The effects of humic acid and chelate applications on some morphophysiological properties and antioxidant enzyme activities of ornamental cabbage (Brassica oleracea var. acephala) under boron stress

Year 2022, , 85 - 95, 13.12.2022

Şenel Birceyudum Eman Gökseven Sevinç Kıran Ş. Şebnem Ellialtıoğlu

https://doi.org/10.21657/soilst.1218454

Abstract

The increase of industrialization, the overuse chemical fertilisers and mining activities are brought about heavy metal-led environment pollution, especially agricultural land. This leads to more boron (B) contamination and accumulation in the soil. This study was carried out to evaluate B uptake from the soil of ornamental cabbage grown as a hyperaccumulator plant under B stress conditions in a controlled greenhouse on plant morphology, physiology, antioxidant enzyme activity the effects of humic acid (50mg kg-1 B + 2% humic acid -HA) and chelate [0.5 g kg-1 chelate (EDTA)] applications. According to the results, especially chelate application significantly increased the B uptake of the plant, and B accumulation was higher in the plant shoot than in the root. However, HA and chelate applications brought out the negative effects of B stress on growth and physiological characteristics and reinforced the increases in malondialdehyde (MDA) content and superoxide dismutase (SOD) and catalase (CAT) enzyme activities. In conclusion, this study shows that HA and chelate additions increase the efficiency of the use of ornamental cabbage to remove excess boron from the soil. According to these results, it is possible to increase the use of ornamental cabbage for phytoremediation purposes, especially with chelate application.

Keywords

Boron toxicity, Brassica oleracea var. acephala, EDTA, phytoremediation, superoxide dismutase

References

• Abbas, M.H.H., & Abdelhafez, A.A. (2013). Role of EDTA in arsenic mobilization and its uptake by maize grown on an As-polluted soil. Chemosphere, 90, 588-594. https://doi.org/10.1016/j.chemosphere.2012.08.042
• Ameri, A., & Tehranifar, A. (2012). Effect of humic acid on nutrient uptake and physiological characteristic Fragaria ananassa var: Camarosa. Acta Horticulturae 6: 77-79. https://doi.org/10.17660/ActaHortic.2014.1049.54
• Angin, I., Turan, M., Ketterings, Q.M., & Cakici, A. (2008). Humic acid addition enhances B and Pb phytoexctraction by Vetiver grass (Vetiveria zizanioides L. Nash). Water Air Soil Pollution, 188, 335-343. https://doi.org/10.1007/s11270-007-9548-0
• Ardıç, M. (2006). Bor toksisitesinin nohut (Cicer arietinum L.) bitkisinde bazi fizyolojik ve biyokimyasal özellikler üzerindeki etkileri. Eskişehir Osmangazi Üniversitesi Fen Bilimleri Enstitüsü, Biyoloji Anabilim Dalı, Doktora Tezi, 83 sy.
• Arshad, M., Naqvi, N., Gul, I., Yaqoob, K., Bilal, M., & Kallerhoff, J. (2020). Lead phytoextraction by Pelargonium hortorum: Comparative assessment of EDTA and DIPA for Pb mobility and toxicity. Science of The Total Environment, 748:141496. https://doi.org/10.1016/j.scitotenv.2020.141496
• Ayvaz, M. (2009). Aşırı bor uygulamasinin patateste (Solanum tuberosum L.) enzimatik aktivite değişimleri ile protein ve oksin içerikleri üzerine etkileri. Ege Üniversitesi Fen Bilimleri Enstitüsü, Biyoloji Anabilim Dalı, Doktora Tezi, 86 s.
• Barışık Kayın, G. (2020). Nitrik oksit uygulamasinin biber bitkisinde (Capsicum annuum L.) kimi stres faktörleri üzerine etkisi. Bursa Uludağ Üniversitesi, Fen Bilimleri Enstitüsü Toprak Bilimi ve Bitki Besleme Anabilim Dalı, Doktora Tezi, 215 s.
• Canal, S.B., Bozkurt, M.A., & Yilmaz, H. (2022). Effects of humic acid and EDTA on phytoremediation, growth and antioxidant activity in rapeseed (Brassica napus L.) grown under heavy metal stress. Polish Journal of Environmental Studies, 31(5): 1-10. https://doi.org/10.15244/pjoes/148120
• Cervilla, L.M., Blasco, B.A., 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.org/10.1093/aob/mcm156
• Chen, Y., Shen, Z., & Li, X. (2004). The use of Vetiver grass (Vetiveria zizanioides) in the phytoremediation of soil contaminated with heavy metals. Applied Geochemistry 19:1553-1565. https://doi.org/10.1016/j.apgeochem.2004.02.003
• Dhanda, S., & Sethi, G. (1998). Inheritance of excised-leaf water loss and relative water content in bread wheat (Triticum aestivum). Euphytica, 104:39–47. https://doi.org/10.1023/A:1018644113378
• Eman Gökseven, Ş.B., & Kıran, S. (2021). Abiyotik stres faktörleri etkisinin azaltılmasında fitoremediasyon uygulamaları. Ş.Ş. Ellialtıoğlu, H.Y. Daşgan, & Ş. Kuşvuran (Eds.), Sebzelerde Stres Toleransı ve Islah Stratejileri (pp. 493-531). Gece Kitaplığı Yayınevi, Ankara.
• Eren, A. (2019a). Phytoextraction of Nickel contaminated soil with citric acid and humic acid treatments using rosemary (Rosmarinus officinalis) plant. International Journal of Environmental Sciences & Natural Resources, 19(4): 89-94. https://doi.org/10.19080/IJESNR.2019.19.556016
• Eren, A. (2019b). Use of rosemary (Rosmarinus officinalis) plant in phytoextraction of cadmium contaminated soil through citric acid and humic acid treatments. International Conference on Agriculture, Animal Science and Rural Development-III, 1013-1028.
• Esringü, A. (2012). Toprakta kurşun (Pb), kadmiyum (Cd) ve bor (B) elementlerinin şelatör desteğiyle kolza (Brassica napus L.) bitkisi kullanilarak fitoremediasyon yöntemiyle giderilmesi. Atatürk Üniversitesi, Fen Bilimleri Enstitüsü, Toprak Bilimi ve Bitki Besleme Anabilim Dalı, Doktora Tezi, 142 s.
• Ferrara, G., & Brunetti, G. (2008) Influence of foliar applications of humic acids on yield and fruit quality of table grape cv. Italia. Journal International des Sciences de la Vigne et du Vin ,42:79–87. https://doi.org/10.20870/oeno-one.2008.42.2.822
• Freed, R., Einensmith, S.P., Guets, S., Reicosky, D., Smail, V.W. & Wolberg, P. (1989). User’s guide to MSTAT-C, an analysis of agronomic research experiment. Michigan State University, USA.
• García-Sánchez, F., Simón-Grao, S., Martínez-Nicolás, J.J., Alfosea-Simón, M., Liu, M.C., Chatzissavvidis, C., Perez-Perez, J.G., & Cámara-Zapata, J.M. (2020). Multiple stresses occurring with boron toxicity and deficiency in plants. Journal of Hazardous Materials,. 397: 122713, https://doi.org/10.1016/j.jhazmat.2020.122713
• Giansoldati, V., Tassi, E., Morelli, E., Gabellieri, E., Pedron, F., & Barbafieri, M. (2012). Nitrogen fertilizer improves boron phytoextraction by Brassica juncea grown in contaminated sediments and alleviates plant stress. Chemosphere, 87: 119-1125. https://doi.org/10.1016/j.chemosphere.2012.02.005
• Göker, M. (2019). Topraklarda krom ağir metalinin mısır (Zea mays L.) bitkisi kullanılarak fitoremediasyon tekniği ile giderilmesi. Tekirdağ Namık Kemal Üniversitesi, Fen Bilimleri Enstitüsü, Toprak Bilimi ve Bitki Besleme Anabilim Dalı, Yüksek Lisans Tezi, 61 sy.
• Güllüce, M., Agar, G., Şahin, F., Turan, M., Güneş, A., Demirtaş, A., Esringü, A., Karaman, M.R., Tutar, A., & Dizman, M. (2012). Pb ve Cd ile kirletilmiş alanlarda yetiştirilen turp bitkisinin verim parametreleri üzerine humik asit ve PGPR uygulamalarinin etkilerinin belirlenmesi. Sakarya Üniversitesi Fen Edebiyat Dergisi, 1: 509-517.
• Güneş, A., Soylemezoğlu, G., Inal, A., Bagci, E.G., Coban, S., & Sahin, O. (2006). Antioxidant and stomatal responses of grapevine (Vitis vinifera L.) to boron toxicity. Scientia Horticulturae, 110:279-284. https://doi.org/10.1016/j.scienta.2006.07.014
• Habiba, U., Ali, S., Farid, M., Shakoor, M.B., Rizwan, M., Ibrahim, M., Abbasi, G.H., Hayat, T., & Ali, B. (2015). EDTA enhanced plant growth, antioxidant defence system, and phytoextraction of copper by Brassica napus L. Environment Science and Pollution Research, 22(2):1534-1544. https://doi.org/ 10.1007/s11356-014-3431-5
• Haghighi, M., Kafi, M., & Fang, P. (2012). Photosynthetic activity and N metabolism of lettuce as affected by humic acid. International Journal of Vegetable Science, 18:182-189. https://doi.org/10.1080/19315260.2011.605826
• Haghighi, M., Kafi, M., Pessarakli, M., Sheibanirad, A., & Sharifinia, M.R. (2016). Using kale (Brassica oleracea var. acephala) as a phytoremediation plant species for lead (Pb) and cadmium (Cd) removal in saline soils. Journal of Plant Nutrition, 39 (10): 1460-1471. https://doi.org/10.1080/01904167.2016.1161768.
• 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, 176:143-153. https://doi.org/10.1016/j.plantsci.2008.10.004
• Hussain, S., Zhang, J.H., Zhong, C., Zhu, L.F., Cao, X.C., Yu, S.M., & Jin, Q.Y. (2017). Effects of salt stress on rice growth, development characteristics and the regulating ways: A review. Journal of Integrative Agriculture, 16: 2357–2374. https://doi.org/10.1016/S2095-3119(16)61608-8
• Jebara, S., Jebara, M., Limam, F., & Aouani, M.E. (2005). Changes in ascorbate peroxidase, catalase, guaiacol peroxidase and superoxide dismutase activities in common bean (Phaseolus vulgaris) nodules under salt stress. Journal of Plant Physiology, 162(8): 929-936. https://doi.org/10.1016/j.jplph.2004.10.005.
• Kacar, B., & İnal, A. (2008). Bitki Analizleri. Nobel Yayıncılık, No: 1241.
• Kaptan, M.A. (2013). Pamukta (Gossypium hirsutum L.) bor toksisitesi ve humik madde uygulamasinin etkileri. Adnan Menderes Üniversitesi, Fen Bilimleri Enstitüsü, Toprak Bilimi ve Bitki Besleme Anabilim Dalı, Doktora Tezi, 191 s.
• 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
• Karabulut, B. (2020). Fitoremediasyon yöntemi ile kurşun akümülasyonunun giderimi: Biberiye (Rosmarinus officinalis) örneği. Tekirdağ Namık Kemal Üniversitesi, Fen Bilimleri Enstitüsü, Toprak Bilimi ve Bitki Besleme Anabilim Dalı, Yüksek Lisans Tezi, 94 s.
• Karaman, M. R., Turan, M., Horuz, A., Tüfenkçi, M. Ş. & Adiloğlu, A. (2017). Interactive Effects of Boron and Humic Acid on the Growth and Nutrient Status of Maize Plant (Zea mays L.). International Journal of Plant & Soil Science, 19(2): 1-9.
• Kıran, S., Özkay, F., Kuşvuran, Ş., & Ellialtıoğlu, Ş. (2014). The effect of humic acid applications on some morphological, physiological and biochemical characteristics of eggplants irrigated with water contained heavy metals in high concentration. Turkish Journal of Agriculture - Food Science and Technology, 2(6): 280-288. https://doi.org/10.24925/turjaf.v2i6.280-288.158
• Kobayashi, M., & Matoh, T. (2004). Boron nutrition of cultured tobacco BX-2 Cells. IV. genes induced under low B supply. Journal of Experimental Botany, 55:1441–1443. https://doi.org/10.1093/jxb/erh142
• Konkolewska, A., Piechalak, A., Ciszewska, L., Antos-Krzemińska, N., Skrzypczak, T., Hanć, A., Sitko, K., Małkowski, E., Barałkiewicz, D., & Małecka, A. (2020). Combined use of companion planting and PGPR for the assisted phytoextraction of trace metals (Zn, Pb, Cd). Environmental Science and Pollution Research, 27:13809-13825. https://doi.org/10.1007/s11356-020-07885-3
• Kusznierewicz, B., Baczek-Kwinta, R., Batoszek, A., Piekarska, A., Huk, A., Manikowska, A., Antonkiewicz, J., Namiesnik, J., & Konieczka, P. (2012). The dose‐dependent influence of zinc and cadmium contamination of soil on their uptake and glucosinolate content in white cabbage (Brassica oleracea var. capitata f. alba). Environmental Toxicology and Chemistry, 31 (11): 2482-2489. https://doi.org/10.1002/etc.1977.
• Landi, M., Degl’Innocenti, E., Pardossi, A., & Guidi, L. (2012). Antioxidant and photosynthetic responses in plants under boron toxicity: A review. American Journal of Agricultural and Biological Sciences, 7(3):255-270. https://doi.org/10.3844/ajabssp.2012.255.270
• Lopez, A.R. (1993). Humic acid effect on the stomata conductance and leaf abscission on apple cv. Golden delicious under tropical conditions. Acta Horticulturae, 329:254-254. https://doi.org/10.17660/ActaHortic.1993.329.58
• Lovatt, C.J., & Bates, L.M. (1984). Early effects of excess boron on photosynthesis and growth of Cucurbita pepo. Journal of Experimental Botany, 5: 297-305. https://doi.org/10.1093/jxb/35.3.297
• Lutts, S., Kinet, J.M., & Bouharmont, J. (1996). NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Annals of Botany, 78 (3): 389- 398. https://doi.org/10.1006/anbo.1996.0134
• Meers, E., Ruttens, A., Hopgood, M.J., Samson, D., & Tack, F.M.G. (2005). Comparison of EDTA and EDDS as potential soil amendments for enhanced phytoextraction of heavy metals. Chemosphere, 58: 1011–1022.https://doi.org/10.1016/j.chemosphere.2004. 09.047
• Mittler, R. (2002). Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science,7:405-410. https://doi.org/10.1016/s1360-1385(02)02312-9
• Molassiotis, A., Sotiropoulos, T., Tanou, G., Diamantidis, G., & Therios, I. (2006). Boron induced oxidative damage and antioxidant and nucleolytic responses in shoot tips culture of the apple rootstock EM9 (Malus domestica Borkh). Environmental and Experimental Botany, 56: 54-62. https://doi.org/10.1016/j.envexpbot.2005.01.002
• Ning, Z., He, L., Xiao, T., & Marton, L. (2015). High accumulation and subcellular distribution of thallium in green cabbage (Brassica oleracea L. var. capitata L.). International Journal of Phytoremediation, 17(11):1097-104. https://doi.org/10.1080/15226514. 2015.1045133.
• Olaniya, M.S., Sur, M.S., Bhide, A.D., & Swarnakar, S.N. (1998). Heavy metal pollution of agricultural soil and vegetation due to application of municipal solid waste-A case study. Indian Journal of Environmental Health, 4: 160-168.
• Onbaşı, S. (2017). Bor toksisitesi koşullarinda uygulanan nitrik oksidin bora farkli tepki gösteren arpa genotiplerinin gelişimi üzerine etkisi. Selçuk Üniversitesi, Fen Bilimleri Enstitüsü, Toprak Bilimi ve Bitki Besleme Anabilim Dalı, Yüksek Lisans Tezi, 76 s
• Özkay, F., Kıran, S., Kuşvuran, Ş., & Ellialtıoğlu, Ş.Ş. (2016). Hümik asit uygulamasının kıvırcık salata bitkisinde ağır metal stresi zararını azaltma etkisi. Türk Tarım-Gıda Bilim ve Teknoloji Dergisi, 4(6):431-437. https://doi.org/10.24925/turjaf.v4i6.431-437.542
• Pandey, N., & Archana, (2013). Antioxidant responses and water status Brassica seedlings subjected to boron stress. Acta Physiologiae Plantarum, 35:697-706. https://doi.org/10.1007/s11738-012-1110-z
• Papadakis, I.E., Dimassi, N., Bosabalidis, A.M., Therios, I.N., Patakas, A., & Giannakoula, A. (2004). Boron toxicity in ‘Clementine’ mandarin plants grafted on two rootstocks. Plant Science, 166, 539-547. https://doi.org/10.1016/j.plantsci.2003.10.027
• Pereira, W.E., de Siqueira, D.L., Martinez, C.A., & Puiatti, M. (2000). Gas exchange and chlorophyll fluorescence in four citrus rootstocks under aluminium stress. Journal of Plant Physiology, 157: 513-520. https://doi.org/10.1016/S0176-1617(00)80106-6
• 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, in: Plant Metal Interaction-Emerging Remediation https://doi.org/10.1016/B978-0-12-803158-2.00005-9
• Rahnama, H., & Ebrahimzadeh, H. (2005). The effect of NaCl on antioxidant enzyme activities in potato seedlings. Biologia Plantarum, 49: 93-97. https://doi.org/10.1007/s10535-005-3097-4
• Sairam, R.K., & Saxena, D.C. (2000). Oxidative stress and antioxidants in wheat genotypes: possible mechanism of water stress tolerance. Journal of Agronomy and Crop Science, 184(1): 55-61. https://doi.org/10.1046/j.1439-037x.2000.00358.x
• Saffari, V.R., & Saffari, M. (2020). Effects of EDTA, citric acid, and tartaric acid application on growth, phytoremediation potential, and antioxidant response of Calendula officinalis L. in a cadmium-spiked calcareous soil. International Journal of Phytoremediation, 22(11): 1204-1214. https://doi.org/10.1080/15226514.2020. 1754758
• Shehata, S.M., Badawy, R.K., & Aboulsoud, Y.I.E. (2019). Phytoremediation of some heavy metals in contaminated soil. Bulletin of the National Research Centre, 43: 189. https://doi.org/10.1186/s42269-019-0214-7
• Sotiropoulos, T.E., Molassiotis, A., Almaliotis, D., Mouhtaridou, G., Dimassi, K., Therios, I., & Diamantidis, G. (2006). Growth, nutritional status, chlorophyll content, and antioxidant responses of the apple rootstock MM111 shoots cultured under high boron concentrations In Vitro. Journal of Plant Nutrition, 29(3): 575-583. https://doi.org/10.1080/01904160500526956
• Stiles, A.R., Liu, C., Kayama, Y., Wong, J., Doner, H., Funston, R., & Terry, N. (2011). Evaluation of the boron tolerant grass, Pucccinellia distans, as an initial vegetative cover for the phytorestoration of a boron-contaminated mining site in southern California. Environment Science and Technology, 45(20):8922-8927. https://doi.org/10.1021/es200879a
• Tursun, T. (2014). Hümik asidin borlu topraklarda yetiştirilen maydanozlarda (Petroselinum sativum Hoffm.) büyüme ve gelişme parametreleri üzerindeki etkisinin incelenmesi. Marmara Üniversitesi, Fen Bilimleri Enstitüsü, Fen Bilimleri Dalı Biyoloji Programı, Yüksek Lisans Tezi, 68 s.
• Vanlı, Ö. (2007). Pb, Cd, B elementlerinin topraklardan şelat destekli fitoremediasyon yöntemiyle giderilmesi. İstanbul Teknik Üniversitesi, Fen Bilimleri Enstitüsü, Çevre Mühendisliği Anabilim Dalı, Yüksek Lisans Tezi, 88 s.
• Varshney, P., Fariduddin, Q., & Yusuf, M. (2015). Boron induced modulation in growth, photosynthesis and antioxidant system in two varieties of Brassica juncea. International Journal of Advanced Research, 3(10): 819-832. https://doi.org/10.1016/j.sjbs.2013. 01.006
• Wang, Y., Yang, R., Zheng, J., Shen, S., & Xu, X. (2019). Exogenous foliar application of fulvic acid alleviate cadmium toxicity in lettuce (Lactuca sativa L.). Exotoxicology and Environmental Safety, 167:10-19. https://doi.org/10.1016/j.ecoenv.2018.08.064