Evaluation of Enzymatic and Non-enzymatic Antioxidant Defense Responses of Durum Wheat (Triticum durum Desf.) in Coping with Boron Stress

Authors

DOI:

https://doi.org/10.24925/turjaf.v12i8.1339-1351.6934

Keywords:

Antioxidant, Antiradical capacity, Boron stress, Phenolic content, ROS

Abstract

Wheat, one of the world's most important agricultural products, plays a vital role in meeting the nutritional needs of our growing global population. However, arid and semi-arid regions face a potential threat from boron (B) toxicity. While boron is an essential nutrient for plant growth and development, its excessive presence can be toxic. It disrupts physiological processes, causing chlorosis and necrosis, ultimately leading to yield loss or plant death. Although B deficiency is a problem in the soils of many countries, Türkiye is one of the few experiencing B toxicity problems in its agricultural areas. This study investigated the physiological and biochemical responses of durum wheat to various B concentrations (0-20 mg L-1) under controlled air-conditioned cabin conditions. Durum wheat exhibited a decrease in chlorophyll content, phenolic content, and antiradical capacity at B doses exceeding 10 mg L-1. However, carotene content increased steadily with increasing B concentrations. The activities of antioxidant enzymes, including superoxide dismutase (SOD), ascorbate peroxidase (APX), and glutathione S-transferase (GST), increased up to a B dose of 15 mg L-1. Catalase (CAT) and glutathione reductase (GR) activities increased up to 10 mg L-1 B dose but decreased at higher B levels. Proline content increased tenfold up to a B dose of 10 mg L-1, indicating an attempt to mitigate stress. Conversely, malondialdehyde (MDA) accumulation increased continuously (approximately 150%) with increasing B doses, suggesting membrane damage. Despite being considered B-sensitive, this study demonstrated that durum wheat can effectively cope with B stress up to a B dose of 10 mg L-1 under controlled conditions. Beyond this threshold, physiological and biochemical changes indicate a decline in stress tolerance. Many osmoregulators, carotenes, alkaloids, flavonoids, tocopherols, phenolic compounds, non-protein amino acids, and several unidentified metabolites are activated to support antioxidant defense. The SOS pathway and the released ROS force gene regulatory systems come into play. Following these, the ROS released in the organism are neutralized, and ionic homeostasis and cellular stress resistance are achieved.

References

Aamer, M., Muhammad, U. H., Li, Z., Abid, A., Su, Q et al. (2018). Foliar application of glycinebetaine (GB) alleviates the cadmium (Cd) toxicity in spinach through reducing Cd uptake and improving the activity of antioxidant system. Applied Ecology and Environmental Research 16, 7575-7583. https://doi:10.15666/aeerr

Açar, I., Doran, I., Aslan, N. & Kalkancı, N. (2016). Boron affects the yield and quality of nonirrigated pistachio (Pistacia vera L.) trees. Turkish Journal of Agriculture and Forestry 40, 664-670. https://doi.org/10.3906/tar-1511-80

Anonimous (2023a). https://www.igc.int/en/ Access: 11 August 2023

Anonimous (2023b). https://www.tarimorman.gov.tr/sgb/Belgeler/ SagMenuVeriler/TMO.pdf Access: 11 August 2023.

Ardic, M., Sekmen, A. H., Turkan, I., Tokur, S. & Ozdemir, F. (2009). The effects of boron toxicity on root antioxidant systems of two chickpea (Cicer arietinum L.) cultivars. Plant and Soil 314, 99-108. https://doi.org/10.1007/s11104-008-9709-y

Asnin, L. & Park, S. W. (2013). Isolation and analysis of bioactive compounds in Capsicum peppers. Critical Reviews in Food Science and Nutrition 55, 254-289. https://doi:10.1080/10408398.2011.652316

Avci, M, & Akar, T. (2005). Severity and spatial distribution of boron toxicity in barley cultivated areas of Central Anatolia and Transitional zones. Turkish Journal of Agriculture and Forestry 29, 377–382. https://journals.tubitak.gov.tr/agriculture/vol29/iss5/6

Balcı, G. (2021). Effects of melatonin applications on certain biochemical characteristics of strawberry seedlings in lime stress conditions. Turkish Journal of Agriculture and Forestry 45, 285-289. https://doi.org/10.3906/tar-2006-83

Beddowes, E. J., Faux, S. P. & Chipman, J. K. (2003). Chloroform, carbon tetrachloride and glutathione depletion induce secondary genotoxicity in liver cells via oxidative stress. Toxicology 187 (2–3), 101-115. https://doi.org/10.1016/S0300-483X(03)00058-1

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, 248-254. https://doi.org/10.1016/0003-2697(76)90527-3

Brand-Williams, W., Cuvelier, M. E. & Berset, C. L. W. T. (1995). Use of a free radical method to evaluate antioxidant activity. LWT-Food science and Technology, 28 (1), 25-30. https://doi.org/10.1016/S0023-6438(95)80008-5

Camacho-Cristóbal, J. J., Navarro-Gochicoa, M. T., Rexach, J., González-Fontes, A. & Herrera-Rodríguez, M. B. (2018). Plant response to boron deficiency and boron use efficiency in crop plants. Plant micronutrient use efficiency. Academic Press, Cambridge, pp 109-121. https://doi.org/10.1016/B978-0-12-812104-7.00007-1

Cervilla, L. M., Blasco, B., Rios, J. J., Romero, L. & Ruiz, J. M. (2007). Oxidative stress and antioxidants in tomato (Solanum lycopersicum) plants subjected to Boron toxicity. Annals of Botany 100, 747-756. https://doi:10.1093/aob/mcm156

Cervilla, L. M., Blasco, B., Rios, J. J., Rosales, M. A., S'anchez-Rodr'ıguez, E., Rubio-Wilhelmi, M. M., Romero, L. & Ruiz, J. M. (2012). Parameters symptomatic for boron toxicity in leaves of tomato plants. Journal of Botany, 1-17. https://doi:10.1155/2012/726206

Chen, M., Mishra, S., Heckathorn, S., Frantz, J. & 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), 235–42. https://doi:10.1016/j.jplph.2013.07.008

Choudhary, S., Zehra, A., Naeem, M., Khan, M. & Aftab, T. (2020). Effects of boron toxicity on growth, oxidative damage, antioxidant enzymes and essential oil fingerprinting in Mentha arvensis and Cymbopogon flexuosus. Chemical and Biological Technologies in Agriculture 7(1), 1–11. https://doi:10.1186/s40538-019-0175-y

Das, K. & Roychoudhury, A. (2014). Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Frontiers in Environmental Science 2, 53. https://doi:10.3389/fenvs.2014.00053

Duman, F., Aksoy, A., Aydin, Z. & Temizgul, R. (2011). Effects of exogenous glycinebetaine and trehalose on cadmium accumulation and biological responses of an aquatic plant (Lemna gibba L.). Water, Air and Soil Pollution 217, 545-556. https://doi.org/10.1007/s11270-010-0608-5

Dustgeer, Z., Seleiman, M. F., Imran, K., Chattha, M. U., Alhammad, B. A. et al. (2021). Glycine-betaine induced salinity tolerance in maize by regulating the physiological attributes, antioxidant defense system and ionic homeostasis. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 49(1), 12248. https://doi:10.15835/nbha49112248

El Sayed, H. E. A. (2011). Influence of NaCl and Na2SO4 treatments on growth development of broad bean (Vicia faba L.) plant. Journal of Life Science, 5, 513-523.

El-Shazoly, R. M., Metwally, A. A. & Hamada, A. M. (2019). Salicylic acid or thiamin increases tolerance to boron toxicity stress in wheat. Journal of Plant Nutrition 42(7), 702–22. https://doi:10.1080/01904167.2018.1549670

Eraslan, F., Inal, A., Gunes, A. & Alpaslan, M. (2007). Boron toxicity alters nitrate reductase activity, proline accumulation, membrane permeability, and mineral constituents of tomato and pepper plants. Journal of Plant Nutrition, 30(6), 981-994. https://doi.org/10.1080/15226510701373221

Farghaly, F. A., Salam, H., Hamada, A. M. & Radi, A. A. (2021). The role of benzoic acid, gallic acid and salicylic acid in protecting tomato callus cells from excessive boron stress. Scientia Horticulturae 278, 109867. https://doi:10.1016/j.scienta.2020.109867

Farooq, M. A., Saqib, Z. A. & Akhtar, J. (2015). Silicon mediated oxidative stress tolerance and genetic variability in rice (Oryza sativa L.) grown under combined stress of salinity and boron toxicity. Turkish Journal of Agriculture and Forestry 39, 718-729. https://doi.org/10.3906/tar-1410-26

Gill, S. S. & Tuteja, N. (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry 48(12), 909-30. https://doi:10.1016/j.plaphy.2010.08.016

Gunes, A., Alpaslan, M., Ozcan, H. & Cikili, Y. (2000). Tolerance to boron toxicity of maize (Zea mays L.) cultivars widely cultivated in Turkey. Turkish Journal of Agriculture and Forestry 24, 277-282. https://journals.tubitak.gov.tr/agriculture/vol24/iss2/17

Gupta, U. C., Jame, Y. W., Campbell, C. A., Leyshon, A. J. & Nicholaichuck, W. (1985). Boron toxicity and deficiency: a review. Canadian Journal of Soil Science 65, 381-409. https://doi.org/10.4141/cjss85-044

Gupta, U. C. (2007). Boron. In Handbook of plant nutrition, ed. A. V. Barker and D. J. Pilbeam, pp. 241-77. Boca Raton, Florida, USA: CRC press. https://doi.org/10.1201/9781420014877

Han, S., Tang, N., Jiang, H. X., Yang, L. T., Li, Y. & Chen, L. S. (2009). CO2 assimilation, photosystem II photochemistry, carbohydrate metabolism and antioxidant system of citrus leaves in response to boron stress. Plant Science 176(1), 143–53. https://doi:10.1016/j.plantsci.2008.10.004

Hoagland, D. R. & Arnon, D. I. (1950). The water-culture method for growing plants without soil. University of California, Berkeley: College of Agriculture, 1938, 347. http://hdl.handle.net/2027/uc2.ark:/13960/t51g1sb8j

Janero, D. R. (1990). Malondialdehyde and thiobarbituric acid-reactivity as diagnostic indices of lipid peroxidation and peroxidative tissue injury. Free Radical Biology and Medicine 9(6), 515-540. https://doi:10.1016/0891-5849(90)90131-2

Kaya, C., Sarıoğlu, A., Ashraf, M., Alyemeni, M. & Ahmad, P. (2020). Gibberellic acid-induced generation of hydrogen sulfide alleviates boron toxicity in tomato (Solanum lycopersicum L.) plants. Plant Physiology and Biochemistry 153, 53-63. https://doi:10.1016/j.plaphy.2020.04.038

Kayıhan, C., Öz, M. T., Eyidoğan, F., Yücel, M. & Öktem, H. A. (2017). Physiological, biochemical, and transcriptomic responses to boron toxicity in leaf and root tissues of contrasting wheat cultivars. Plant Molecular Biology Reporter 35(1), 97-109. https://doi:10.1007/s11105-016-1008-9

Keles, Y., Öncel, I. & Yenice, N. (2004). Relationship between boron content and antioxidant compounds in Citrus leaves taken from fields with different water source. Plant and Soil 265, 345-353. https://doi.org/10.1007/s11104-005-0646-8

Landi, M., Margaritopoulou, T., Papadakis, I. E. & Araniti, F. (2019). Boron toxicity in higher plants: an update. Planta 250, 1011-1032. https://doi.org/10.1007/s00425-019-03220-4

Lovatt, C. J. & Dugger, W. M. (1984). Boron. In: Frieden, E. (eds) Biochemistry of the essential ultratrace elements. Biochemistry of the Elements, vol 3. Springer, Boston, MA. https://doi.org/10.1007/978-1-4684-4775-0_17

Madhava, R. K. & Sresty, T. V. (2000). Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan (L.) Millspaugh) in response to Zn and Ni stresses. Plant Science 157, 113-128. https://doi.org/10.1016/S0168-9452(00)00273-9

Mahalakshmi, V., Yau, S. K., Ryan, J. & Peacock, J. M. (1995). Boron toxicity in barley (Hordeum vulgare L.) seedlings in relation to soil temperature. Plant and Soil 177, 151-156. https://doi.org/10.1007/BF00010121

Maoka, T., Mochida, K., Kozuka, M., Ito, Y., Fujiwara, Y., Hashimoto, K., Enjo, F., Ogata, M., Nobukuni, Y., Tokuda, H. et al. (2001). Cancer chemopreventive activity of carotenoids in the fruits of red paprika Capsicum annuum L. Cancer Letters 172, 103-109. https://doi:10.1016/s0304-3835(01)00635-8

Marco, F., Bitri'an, M., Carrasco, P., Rajam, M., Alc'azar, R. & Tiburcio, A. (2015). Genetic engineering strategies for abiotic stress tolerance in plants. In Plant biology and biotechnology pp. 579–609. New Delhi: Springer. https://doi:10.1007/978-81-322-2283-5_29

Mattos-Jr, D., Hippler, F. W., Boaretto, R. M., Stuchi, E. S. & Quaggio, J. A. (2017). Soil boron fertilization: The role of nutrient sources and rootstocks in citrus production. Journal of Integrative Agriculture 16(7), 1609-16. https://doi:10.1016/S2095-3119(16)61492-2

Metwally, A. M., Radi, A. A., El-Shazoly, R. M. & Hamada, A. M. (2018). The role of calcium, silicon and salicylic acid treatment in protection of canola plants against boron toxicity stress. Journal of Plant Research 131(6), 1015-28. https://doi:10.1007/s10265-018-1008-y

Miller, G., Suzuki, N., Ciftci-Yilmaz, S. & Mittler, R. O. (2010). Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, Cell and Environment 33(4), 453-67. https://doi:10.1111/j.1365-3040.2009.02041.x

Mishra, B. & Sangwan, N. (2019). Amelioration of cadmium stress in Withania somnifera by ROS management: Active participation of primary and secondary metabolism. Plant Growth Regulation 87(3), 403-412. https://doi:10.1007/s10725-019-00480-8

Misra, N. & Gupta, A. (2006). Effect of salinity and different nitrogen sources on the activity of antioxidant enzymes and indole alkoloid content in Catarantus roseus seedlings. Journal of Plant Physiology 164, 11e18. https://doi.org/10.1016/j.jplph.2005.02.011

Miwa, K., Takano, J., Omori, H., Seki, M., Shinozaki, K. & Fujiwara, T. (2007). Plants tolerant of high boron levels. Science 318(5855), 1417. https://doi.org/10.1126/science.1146634

Oboh, G., Batista, J. & Bocha, T. (2007). Polyphenols in red pepper [Capsicum annuum var. aviculare (Tepin)] and their protective effect on some pro-oxidants induced lipid peroxidation in brain and liver. European Food Research and Technology 225, 239-247. https://doi.org/10.1007/s00217-006-0410-1

Oz, M. F., Yilmaz, R., Eyidoğan, F., Graff, L. D., Yücel, M. & Oktem, H. A. (2009). Microarray analysis of late response to boron toxicity in Barley (Hordeum vulgare L.) Leaves. Turkish Journal of Agriculture and Forestry 33, 191-202. https://doi.org/10.3906/tar-0806-22

Ozturk, M., Sakcali, S., Gucel, S. & Tombuloglu, H. (2010). Boron and Plants. In: Ashraf, M., Ozturk, M., Ahmad, M. (eds) Plant Adaptation and Phytoremediation. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-9370-7_13

Papadakis, I., Tsiantas, P., Tsaniklidis, G., Landi, M., Psychoyou, M. & Fasseas, C. (2018). Changes in sugar metabolism associated to stem bark thickening partially assist young tissues of Eriobotrya japonica seedlings under boron stress. Journal of Plant Physiology 231, 337-45. https://doi:10.1016/j.jplph.2018.10.012

Papadakis, I., Tsiantas, P., Gerogiannis, O., Vemmos, S. & Psychoyou, M. (2015). Photosynthetic activity and concentration of chlorophylls, carotenoids, hydrogen peroxide and malondialdehyde in loquat seedlings growing under excess boron conditions. Acta Horticulturae 1092, 221-226. https://doi:10.17660/ActaHortic.2015.1092.33

Parks, J. L. & Edwards, M. (2005). Boron in the environment. Critical Reviews in Environmental Science and Technology 35(2), 81-114. https://doi.org/10.1080/10643380590900200

Princi, M. P., Lupini, A., Araniti, F., Longo, C., Mauceri, A., Sunseri, F. & Abenavoli, M. R. (2016). Boron toxicity and tolerance in plants: recent advances and future perspectives. Plant metal interaction. Elsevier, Amsterdam, pp 115-147. https://doi:10.1016/B978-0-12-803158-2.00005-9

Rab, A. & Haq, I. (2012). Foliar application of calcium chloride and borax influences plant growth, yield, and quality of tomato (Lycopersicon esculentum Mill.) fruit. Turkish Journal of Agriculture and Forestry 36, 695-701. https://doi.org/10.3906/tar-1112-7

Reid, R. J. & Fitzpatrick, K. L. (2009). Influence of leaf tolerance mechanisms and rain on boron toxicity in barley and wheat. Plant Physiology 151, 413-420. https://doi:10.1104/pp.109.141069

Reid, R. J. (2013). Boron toxicity and tolerance in crop plants. In N. Tuteja & S. S. Gill (Ed.), Crop improvement under adverse conditions. Springer. https://doi.org/10.1007/978-1-4614-4633-0_15

Reid, R. J., Hayes, J. E., Post, A., Stangoulis, J. C. R. & Graham, R. D. (2004). A critical analysis of the causes of boron toxicity in plants. Plant, Cell and Environment 25, 1405-1414. https://doi.org/10.1111/j.1365-3040.2004.01243.x

Risom, L., Møller, P. & Loft, S. (2005). Oxidative stress–induced DNA damage by particulate air pollution. Mutation Research 592, 119-137. https://doi:10.1016/j.mrfmmm.2005.06.012

Sarabandi, M., Farokhzad, A., Mandoulakani, B. & Ghasemzadeh, R. (2019). Biochemical and gene expression responses of two Iranian grape cultivars to foliar application of methyl jasmonate under boron toxicity conditions. Scientia Horticulturae 249, 355-63. https://doi:10.1016/j.scienta.2019.02.019

Sarafi, E., Siomos, A., Tsouvaltzis, P., Chatzissavvidis, C. & Therios, I. (2018). Boron and maturity effects on biochemical parameters and antioxidant activity of pepper (Capsicum annuum L.) cultivars. Turkish Journal of Agriculture and Forestry 42(4), 237-47. https://doi:10.3906/tar-1708-31

Sarafi, E., Siomos, A., Tsouvaltzis, P., Chatzissavvidis, C. & Therios, I. (2017). Boron toxicity effects on grafted and non-grafted pepper (Capsicum annuum) plants. Journal of Soil Science and Plant Nutrition 17(2), 441-460. https://doi:10.4067/S0718-95162017005000032

Savic, J., Römheld, V. & Nikolic, M. (2012). Oilseed rape (Brassica napus L.) genotypic variation in response to boron deficiency. Turkish Journal of Agriculture and Forestry 36, 408-414. https://doi.org/10.3906/tar-1109-43

Scalbert, A., Monties, B. & Janin, G. (1989). Tannins in wood: comparison of different estimation methods. Journal of Agriculture and Food Chemistry 37, 1324-1329. https://doi.org/10.1021/jf00089a026

Serrano, M., Zapata, P. J., Castillo, S., Guillen, F., Martinez-Romero, D. & Valero, D. (2010). Antioxidant and nutritive constituents during sweet pepper development and ripening are enhanced by nitrophenolate treatments. Food Chemistry 118, 497-503. https://doi.org/10.1016/j.foodchem.2009.05.006

Shah, A., Wu, X., Ullah, A., Fahad, S., Muhammad, R., Yan, L. & Jiang, C. (2017). Deficiency and toxicity of boron: Alterations in growth, oxidative damage and uptake by citrange orange plants. Ecotoxicology and Environmental Safety 145, 575-582. https://doi:10.1016/j.ecoenv.2017.08.003

Sharma, A., Shahzad, B., Rehman, A., Bhardwaj, R., Landi, M. & Zheng, B. (2019). Response of phenylpropanoid pathway and the role of polyphenols in plants under abiotic stress. Molecules 24(13), 2452. https://doi:10.3390/molecules24132452

Shetty, K. (2004). Role of proline-linked pentose phosphate pathway in biosynthesis of plant phenolics for functional food and environmental applications: a review. Process Biochemistry 39, 789-804. https://doi.org/10.1016/S0032-9592(03)00088-8

Soylu, S., Sade, B., Topal, A., Akgün, N., Gezgin, S., Hakkı, E. E. & Babaoğlu, M. (2005). Responses of irrigated durum and bread wheat cultivars to boron application in a low boron calcareous soil. Turkish Journal of Agriculture and Forestry 29, 275-286. https://journals.tubitak.gov.tr/agriculture/vol29/iss4/7

Stiles, A. R., Liu, C., Kayama, Y., Wong, J., Doner, H., Funston, R. & Terry, N. (2011). Evaluation of the boron tolerant grass, Puccinellia distans, as an initial vegetative cover for the phytorestoration of a boron-contaminated mining site in southern California. Environmental Science and Technology 45(20), 8922-8927. https://doi.org/10.1021/es200879a

Symes, A., Shavandi, A., Zhang, H., Mohamed-Ahmed, I., Al-Juhaimi, F. & Bekhit, A. (2018). Antioxidant activities and caffeic acid content in New Zealand asparagus (Asparagus officinalis) roots extracts. Antioxidants 7(4), 52. https://doi:10.3390/antiox7040052

Taban, S. & Erdal, I. (2000). Effects of boron on growth of various wheat varieties and distribution of boron in aerial part. Turkish Journal of Agriculture and Forestry 24, 255-262. https://journals.tubitak.gov.tr/agriculture/vol24/iss2/15

Tanaka, M. & Fujiwara, T. (2008). Physiological roles and transport mechanisms of boron: Perspectives from plants. Pflugers Archiv - European Journal of Physiology 456(4), 671-677. https://doi.org/10.1007/s00424-007-0370-8

Taşcı, R., Özercan, B., Tarhan, S., Söylemez, E., Hamarat, T., Karabak, S. & Bolat, M. (2023).TAGEM tarafından geliştirilen buğday çeşitlerinin üreticiler açısından değerlendirilmesi; Kayseri ili örneği. Ziraat Mühendisliği, (377), 4-18. https://doi.org/10.33724/zm.1259739

Temizgul, R. (2024). Antioxidant defense responses of hulled wheat varieties to the addition of sodium and potassium salts and exogenous glycine-betaine, and evaluation of the usability of these hulled wheats in the remediation of saline soils. In Preprint, available at Research Square https://doi.org/10.21203/rs.3.rs-4368507/v1

Temizgul, R., Ciftci, B., Kardes, Y. M., Kara, R., Temizgul, S., Yilmaz, S. & Kaplan, M. (2024). Comparison of different hulled wheat genotypes in terms of yield, morphological, and nutritional properties. Genetic Resources and Crop Evolution https://doi.org/10.1007/s10722-024-01994-5

Temizgul, R., Kaplan, M., Kara, R. & Yilmaz, S. (2016). Effects of salt concentrations on antioxidant enzyme activity of grain sorghum. Current Trends in Natural Sciences 5, 171-178. https://api.semanticscholar.org/CorpusID:89938550

Tepe, M. & Aydemir, T. (2011). Antioxidant responses of lentil and barley plants to boron toxicity under different nitrogen sources. African Journal of Biotechnology 10(53), 10882-10891. https://doi:10.5897/AJB10.1076

Torun, A., Yazici, A., Erdem, H. & Çakmak, I. (2006). Genotypic variation in tolerance to boron toxicity in 70 durum wheat genotypes. Turkish Journal of Agriculture and Forestry 30, 49-58. https://journals.tubitak.gov.tr/agriculture/vol30/iss1/6

Turan, M. A., Taban, S., Kayin, G. B. & Taban, N. (2018). Effect of boron application on calcium and boron concentrations in cell wall of durum (Triticum durum) and bread (Triticum aestivum) wheat. Journal of plant nutrition 41(11), 1351-1357. https://doi.org/10.1080/01904167.2018.1450424

Verbruggen, N. & Hermans, C. (2008). Proline accumulation in plants: A review. Amino Acids 35(4), 753-759. https://doi:10.1007/s00726-008-0061-6

Yalın, S. B., Orman, Ş., Hüseyin, O. K. & Özgür, A. Z. (2019). Antalya ilinde yetiştirilen kışlık ekmeklik buğdayın bor beslenme durumunun belirlenmesi. Mediterranean Agricultural Sciences 32, 157-161. https://doi.org/10.29136/mediterranean.559042

Yang, Y. & Guo, Y. (2018). Elucidating the molecular mechanisms mediating plant salt-stress responses. New Phytologist 217, 523-539. https://doi.org/10.1111/nph.14920

Yau, S. K., Nachit, M. M., Hamblin, J. & Ryan, J. (1995). Phenotypic variation in boron–toxicity tolerance at seedling stage in durum wheat (Triticum durum). Euphutica 83, 185-191. https://doi.org/10.1007/BF01678128

Yau, S. K. & Ryan, J. (2008). Boron toxicity tolerance in crops: A viable alternative to soil amelioration. Crop Science 48(3), 854-865. https://doi.org/10.2135/cropsci2007.10.0539

Yılmaz, A. M. & Tomar, O. (2022). Türkiye’de buğdayın kendi kendine yeterlilik ve ithalata bağımlılık açısından değerlendirilmesi. Avrupa Bilim ve Teknoloji Dergisi (41), 449-456. https://doi:10.31590/ejosat.1192874

Yilmaz, S., Temizgül, R., Yürürdurmaz, C. & Kaplan, M. (2020). Oxidant and antioxidant enzyme response of redbine sweet sorghum under NaCl salinity stress. Bioagro 32(1), 31-38. https://revistas.uclave.org/index.php/bioagro/article/view/2684

Yilmaz, S. H., Kaplan, M., Temizgul, R. & Yilmaz, S. (2017). Antioxidant enzyme response of sorghum plant upon exposure to Aluminum, Chromium and Lead heavy metals. Turkish Journal of Biochemistry 42(4), 503-512. https://doi.org/10.1515/tjb-2016-0112

Yüksel, F., Koyuncu, M. & Sayaslan, A. (2011). Makarnalık buğday (Triticum durum) kalitesi. Türk Bilimsel Derlemeler Dergisi, (2), 5-31.

Zainab, Q., Tanees, C., Xiongming, D., Lori, H. & Tehseen, A. (2021). Review of oxidative stress and antioxidative defense mechanisms in Gossypium hirsutum L. in response to extreme abiotic conditions. Journal of Cotton Research 4(1), 1-9. https://doi:10.1186/s42397-021-00086-4

Downloads

Published

24.08.2024

How to Cite

Temizgül, R. (2024). Evaluation of Enzymatic and Non-enzymatic Antioxidant Defense Responses of Durum Wheat (Triticum durum Desf.) in Coping with Boron Stress. Turkish Journal of Agriculture - Food Science and Technology, 12(8), 1339–1351. https://doi.org/10.24925/turjaf.v12i8.1339-1351.6934

Issue

Section

Research Paper