbaijan Agricultural and Natural Resources Research and Education Centre, AREEO, Urmia, Iran
4 Soil and Water Research Department, Zanjan Agricultural and Natural Resources Research and Education Centre, AREEO, Zanjan, Iran
10.22055/ppd.2025.49459.2269
Abstract
Introduction
Boron (B) is an essential micronutrient for growth and development, distributed unevenly across plant organs, particularly in reproductive tissues. The ongoing trend of rapid climate change, characterized by global warming and decreased rainfall, has increased the risk of boron accumulation and toxicity in soils. Boron toxicity is now recognized as a major abiotic stress that negatively affects the yield and quality of agricultural products in arid and semi-arid regions. Given the potentially irreversible damage associated with boron toxicity for crop production, it is crucial to develop strategies to mitigate its adverse effects. Among these strategies, the selection of tolerant cultivars and rootstocks offers a practical and cost-effective solution. Therefore, his study aims to evaluate the performance of various apple rootstocks and local cultivars under different boron concentrations.
Materials and Methods
In this experiment, different apple rootstocks including MM106, MM111, M26, M9, M7, P22, Ottawa3, Suporter4, and Gami-Almasi local rootstock were subjected to different levels of boron stress (0, 1, 1.5, 2, and 2.5 mg.l-1) and three months after applying the treatments, different vegetative, physiological and biochemical characteristics of the bases were evaluated. In this study, boric acid was used as a source of boron stress. Vegetative characteristics including vegetative growth rate, fresh and dry weight of the aerial parts and roots were measured. Also, physiological and biochemical characteristics including chlorophyll a, b and carotenoid levels, proline, soluble carbohydrate, glycine betaine content and protein content were measured.
Results and Discussion
The results of the analysis of variance showed that the rootstock treatment, boron level, and the interaction effects of rootstock and boron level had a significant effect on the fresh and dry weights of the aerial parts and roots. The results of the mean comparison of different boron levels on the rootstocks showed that the highest fresh and dry aerial parts weights in rootstock MM106 were obtained at the boron level of 1 mg.l-1, with mean values of 611 g and 318 g, respectively. The results of the analysis of variance of chlorophyll data showed that the effects of rootstock treatment, boron, and the interaction of rootstock with boron levels on the amounts of chlorophyll a and b were significant, with this significance statistically at P ≤ 0.01. Based on the mean comparison results, the highest amount of chlorophyll a was observed in the M9 rootstock in the control treatment, although it did not differ significantly from the M26 and P22 rootstocks at the boron level of 1 mg.l-1. According to the analysis of variance results of soluble protein data, the main boron treatment had a significant effect on the amounts of soluble protein and soluble carbohydrate. In this study, with the increase in boron concentration, the soluble carbohydrate content initially increased up to a concentration of 1 mg.l-1 and then decreased at higher concentrations, but this decrease was not significant among the concentrations of 1.5, 2, and 2.5 mg.l-1 boron. According to the analysis of variance results, the interaction effect of rootstock and boron on glycine betaine content was significant. The results showed that glycine betaine content slightly increased up to the level of 1 mg.l-1, but at higher levels, the increase in glycine betaine was more pronounced. The highest glycine betaine content was obtained in the MM106 rootstock at the boron level of 2.5 mg.l-1. Based on the mean comparison chart, with the increase in boron concentration, the proline content in all rootstocks increased. However, the rate of increase in proline content was not the same across all apple rootstocks. The highest proline accumulation was observed in the Ottawa3 rootstock at the boron level of 2.5 mg.l-1.
Conclusion
The results of this study showed that varying boron concentrations significantly influence the vegetative, physiological, and biochemical traits of different apple rootstocks, with responses differing according to both rootstock type and boron concentration. A comprehensive evaluation based on these traits showed that the M26 and P22 rootstocks exhibited higher tolerance to boron toxicity compared with the other rootstocks tested. Therefore, these rootstocks can be recommended for use in cultivation programs in regions where soil boron levels exceed 2 mg. l⁻¹.
Keywords
Abiotic stress
Boron toxicity
Glycine betaine
Proline
Subjects
Ali-Ehyaee, M., & Behbahani-Zadeh, A.A. (1997). Description of soil chemical analysis methods. Soil and Water Research Institute Technical publication. 1024 (2). [In Persian].
Asghari, M.R., Ghaffari Bagtash, H., Rasmiy, Y., & Farokhzad, A.R. (2015). The interaction of post-harvest salicylic acid and nitric oxide treatments on quality retention and marketability enhancement in red delicious apples. Journal of Crop Production and Processing, 4 (13), 51-62 [in Persian].
Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1-2), 248-254.  https://doi.org/10.1016/0003-2697(76)90527-3 
Chen, M., Mishra, S., Heckathorn, S.A., Frantz, J.M., & Krause, C. (2014). Proteomic analysis of Arabidopsis thaliana leaves in response to acute boron deficiency and toxicity reveals effects on photosynthesis, carbohydrate metabolism, and protein synthesis. Journal of Plant Physiology, 171(3-4), 235-242. https://doi.org/10.1016/j.jplph.2013.07.008
Doganlar, Z.B., Demir, K., Basak, H., & Gul, I. (2010). Effects of salt stress on pigment and total soluble protein contents of three different tomato cultivars. African Journal of Agriculture Research, 5(15), 2056-2065.
Dubey, R., Gupta, D.K., & Sharma, G.K., (2020). Chemical Stress on Plants. New Frontiers in Stress Management for Durable Agriculture. Publisher Springer, PP. 101-128. https://doi.org/10.5897/AJAR10.258
El-Fekey, S.S., El-Shintinawy, F.A., & Shaker, E.M. (2014). Role of CaCl2 and salicylic acid on metabolic activities and productivity of boron stressed barley (Hordeum vulgare L.). International Journal of Current Microbiology and Applied Sciences, 3 (2): 368-380.
Eraslan, F., Polat, M., Yildirim, A., & Kucukyumuk, Z. (2016). Physiological and nutritional responses of two distinctive Quince (Cydonia oblonga Mill) rootstocks to Boron toxicity. Pakistan Journal of Botany, 48(1), 75-80.
Furlani, Â.M.C., Carvalho, C.P., Freitas, J.G.D., & Verdial, M.F. (2003). Wheat cultivar tolerance to boron deficiency and toxicity in nutrient solution. Scientia Agricola, 60, 359-370. https://doi.org/10.1590/s0103-90162003000200022 
Grieve, C. M., & Grattan, S. R. (1983). Rapid assay for determination of water-soluble quaternary ammonium compounds. Plant and Soil, 70, 303-307. https://doi.org/10.1007/BF02374789
Gunes, A., Inal, A., Bagci, E.G., Coban, S., & Sahin, O. (2007). Silicon increases boron tolerance and reduces oxidative damage of wheat grown in soil with excess boron. Biologia Plantarum, 51, 571-574. https://doi.org/10.1007/s10535-007-0125-6
Gunes, A., Soylemezoglu, G., Inal, A., Bagci, E.G., Coban, S., & Sahin, O. (2006). Antioxidant and stomatal responses of grapevine (Vitis vinifera L) to boron toxicity. Science Horticulture, 110, 279–284. https://doi.org/10.1016/j.scienta.2006.07.014
Haddad, R., & Kamangar, A. (2015). The ameliorative effect of silicon and potassium on drought stressed grape (Vitis vinifera L.) leaves. Iranian Journal of Genetics and Plant Breeding, 4(2), 48-58.
Hajebi, A.H., & Heidari-Sharifabad, H. (2005). Investigation of effect of drought on growth and nodulation of three species of clover. Pajouhesh-va-sazandegi, 13-22. Sid. https://sid.ir/paper/19927/en. [In Persian].
Hassani, G., Farrokhzad, A., Majidi, A., & Sepehr, E. (2020a). Evaluating some apple rootstocks in Boron toxicity condition using Morpho-physiological and biochemical indexes in soil. Iranian Journal of Horticultural Science. 52(1), 861-875. https://doi.org/10.22059/ijhs.2020.296200.1760 [In Persian].
Hassani, G., Majidi, A., Farrokhzad, A., & Sepehr, E. (2021b). Interactive Effect of Boron and Rootstock on the Growth, Physiological and Biochemical Characteristics Apple c.v. Golden Delicious. Seed and Plant Production Journal. 31(1).
Hsiao, T.C., & Xu, L.K. (2000). Sensitivity of growth of roots versus leaves to water stress: biophysical analysis and relation to water transport. Journal of Experimental Botany, 51, 1595-1616. https://doi.org/10.1093/jexbot/51.350.1595
Huynh, B.L., Pallotta, M., Choi, E.Y., Garnett, T., Graham, R., & Stangoulis, J. (2009). Quantitative trait loci for reducing sugar concentration in the barley root tip under boron toxicity. Bioresource Technology, 101(22), 8891-8896.
Irigoyen, J.J., Einerich, D.W., & Sánchez‐Díaz, M. (1992). Water stress induced changes in concentrations of proline and total soluble sugars in modulated alfalfa (Medicago sativa) plants. Physiologia Plantarum, 84(1), 55-60. https://doi.org/10.1111/j.1399-3054.1992.tb08764.x 
Jalili-Marandi, R., (2011). Physiology Of Environmental Stresses and Resistance Mechanisms in Garden Plants (Fruit Trees, Vegetables, Ornamental Plants and Medicinal Plants). Urmia University Academic Jihad Publications. 636. [In Persian].
Karabal, E., Yücel, M., & Öktem, H.A. (2003). Antioxidant responses of tolerant and sensitive barley cultivars to boron toxicity. Plant Science, 164(6), 925-933. https://doi.org/10.1016/s0168-9452(03)00067-0 
Kaya, C., Tuna, A.L., Dikilitas, M., Ashraf, M., Koskeroglu, S., & Guneri, M. (2009). Supplementary phosphorus can alleviate boron toxicity in tomato. Scientia Horticulturae, 121(3), 284-288. https://doi.org/10.1016/j.scienta.2009.02.011 
Keles, Y., & Öncel, I. (2004). Growth and solute composition in two wheat species experiencing combined influence of stress conditions. Russian Journal of Plant Physiology, 51, 203-209. https://doi.org/10.1023/b:rupp.0000019215.20500.6e 
Koutinase, N. (2013). Respone of the apple rootstocks M9, M26 and MM106 to Boron toxicity. Acta Horticulturae, 981, 471-474.
Lambers, H., Chapin, F.S., & Pons, T.L. (1998). Role in Ecosystem and Global Processes. In: Plant Physiological Ecology. Springer, New York. https://doi.org/10.1007/978-1-4757-2855-2_10
Lee, D.H., Kim, Y.S., & Lee, C.B. (2001). The inductive responses of the antioxidant enzymes by salt stress in the rice (Oryza sa­tiva L.). Journal of Plant Physiology, 158, 737-745. https://doi.org/10.1078/0176-1617-00174 
Lichtenthaler, H. K, (1987). Chlorophylls and carotenoids: pigments of photosynthetic membranes. Methods Enzymology, 148, 350-383.
Macho-Rivero, M.A., Herrera-Rodríguez, M.B., Brejcha, R., Schäffner, A.R., Tanaka, N., Fujiwara, T., González-Fontes, A., & Camacho-Cristóbal, J.J. (2018). Boron toxicity reduces water transport from root to shoot in Arabidopsis plants. Evidence for a reduced transpiration rate and expression of major PIP aquaporin genes. Plant and Cell Physiology, 59(4), 841-849. https://doi.org/10.1093/pcp/pcy026 
Majidi, A., & Malakouti, M.J., (2008). Boron toxicity in Urmia Lake around Orchards. Sana Publication. [In Persian].
Molassiotis, A., Sotiropolos, T., Tanou, G., Diamanitidis, G., &Therios, I. (2006). Boron-induced oxidative damage and antioxidant and nucleolytic responses in shoot tips culture of the apple rootstock EM 9 (Malus domestica Borkh). Environmental and Experimental Botany, 56, 54-62. https://doi.org/10.1016/j.envexpbot.2005.01.002 
Nable, R.O., Banuelos, G.S., & Paull, G. (1997). Boron toxicity. Plant and soil, 193, 181- 198.
Nezamdoost, S., Farrokhzad, A. & Rasouli-Sadaghiani, M.H. (2017). Effect of potasium silicate on reduction of boron accumulation and oxidative damages in grape (Vitis vinifera cv. Bidaneh Sefid) under boron toxicity stress. Iranian Journal of Horticultural Science, 48(2), 391-401. https://doi.org/10.22059/ijhs.2017.140928.922 [In Persian].
Oraei, M., Tabatabaei, S.J., Fallahi, E., & Imani, A. (2012). The effects of boron stress on growth, physiological   characteristics and the distribution of boron in scion-rootstock combination of almond (Prunus dulcis Mill). Journal of Horticultural Sciences, 26, 440-447. https://doi.org/10.22067/jhorts4.v0i0.18259  [In Persian].
Paparankis, A., Chatzissavvidis, C., & Antoniadis, V. (2013). How apple responds to boron excess in acidic and limed soil. Journal of Soil Sscience and Plant Nutrition, (4), 787- 796.
Paquin, R., & Lechasseur, P. (1979). Observations on a method of dosing free proline in plant extracts. Canadian Journal of Botany, 57(18), 1851-1854.
Patakas, A., Nikolaou, N., Zioziou, E., Radoglou, K., & Noitsakis, B. (2002). The role of organic solute and ion accumulation in osmotic adjustment in drought-stressed grapevines. Plant Science, 163(2), 361-367. https://doi.org/10.1016/s0168-9452(02)00140-1 
Reid, R. (2014). Understanding the boron transport network in plants. Plant and Soil, 385, 1-13. https://doi.org/10.1007/s11104-014-2149-y 
Rostami, H., Tabatabai, S.J., Zare Nahandi, F., & Hajiloo, J, (2013). Concentrations of boron (B) on the growth and phisiological characteristics of olives. Journal of Horticultural Science, 27, 26-18. https://doi.org/10.22067/jhorts4.v0i0.20781 [In Persian].
Sakamoto, A., & Murata, N. (2002). The role of glycine betaine in the protection of plants from stress: clues from transgenic. Plant Cell and Environment, 25 (2), 163-171. https://doi.org/10.1046/j.0016-8025.2001.00790.x 
Saleem, M., Yusop, M.K., Ishak, F., Samsuri, A.W., & Hafeez, B. (2011). Boron fertilizers borax and colemanite application on rice and their residual effect on the following crop cycle. Soil Science and Plant Nutrition, 57(3), 403-410. https://doi.org/10.1080/00380768.2011.582589
Sarabandi, M., Farrokhzad, A., Abdulahi, B. & Ghasim-zadeh, R. (2019). The effect of methyl jasmonate foliar application on some vegetative indicators of two grape varieties under boron toxicity conditions. P. 1-9. Second International Conference on Medicinal Plants, Organic Agriculture. 13 March 2019, Mashhad, Iran. [In Persian].
Schobert, B. (1977). Is there an osmotic regulatory mechanism in algae and higher plants? Journal of Theoretical Biology, 68(1), 17-26. https://doi.org/10.1016/0022-5193(77)90224-7
Sotiropoulos, T.E., Fotopoulos, S., Dimassi, K.N., Tsirakoglou, V., & Therios, I.N. (2006). Response of the pear rootstock to boron and salinity in vitro. Biologia Plantarum, 50, 779-781. https://doi.org/10.1007/s10535-006-0130-1
Tanaka, M., & Fujiwara, T. (2008). Physiological roles and transport mechanisms of boron: perspectives from plants. Pflügers Archiv-European Journal of Physiology, 456(4), 671-677. https://doi.org/10.1007/s00424-007-0370-8
Tariq, M., & Mott, C.J.B. (2007). The Significance of Boron in Plant Nutrition and Environment-A Review. Journal of Agronomy, 6(1), 1–10. https://doi.org/10.3923/ja.2007.1.10.
Wang, J.Z., Tao, S.T., Qi, K.J., Wu, J., Wu, H.Q., & Zhang, S.L. (2011). Changes in photosynthetic properties and antioxidative system of pear leaves to boron toxicity. African Journal of Biotechnology. 10(85), 19693- 19700. https://doi.org/10.5897/AJB11.2608
Wolf, B. (1974). Improvement in the azomethine-H method for the determination of boron. Communication in Soil Science and Plant Analysis, 5: 39-44.  https://doi.org/10.1080/00103627409366478
Xiong, L., & Zhu, J.K. (2002). Molecular and genetic aspects of plant responses to osmotic stress. Plant, Cell and Environment, 25(2), 131-139. https://doi.org/10.1046/j.1365-3040.2002.00782.x
Yau, S.K., & Ryan, J. (2008). Boron toxicity tolerance in crops: a viable alternative to soil Amelioration. Crop Sciences. 48(3), 854- 865. https://doi.org/10.2135/cropsci2007.10.0539 
Plant Productions
Volume 49, Issue 1
Spring 2026
Pages 137-156