Combined effects of excess boron and salinity on the growth and ionic imbalance of lavandin (Lavandula × intermedia) plant
Halil Samet
Department of Crop and Animal Production, Izmit Vocational School, Kocaeli University, Arslanbey Campus 41280 Kartepe, Kocaeli, Turkiyehttps://orcid.org/0000-0003-2376-7944
Yakup Çikili
Department of Soil Science and Plant Nutrition, Faculty of Agriculture, Çanakkale Onsekiz Mart University, Terzioğlu Campus 17100 Çanakkale, Turkiyehttps://orcid.org/0000-0002-0393-6248
Aysun Çavuşoğlu
Department of Plant Protection, Faculty of Agriculture, Kocaeli University, Arslanbey Campus 41280 Kartepe, Kocaeli, Turkiyehttps://orcid.org/0000-0001-6921-7097
Abstract
Generally, moderate to high salinity conditions and excess boron (B) occur together as limiting factors for plant growth in the soils of arid and semiarid regions. To determine the combined effect of excessive boron, salinity stress, or both, five different levels of B (0, 0.3, 0.6, 1.2, and 1.8 mM) and 80 mM sodium chloride (NaCl) were applied to lavandin plants grown in a greenhouse. The results showed that under nonsaline conditions, biomass production in shoots and roots and photosynthetic pigment contents (chlorophyll (Chl) a, b, and Chl a + b) decreased with exceptionally high B applications compared to the control. Moreover, the bioconcentration (BCF) of B (in shoots and roots), potassium (K) concentrations (in roots), K/sodium (Na) and calcium (Ca)/Na ratios (in shoots), and Ca/B ratios (in shoots and roots) decreased for all B applications compared to the control. In contrast, all B applications caused a remarkable increase in the carotenoid (Car)/Chl ratio, B concentrations (in shoots and roots), translocation (TF) of B, and net B accumulation compared to the control. In addition, under nonsaline conditions, concentrations of K (in shoots), Ca (in shoots and roots), and K/Na and Ca/Na ratios (in roots) were significantly increased by B applications compared with the control. Under saline conditions, significant decreases in Chl b, Chl a + b, BCF of B (in shoots and roots), and Ca/B ratio (in shoots) were observed in all B applications compared to the control. However, under saline conditions, B application caused significant increases in the Car/Chl ratio, TF of B, net B accumulation, and concentrations of B (in shoots and roots), K (in shoots), Ca, and Na (in shoots and roots) compared to the control. It was concluded that although it is not seen in the growth parameters, NaCl application could effectively alleviate the harmful effects of B toxicity in lavandin plants. Under saline conditions, notable decreases in the mean B concentration in shoots could be strong evidence for this hypothesis.
Keywords:
biomass, boron toxicity, chlorophyll, ion accumulation, Lavandula hybrida, NaCl-salinityReferences
Assaha, D.V., Ueda, A., Saneoka, H., Al-Yahyai, R., Yaish, M. W. (2017). The role of Na+ and K+ transporters in salt stress adaptation in glycophytes. Front. Physiol., 8, 509. https://doi.org/10.3389/fphys.2017.00509 DOI: https://doi.org/10.3389/fphys.2017.00509
Berntein, N., Kafkafi, U. (2002). Root growth under salinity stress. In: Plant roots: The hidden half, Waisel, Y., Eshel, A., Kafkafi, U. (eds.), 3rd ed. Marcel Dekker, New York, NY. DOI: https://doi.org/10.1201/9780203909423.ch44
Brown, P.H., Shelp, B.J. (1997). Boron mobility in plants. Plant Soil 193(1), 85–101. https://doi.org/10.1023/A:1004211925160 DOI: https://doi.org/10.1023/A:1004211925160
Burkhard, L.P., Arnot, J.A., Embry, M.R., Farley, K.J., Hoke, R.A., Kitano, M., Leslie, H.A, Lotufo, G.R., Parkerton, T.F., Sappington K.G., Tomy, G.T., Woodburn, K.B. (2012). Comparing laboratory and field measured bioaccumulation end points. Integr. Environ. Assessm. Manag., 8(1), 17–31. https://doi.org/10.1002/ieam.260 DOI: https://doi.org/10.1002/ieam.260
Carmassi, G., Romani, M., Diara, C., Massa, D., Maggini, R., Incrocci, L., Pardossi, A. (2013). Response to sodium chloride salinity and excess boron in greenhouse tomato grown in semi-closed substrate culture in a Mediterranean climate. J. Plant Nutr., 36(7), 1025–1042. https://doi.org/10.1080/01904167.2013.766209 DOI: https://doi.org/10.1080/01904167.2013.766209
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. Chem. Biol. Technol. Agric., 7(1), 1–11. https://doi.org/10.1186/s40538-019-0175-y DOI: https://doi.org/10.1186/s40538-019-0175-y
Cikili, Y., Samet, H., Dursun, S. (2016). Cadmium toxicity and its effects on growth and metal nutrient ion accumulation in Solanaceae plants. J. Agric. Sci., 22(4), 576–587. https://doi.org/10.1501/Tarimbil_0000001416 DOI: https://doi.org/10.1501/Tarimbil_0000001416
Cordovilla, M.P., Bueno, M., Aparicio, C., Urrestarazu, M. (2014). Effects of salinity and the interaction between Thymus vulgaris and Lavandula angustifolia on growth, ethylene production and essential oil contents. J. Plant Nutr., 37(6), 875–888. https://doi.org/10.1080/01904167.2013.873462 DOI: https://doi.org/10.1080/01904167.2013.873462
Eraslan, F., Inal, A., Gunes, A., Alpaslan, M. (2007). Impact of exogenous salicylic acid on the growth, antioxidant activity and physiology of carrot plants subjected to combined salinity and boron toxicity. Sci. Hortic., 113, 120–128. https://doi.org/10.1016/j.scienta.2007.03.012 DOI: https://doi.org/10.1016/j.scienta.2007.03.012
Farooq, M.A., Saqib, Z.A., Akhtar, J., Bakhat, H.F., Pasala, R.K., Dietz, K.J. (2019). Protective role of silicon (Si) against combined stress of salinity and boron (B) toxicity by improving antioxidant enzymes activity in rice. Silicon, 11(4), 2193–2197. https://doi.org/10.1007/s12633-015-9346-z DOI: https://doi.org/10.1007/s12633-015-9346-z
Franco, J.A., Bañón, S., Vicente, M.J., Miralles, J., Martínez-Sánchez, J.J. (2011a). Root development in horticultural plants grown under abiotic stress conditions – a review. J. Hortic. Sci. Biotechnol., 86(6), 543–556. https://doi.org/10.1080/14620316.2011.11512802 DOI: https://doi.org/10.1080/14620316.2011.11512802
Franco, J.A., Cros, V., Vicente, M.J., Martínez-Sánchez, J.J. (2011b). Effects of salinity on the germination, growth, and nitrate contents of purslane (Portulaca oleracea L.) cultivated under different climatic conditions. J. Hortic. Sci. Biotechnol., 86(1), 1–6. https://doi.org/10.1080/14620316.2011.11512716 DOI: https://doi.org/10.1080/14620316.2011.11512716
García‐Caparrós, P., Llanderal, A., Pestana, M., Correia, P.J., Lao, M.T. (2017). Lavandula multifida response to salinity: Growth, nutrient uptake, and physiological changes. J. Plant Nutr. Soil Sci., 180(1), 96–104. https://doi.org/10.1002/jpln.201600062 DOI: https://doi.org/10.1002/jpln.201600062
García-Sánchez, F., Simón-Grao, S., Martínez-Nicolás, J.J., Alfosea-Simón, M., Liu, C., Chatzissavvidis, C., Pérez-Pérez, J.G., Cámara-Zapata, J.M. (2020). Multiple stresses occurring with boron toxicity and deficiency in plants. J. Haz. Mat., 397, 122713. https://doi.org/10.1016/j.jhazmat.2020.122713 DOI: https://doi.org/10.1016/j.jhazmat.2020.122713
Gupta, B., Huang, B. (2014). Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Intern. J. Gen., 2014. http://dx.doi.org/10.1155/2014/701596 DOI: https://doi.org/10.1155/2014/701596
Hadi, M.R., Karimi, N. (2012). The role of calcium in plants' salt tolerance. J. Plant Nutr., 35(13), 2037–2054. https://doi.org/10.1080/01904167.2012.717158 DOI: https://doi.org/10.1080/01904167.2012.717158
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 Sci., 176(1), 143–153. https://doi.org/10.1016/ j.plantsci.2008.10.004 DOI: https://doi.org/10.1016/j.plantsci.2008.10.004
Javid, M., Ford, R., Norton, R., Nicolas, M. (2014). Sodium and boron exclusion in two Brassica juncea cultivars exposed to the combined treatments of salinity and boron at moderate alkalinity. Biologia, 69, 1157–1163. https://doi.org/10.2478/s11756-014-0412-6 DOI: https://doi.org/10.2478/s11756-014-0412-6
Ketehouli, T., Idrice Carther, K.F., Noman, M., Wang, F.W., Li, X.W., Li, H.Y. (2019). Adaptation of plants to salt stress: characterization of Na+ and K+ transporters and role of CBL gene family in regulating salt stress response. Agronomy, 9(11), 687. https://doi.org/10.3390/agronomy9110687 DOI: https://doi.org/10.3390/agronomy9110687
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 DOI: https://doi.org/10.1007/s00425-019-03220-4
Lichtenthaler, H.K. (1987). Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. Meth. Enzymol., 148, 350–382. https://doi.org/10.1016/0076-6879(87)48036-1 DOI: https://doi.org/10.1016/0076-6879(87)48036-1
Masood, S., Wimmer, M.A., Witzel, K., Zörb, C., Mühling, K.H. (2012). Interactive effects of high boron and NaCl stresses on subcellular localization of chloride and boron in wheat leaves. J. Agron. Crop Sci., 198(3), 227–235. https://doi.org/10.1111/j.1439-037X.2011.00501.x DOI: https://doi.org/10.1111/j.1439-037X.2011.00501.x
Miller, R.O. (1988). High-temperature oxidation: dry ashing. In: Handbook of reference methods for plant analysis, Kaira, Y.P. (ed.). CRC Boca Raton, 53–56.
Mohamed, A.K., Qayyum, M.F., Shahzad, A.N., Gul, M., Wakeel, A. (2016). Interactive effect of boron and salinity on growth, physiological and biochemical attributes of wheat (Triticum aestivum). Intern. J. Agric. Biol., 18, 238–244. https://doi.org/10.17957/IJAB/15.0032 DOI: https://doi.org/10.17957/IJAB/15.0032
Moradi, L., Ehsanzadeh, P. (2015). Effects of Cd on photosynthesis and growth of safflower (Carthamus tinctorius L.) genotypes. Photosynthetica, 53(4), 506–518. https://doi.org/10.1007/s11099-015-0150-1 DOI: https://doi.org/10.1007/s11099-015-0150-1
Munns, R., Tester, M. (2008). Mechanisms of salinity tolerance. Ann. Rev. Plant Biol., 59, 651–681. https://doi.org/10.1146/annurev.arplant.59.032607.092911 DOI: https://doi.org/10.1146/annurev.arplant.59.032607.092911
Özfidan-Konakçı, C., Yildiztugay, E., Elbasan, F., Yildiztugay, A., Küçüködük, M. (2020). Assessment of antioxidant system and enzyme/nonenzyme regulation related to ascorbate-glutathione cycle in ferulic acid-treated Triticum aestivum L. roots under boron toxicity. Turk. J. Bot., 44(1), 36–46. http://doi:10.3906/bot-1904-23 DOI: https://doi.org/10.3906/bot-1904-23
Pandey, A., Khan, M.K., Hakki, E.E., Gezgin, S., Hamurcu, M. (2019). Combined boron toxicity and salinity stress – An insight into its interaction in plants. Plants, 8(10), 364. https://doi.org/10.3390/plants8100364 DOI: https://doi.org/10.3390/plants8100364
Parks, J.L., Edwards, M. (2005). Boron in the environment. Critic. Rev. Environ. Sci. Technol., 35(2), 81–114. https://doi.org/10.1080/10643380590900200 DOI: https://doi.org/10.1080/10643380590900200
Samet, H., Çıkılı, Y. (2019). Response of purslane (Portulaca oleracea L.) to excess boron and salinity: Physiological approach. Russ. J. Plant Physiol., 66, 316–325. https://doi.org/10.1134/S1021443719020110 DOI: https://doi.org/10.1134/S1021443719020110
Tanaka, M., Fujiwara, T. (2008). Physiological roles and transport mechanisms of boron: perspectives from plants. Pflügers Archiv – Europ. J. Physiol., 456(4), 671–677. https://doi.org/10.1007/s00424-007-0370-8 DOI: https://doi.org/10.1007/s00424-007-0370-8
Tsiantas, P.I., Papadakis, I.E., Tsaniklidis, G., Landi, M., Psychoyou, M. (2019). Allocation pattern, nutrient partitioning, sugar metabolism, and pigment composition in hydroponically grown loquat seedlings subjected to increasing boron concentrations. J. Soil Sci. Plant Nutr., 19, 556–564. https://doi.org/10.1007/s42729-019-00054-7 DOI: https://doi.org/10.1007/s42729-019-00054-7
Van Duin, M., Peters, J.A., Kieboom, A.P., Van Bekkum, H. (1987). Synergic coordination of calcium in borate-polyhydroxycarboxylate systems. Carbohydr. Res., 162(1), 65–78. https://doi.org/10.1016/0008-6215(87)80201-X DOI: https://doi.org/10.1016/0008-6215(87)80201-X
Wang, Y., Wu, W.H. (2013). Potassium transport and signaling in higher plants. Ann. Rev. Plant Biol., 64, 451–476. https://doi.org/10.1146/annurev-arplant-050312-120153 DOI: https://doi.org/10.1146/annurev-arplant-050312-120153
Wimmer, M.A., Muhling, K.H., Lauchli, A., Brown, P.H., Goldbach, H.E. (2003). The interaction between salinity and boron toxicity affects the subcellular distribution of ions and proteins in wheat leaves. Plant Cell Environ., 26, 1267–1274. https://doi.org/10.1046/ j.0016-8025.2003.01051.x DOI: https://doi.org/10.1046/j.0016-8025.2003.01051.x
Yermiyahu, U., Ben-Gal, A., Keren, R., Reid, R.J. (2008). Combined effect of salinity and excess boron on plant growth and yield. Plant Soil, 304(1), 73–87. https://doi.org/10.1007/s11104-007-9522-z DOI: https://doi.org/10.1007/s11104-007-9522-z
Department of Crop and Animal Production, Izmit Vocational School, Kocaeli University, Arslanbey Campus 41280 Kartepe, Kocaeli, Turkiye https://orcid.org/0000-0003-2376-7944
Department of Soil Science and Plant Nutrition, Faculty of Agriculture, Çanakkale Onsekiz Mart University, Terzioğlu Campus 17100 Çanakkale, Turkiye https://orcid.org/0000-0002-0393-6248
Department of Plant Protection, Faculty of Agriculture, Kocaeli University, Arslanbey Campus 41280 Kartepe, Kocaeli, Turkiye https://orcid.org/0000-0001-6921-7097
License
This work is licensed under a Creative Commons Attribution 4.0 International License.
Articles are made available under the conditions CC BY 4.0 (until 2020 under the conditions CC BY-NC-ND 4.0).
Submission of the paper implies that it has not been published previously, that it is not under consideration for publication elsewhere.
The author signs a statement of the originality of the work, the contribution of individuals, and source of funding.
