Farklı Amerikan Asma Anaçlarında Kurşun Stresi Üzerine Salisilik Asit Uygulamalarının Etkileri

Year 2022, Volume: 36 Issue: 1, 129 - 156, 01.06.2022

Selda Daler Emine Sema Çetin Salih Seren

https://doi.org/10.20479/bursauludagziraat.948894

Abstract

Salisilik asit (SA), bitkilerde biyotik ve abiyotik stres kaynaklı birçok fizyolojik tepkiye aracılık eden önemli bir sinyal molekülüdür. Bu çalışmada, faklı konsantrasyonlarda kurşun [Pb(NO3)2] stresine maruz bırakılan 5 BB, 41 B ve 1103 P Amerikan asma anaçlarında değişen dozlardaki SA uygulamalarının morfolojik, fizyolojik ve biyokimyasal özellikler üzerine etkileri incelenmiştir. Dikimden 6 hafta sonra 0, 1.0, 2.5 ve 5.0 mM dozlardaki SA, bitkilerin tüm yeşil aksamına pülverizasyon yöntemiyle; 0, 10, 25 ve 50 ppm konsantrasyonlardaki Pb(NO3)2, bitki kök bölgesine enjeksiyon yöntemiyle uygulanmıştır. Elde edilen sonuçlar, farklı konsantrasyonlarda Pb(NO3)2 ve SA uygulamalarına yanıt olarak her üç anaçta da incelenen özellikler bakımından farklılıklar olduğunu göstermektedir. Köklenme oranı bakımından en etkili uygulamanın 5.0 mM SA konsantrasyonu olduğu belirlenirken, fiziksel zararlanma derecesi ve membran zararlanma derecesinin azaltılmasında tüm SA konsantrasyonlarının etkili olduğu tespit edilmiştir. Klorofil miktarının, 5 BB ve 1103 P anaçlarında artan SA konsantrasyonlarına paralel olarak artış gösterdiği; fenolik madde içeriğinin 5 BB ve 41 B anaçlarında 2.5 mM SA konsantrasyonunda en yüksek değere ulaştığı, prolin miktarının 5 BB anacında, 1.0 mM; 41 B anacında, 2.5 ve 5.0 mM; 1103 P anacında ise 1.0, 2.5 ve 5.0 mM SA konsantrasyonlarında azalma gösterdiği ve sürgün uzunluğunun ise 5 BB anacında, 5.0 mM SA konsantrasyonuyla en yüksek değeri aldığı belirlenmiştir. Aynı zamanda köklenme oranı ile toplam fenolik madde miktarı; fiziksel zararlanma derecesi ile klorofil miktarı ve membran zararlanma derecesi ile klorofil miktarı arasında önemli düzeyde ancak negatif yönde bir ilişki olduğu saptanmıştır. Çalışmada ekzojen SA uygulamalarının, bitkilerde Pb(NO3)2 varlığından kaynaklanan oksidatif stresi hafifletme bakımından etkili bir uygulama olduğu ve SA aktivitesinin, Amerikan asma anaçlarının türlerine bağlı olarak değişiklik gösterdiği sonucuna varılmıştır.

Keywords

Anaç, ağır metal, kurşun stresi, asma, salisilik asit

Supporting Institution

TÜBİTAK 2209-A Üniversite Öğrencileri Araştırma Projeleri Destekleme Programı (2019/2)

Project Number

1919B011904222

Thanks

Yazarlar finansal desteği için 1919B011904222 Başvuru Numaralı 2209-A Üniversite Öğrencileri Araştırma Projeleri Destekleme Programına (2019/2) teşekkür ederler.

Effects of Salicylic Acid Application on Lead Stress in Different American Grapevine Rootstocks

Abstract

Salicylic acid (SA) is an important signalling molecule that mediates many physiological responses from biotic and abiotic stress-induced in plants. In this study, the effects on morphological, physiological and biochemical properties of varying doses of SA applications in 5 BB, 41 B and 1103 P American grapevine rootstocks exposed to different concentrations of lead [Pb(NO3)2] stress were investigated. Six weeks after planting, 0, 1.0, 2.5 and 5.0 mM doses of SA were applied onto the entire green surface of the plant by the pulverisation method; 0, 10, 25 and 50 ppm concentrations of Pb(NO3)2 were applied by the injection method to the plant root zone. The results show that there were differences in the examined properties in all three rootstocks in response to Pb(NO3)2 and SA applications at different concentrations. It was determined that the most effective application in terms of rooting rate 5.0 mM SA concentration, determined that all SA concentrations effective in reducing the degree of physical damage and the degree of membrane damage. It was found that the amount of chlorophyll increased in parallel with the rising SA concentrations in 5 BB and 1103 P rootstocks; It determined that phenolic content reached the highest value at 2.5 mM SA concentration in 5 BB and 41 B rootstocks, the amount of proline decreased in SA concentrations of 1.0 mM in 5 BB rootstocks, 2.5 and 5.0 mM in 41 B rootstocks, and 1.0, 2.5 and 5.0 mM in 1103 P rootstocks. It was determined that 5.0 mM SA concentration increased shoot length in 5 BB rootstocks. Simultaneously, it was determined that there a significant but negative correlation between rooting rate with total phenolic substance content, the degree of physical damage with the amount of chlorophyll and the degree of membrane damage with the amount of chlorophyll. In the study, it was concluded that exogenous SA applications an effective application in terms of alleviating the oxidative stress caused by the presence of Pb(NO3)2 in plants, and the activity of SA varies depending on the species of American grapevine rootstocks.

Keywords

heavy metal, lead stress, salicylic acid, grapevine, rootstock

Project Number

1919B011904222

References

• Agamy, R.A., Hafez, E.E. and Tarek, H. 2013. Acquired resistant motivated by salicylic acid applicationson salt stressed tomato (Lycopersicon esculentum Mill.). American-Eurasian Journal Agriculture and Environment Science, 13: 50-57.
• Akıncı, İ.E., Akıncı, S. and Yılmaz, K. 2010. Response of tomato (Solanum lycopersicum L.) to lead toxicity: Growth, element uptake, chlorophyll and water content. African Journal of Agricultural Research, 5(6): 416- 423.
• Akpınar, A., Cansev, A. and Altınşeker Acun, D.Z. 2021. Responses of Spinacia oleracea L. cv. Matador plants to various abiotic stresses such as cadmium metal toxicity, drought and salinity. Journal of Agricultural Faculty of Bursa Uludag University, 35(1): 103-117.
• Alamer, K.H. and Fayez, K.A. 2020. Impact of salicylic acid on the growth and physiological activities of parsley plants under lead toxicity. Physiology and Molecular Biology of Plants, 26: 1361-1373.
• Alberici, A., Quattrini, E., Penati, M., Martinetti, L., Gallina, P.M., Ferrante, A. and Schiavi, M. 2007. Effect of the reduction of nutrient solution concentration on leafy vegetables quality grown in floating system. International Symposium on High Technology for Greenhouse System Management: Greensys 2007. De Pascale S ve ark. (eds). Acta Horticulturae, 801: 1167-1176.
• Amarowicz, R., Estrella, I., Hernandez, T., Robredo, S., Troszynska, A., Kosinska, A. and Pegg, R.B. 2010. Free radical-scavenging capacity, antioxidant activity, and phenolic composition of green lentil (Lens culinaris). Food Chemistry, 121(3): 705-711.
• Ananieva, E.A., Christov, K.N. and Popova, L.P. 2004. Exogenous treatment with salicylic acid leads to increased antioxidant capacity in leaves of barley plants exposed to paraquat. Journal of Plant Physiology, 161(3): 319-328.
• Anonymous 2019. Food and Agriculture Organization of the United Nations (FAO). http://www.fao.org/faostat/en/#data/QC. (Erişim tarihi: 15.05.2021).
• Ashraf, M. and Foolad, M.R. 2007. Roles of glycine betaine and proline in ımproving plant abiotic stress resistance. Environmental and Experimental Botany, 59: 206-216.
• Ashraf, M., Athar, H.R., Harris, P.J.C. and Kwon, T.R. 2008: Some prospective strategies for improving crop salt tolerance. Advances in Agronomy, 97: 45-110.
• Aydın, B. and Nalbantoğlu, B. 2011. Effects of cold and salicylic acid treatments on nitrate reductase activity in spinach leaves. Turkish Journal of Biology, 35: 443-448.
• Bates, L.S., Waldren, R.P. and Teare, I.D. 1973. Rapid determination of free proline for water-stress studies. Plant and Soil, 39: 205-207.
• Bautista, I., Boscaiu, M., Lidón, A., Llinares, J.V., Lull, C., Donat, M.P., Mayoral, O. and Vicente, O. 2016. Environmentally induced changes in antioxidant phenolic compounds levels in wild plants. Acta Physiologiae Plantarum, 38: 1-15.
• Bhattacharya, A., Sood, P. and Citovsky, V. 2010. The roles of plant phenolics in defence and communication during Agrobacterium and Rhizobium infection. Molecular Plant Pathology, 11: 705-719.
• Borsani, O., Valpuesta, V. and Botella, M.A. 2001. Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiology, 126: 1024-1030.
• Cai, H., He, M., Ma, K., Huang, Y. and Wang, Y. 2015. Salicylic acid alleviates cold-induced photosynthesis inhibition and oxidative stress in Jasminum sambac. Turkish Journal of Biology, 39: 241-247.
• Cheynier, V. 2012. Phenolic compounds: From plants to foods. Phytochemistry Reviews, 11: 153-177.
• Choudhury, S. and Panda, S.K. 2004. Role of salicylic acid in regulating cadmium induced oxidative in Oryza sativa L. roots. Bulgarian Journal of Plant Physiology, 30(3-4): 95-110.
• Ciğerli, S. 2018. Farklı Salisilik Asit Dozlarının Bazı Amerikan Asma Anaçlarının Tuzluluğa Olan Dayanımları Üzerine Etkilerinin In Vitro Koşullarda Belirlenmesi. Yüksek lisans tezi, Ordu Üniversitesi, Fen Bilimleri Enstitüsü, Bahçe Bitkileri Anabilim Dalı.
• Çelik, H. 1996. Bağcılıkta anaç kullanımı ve yetiştiricilikteki önemi. Anadolu Dergisi, 6(2): 127-48.
• Demirevska, K., Simova-Stoilova, L., Fedina, I., Georgieva, K. and Kunert, K. 2010. Response of oryzacystatin I transformed tobacco plants to drought, heat and light stress. Journal of Agronomy and Crop Science, 196: 90-99.
• Dong, C.J., Wang, X.L. and Shang, Q.M. 2011. Salicylic acid regulates sugar metabolism that confers tolerance to salinity stress in cucumber seedlings. Scientia Horticulturae, 129: 629-636.
• Dere, S. 2019. Kurşun kirliliğinin tarımsal üretime etkileri. International Journal on Mathematic, Engineering and Natural Sciences, 12: 108-118.
• Elguera, J.C.T., Barrientos, E.Y., Wrobel, K. and Wrobel, K. 2013. Effect of cadmium (Cd(II)), selenium (Se(IV)) and their mixtures on phenolic compounds and antioxidant capacity in Lepidium sativum. Acta Physiologiae Plantarum, 35: 431-441.
• El-Tayeb, M.A. 2005. Response of barley grains to the interactive effect os salinity and salicylic acid. Plant Growth Regulation, 45: 215-224.
• Fan, S. and Blake, T.J. 1994. Abscisic acid induced electrolyte leakage in woody species with contrasting ecological requirements. Physiologia Plantarum, 90(2): 414-419.
• Geravandi, M., Farshadfar, E. and Kahrizi, D. 2011. Evaluation of some physiological traits as indicators of drought tolerance in bread wheat genotypes. Russian Journal of Plant Physiology, 58(1): 69-75.
• Ghasemzadeh, A. and Jaafar, H.Z.E. 2012. Effect of salicylic acid application on biochemical changes in Ginger (Zingiber officinale Roscoe). Journal of Medicinal Plants Research, 6: 790-795.
• Gratão, P.L., Polle, A., Lea, P.J. and Azevedo, R.A. 2005. Making the life of heavy metal-stressed plants a little easier. Functional Plant Biology, 32: 481-494.
• Guo, B., Liang, Y. and Zhu, Y. 2009. Does salicylic acid regulate antioxidant defense system, cell death, cadmium uptake and partitioning to acquire cadmium tolerance in rice?. Journal of Plant Physiology, 166(1): 20-31.
• Haider, S., Kanwal, S., Uddin, F. and Azmat, R. 2006. Phytotoxicity of Pb II: changes in chlorophyll absorption spectrum due to toxic metal Pb stress on Phaseolus mungo and Lens culinaris. Pakistan Journal of Biological Sciences, 9: 2062-2068.
• Hakimi, A.B.M. and Hamada, A.M. 2011. Ascorbic acid, thiamine or salicylic acid induced changes in some physiological parameters in wheat grown under copper stress. Plant Protection Science, 47: 92-108.
• Hayat, S. and Ahmad, A. 2007. Salicylic acid: A plant hormone. Springer, United Kingdom. 400p.
• Horváth, E., Szalai, G. and Janda, T. 2007. Induction of abiotic stress tolerance by salicylic acid signaling. Journal of Plant Growth Regulation, 26: 290-300.
• Ivanova, A., Krantev, A., Stoynova, Z. and Popova, L. 2008. Cadmium induced changes in maize leaves and the protective role of salicylic acid. General and Applied Plant Physiology, 34(3-4): 149-159.
• Janda, T., Szalai, G., Tari, I. and Paldi, E. 1999. Hydroponic treatment with salicylic acid decreases the effects of chilling injury in maize (Zea mays L.) plants. Planta, 208: 175-180.
• Janda, T., Gondor, O.K., Yordanova, R., Szalai, G. and Pál, M. 2014. Salicylic acid and photosynthesis: signalling and effects. Acta Physıologiae Plantarum, 36(10): 2537-2546.
• Kadioglu, A., Saruhan, N., Saglam, A., Terzi, R. and Acet, T. 2011. Exogenous salicylic acid alleviates effects of long term drought stress and delays leaf rolling by inducing antioxidant system. Plant Growth Regulation, 63: 27-37.
• Kıran, Y. and Şahin, A. 2005. The effects of the lead on the seed germination, root growth and root tip cell mitotic divisions of lens culinaris medik. Gazi University Journal of Science, 18(1): 17-25.
• Kıran, S., Özkay, F., Kavuşturan, Ş. ve Ellialtıoğlu, Ş. 2015. Kurşunun kıvırcık salata (lactuca sativa var. Crispa) bitkisinin bazı morfolojik ve biyokimyasal özelliklerine etkisi. Iğdır Üniversitesi Fen Bilimleri Enstitüsü Dergisi, 5(1): 83-88.
• Kisa, D., Kayir, O., Saglam, N. and Sahin, S. 2019. Changes of phenolic compounds in tomato associated with the heavy metal stress. Bartın University International Journal of Natural and Applied Sciences, 2(1): 35-43.
• Kiselev, K.V., Dubrovina, A.S., Veselova, M.V., Bulgakov, V.P., Fedoreyev, S.A. and Zhuravlev, Y.N. 2007. The rol-B gene-induced over production of resveratrol in Vitis amurensis transformed cells. Journal of Biotechnology, 128(3): 681-692.
• Koç, E., Üstün, A.S., Öncel, I. ve Kaptanbaş, Y. 2013. Salisilik asitin domateste (Lycopersicon esculentum Mill.) kadmiyum stresini iyileştirici etkinliğinin bazı fizyolojik parametrelerde incelenmesi. Süleyman Demirel Üniversitesi Fen Bilimleri Enstitüsü Dergisi, 17(1): 22-28.
• Kosobrukhov, A., Knyazeva, I. and Mudrik, V. 2004. Plantago major plants responses to increase content of lead in soil: growth and photosynthesis. Journal of Plant Growth Regulation, 42: 145–151.
• Kök, D. 2012. Farklı salisilik asit dozlarının asma anaçlarının tuzluluğa dayanımı üzerine etkileri. Tekirdağ Ziraat Fakültesi Dergisi, 9(2): 32-40.
• Krantev, A., Yordonova, R., Janda, T., Szalar, G. and Popova, L. 2008. Treatment with salicylic acid decreases the effect of cadmium on photosynthesis in maize plants. Journal of Plant Physiology, 165: 920-931.
• Król, A., Amarowicz, R. and Weidner, S. 2014. Changes in the composition of phenolic compounds and antioxidant properties of grapevine roots and leaves (Vitis vinifera L.) under continuous of long-term drought stress. Acta Physiologiae Plantarum, 36: 1491-1499.
• Król, A., Amarowicz, R. and Weidner, S. 2015. The effects of cold stress on the phenolic compounds and antioxidant capacity of grapevine (Vitis vinifera L.) leaves. Journal of Plant Physiology, 189: 97-104.
• Lamhamdi, M., Bakrim, A., Aarab, A., Lafont, R. and Sayah, F., 2011. Effects of lead phytotoxicity on wheat (Triticum aestivum L.) seed germination and seedling growth. Comptes Rendus Biologies, 334(2): 118-126.
• Lamhamdi, M., El Galiou, Q., Bakrim, A., Nóvoa-Muñoz, J.C., Arias-Estévez, M., Aarab, A. and Lafont, R. 2013. Effect of lead stress on mineral content and growth of wheat (Triticum aestivum) and spinach (Spinacia oleracea) seedlings. Saudi Journal of Biological Sciences, 20(1): 29-36.
• Liu, D.H., Jiang, W.S., Wang, W., Zhao, F.M. and Lu, C. 1994. Effects of lead on root growth cell division and nucleolus of Allium cepa. Environmental Pollution, 86: 1-4.
• Maestri, E., Marmiroli, M., Visioli, G. and Marmiroli, N. 2010. Metal tolerance and hyperaccumulation: costs and trade-offs between traits and environment. Environmental and Experimental Botany, 68(1): 1-13.
• Mandal, S., Mallick, N. and Mitra, A. 2009. Salicylic acid-induced resistance to Fusarium oxysporum f. sp. lycopersici in tomato. Plant Physiology and Biochemistry, 47: 642-649.
• Materne, M.A. 1989. Genetic variability in the response of field pea varieties to soil boron. Honours thesis, University of Adelaide, Faculty of Agriculture.
• Mesmar, M.N. and Jaber, K. 1991. The toxic effect of lead on seed germination, growth, chlorophyll and protein contents of wheat and lens. Acta Biologica Hungarica, 42: 331-344.
• Metwally, A., Finkemeier, I., Georgi, M. and Dietz, K.J. 2003. Salicylic acid alleviates the cadmium toxicity in barley seedlings. Plant Physiology, 132: 272-281.
• Miranda, M.G. and Ilangovan, K., 1996. Uptake of lead by Lemna gibba L. influnce on spesific growth rate and basic biochemical changes. Bulletin of Environmental Contamination and Toxicology, 56: 1000-1007.
• Mittler, R. 2017. ROS are good. Trends in Plant Science, 22: 11-19.
• Mostofa, M.G., Fujita, M. and Tran, L.S.P. 2015. Nitric oxide mediates hydrogen peroxide-and salicylic acidinduced salt tolerance in rice (Oryza sativa L.) seedlings. Plant Growth Regulation, 77: 265–277.
• Mustafa, N.R. and Verpoorte, R. 2007. Phenolic compounds in Catharanthus roseus. Phytochemistry Reviews, 6: 243-258.
• Nriagu, J.O. 1992. Toxic Metal Pollution in Africa. Science of the Total Environment, 121: 1-37.
• Özay, C. ve Mammadov, R. 2013. Ağır Metaller ve süs bitkilerinin fitoremediasyonda kullanılabilirliği. Balıkesir Üniversitesi Fen Bilimleri Enstitüsü Dergisi, 15(1) 67-76.
• Pal, M., Szalai, G., Horvath, E., Janda, T. and Paldi, E., 2002. Effect of salicylic acid during heavy metal stress. Acta Biologica Szegediensis, 46(3-4):119-120.
• Petridis, A., Therios, I., Samouris, G., Koundouras, S. and Giannakoula, A. 2012. Effect of water deficit on leaf phenolic composition, gas exchange, oxidative damage and antioxidant activity of four Greek olive (Olea europaea L.) cultivars. Plant Physiology and Biochemistry, 60: 1-11.
• Rascio, N. and Navari-Izzo, F. 2011. Heavy metal hyperaccumulating plants: How and why do they do it? And what makes them so interesting? Plant Science, 180: 169-181.
• Raskin, I., Kumar, P.B.A.N., Dushenkov, S. and Salt, D.E. 1994. Bioconcentration of Heavy Metals by Plants. Current Opinion in Biotechnology, 5: 285-290.
• Sahar, K., Baghizadeh, A. and Taher, N.M. 2011. The Salicylic acid effect on the Salvia officianlis L. sugar, protein and proline contents under salinity (NaCl) stress. Journal of Stress Physiology and Biochemistry, 7: 80-87.
• Sannchez-Rodriguez, E., Moreno, D.A., Ferreres, F., Rubio-Wilhelmi, M.D.M. and Ruiz, J.M. 2011. Differential responses of five cherry tomato varieties to water stress: changes on phenolic metabolites and related enzymes. Phytochemistry, 72: 723-729.
• Sartor, T., Xavier, V.B., Falcao, M.A., Mondin, C.A., Dos Santos, M.A., Cassel, E., Astarita, L.V. and Santarem, E.R. 2013. Seasonal changes in phenolic compounds and in the biological activities of Baccharis dentata (Vell.) Graziela Maciel Barroso. Industrial Crops and Products, 51: 355-359.
• Saruhan, N., Saglam, A. and Kadioglu, A. 2012. Salicylic acid pretreatment induces drought tolerance and delays leaf rolling by inducing antioxidant systems in maize genotypes. Acta Physiologiae Plantarum, 34: 97- 106.
• Senaratna, T., Touchell, D., Bunns, E. and Dixon, K. 2000. Acetyl salicylic acid (aspirin) and salicylic acid induce multiple stress tolerance in bean and tomato plants. Plant Growth Regulation, 30: 157-61.
• Sengar, R.S. and Pandey, M. 1996. Inhibition of chlorophyll biosynthesis by lead in greening Pisum sativum leaf segment. Biologia Plantarum, 38: 459-462.
• Seven, T., Can, B., Darende, B.N. ve Ocak, S. 2018. Hava ve toprakta ağır metal kirliliği. Ulusal Çevre Bilimleri Araştırma Dergisi, 1(2): 91-103.
• Sharma, P. and Dubey, S. 2005. Lead toxicity in plants. Brazilian Journal of Plant Physiology, 17(1): 35-52. Shrivastav, R. 2001. Atmospheric heavy metal pollution, Resonance, 68: 62-68.
• Singh, R.P., Tripathi, R.D., Sinha, S.K., Maheshwari, R. and Srivastava, H.S. 1997. Response of higher plants to lead contaminated environment. Chemosphere, 34: 2467-2493.
• Singleton, V.L. and Rossi, J.R. 1965. Colorimetry of total phenolics with phosphomolybdic phosphotungstic acid. American Journal of Enology and Viticulture, 16: 144-158.
• Siripornadulsil, S., Traina, S., Verma, D.P.S. and Sayre, R.T. 2002. Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae. Plant Cell, 14: 2837-2847.
• Soares, C., Carvalho, M.E.A., Azevedo, R.A. and Fidalgo, F. 2019. Plants facing oxidative challenges - a little help from the antioxidant networks. Environmental and Experimental Botany, 161: 4-25.
• Şafak, N. 2011. Kara Lahana (Brassica oleracea var. Acephala) ve Pazı (Beta vulgaris var. Cicla)'da Kurşun Ve Çinko Stresinin Araştırılması. Yüksek lisans tezi, İstanbul Üniversitesi, Fen Bilimleri Enstitüsü, Biyoloji Anabilim Dalı.
• Verbruggen, N. and Hermans, C. 2008. Proline Accumulation in Plants: a review. Amino Acids, 35: 753-759. Verma, S. and Dubey, R.S. 2003. Lead toxicity induces lipid peroxidation and alters the activites of antioxidant enzymes in growing rice plants. Plant Science, 164(4): 645-655.
• Vernay, P., Gauthier-Moussard, C., Jean, L., Bordas, F., Faure, O., Ledoigt, G. and Hitmi A. 2008. Effect of chromium species on phytochemical and physiological parameters in Datura innoxia. Chemosphere, 72: 763-771.
• Vicente, M.R.S. and Plasencia, J. 2011. Salicylic acid beyond defence: its role in plant growth and development. Journal of Experimental Botany, 62(10): 3321-3338.
• Wang, L.J., Fan, L., Loescher, W., Duan, W., Liu, G.J., Cheng, J.S., Luo, H.B. and Li, S.H. 2010. Salicylic acid alleviates decreases in photosynthesis under heat stress and accelerates recovery in grapevine leaves. BMC Plant Biology, 10: 34-44.
• Waśkiewicz, A., Muzolf-Panek, M. and Goliński, P. 2013. Ecophysiology and responses of plants under salt stress: Phenolic content changes in plants under salt stress. Ed.: Parvaiz, A., Azooz, M.M., Prasad, M.N.V., Springer, New York, pp: 283-314.
• Van Assche, F. and Clijsters, H. 1990. Effects of metals on enzyme activity in plants. Plant Cell and Environment, 13: 195-206.
• Yenilmez, N. 2016. Farklı Salisilik Asit Dozlarının Bazı Amerikan Asma Anaçlarının Tuzluluğa Olan Dayanımı Üzerine Etkisi. Yüksek lisans tezi, Ordu Üniversitesi, Fen Bilimleri Enstitüsü, Bahçe Bitkileri Anabilim Dalı.
• Yerli, C., Çakmakçı, T., Şahin, Ü. ve Tüfenkçi, Ş. 2020. Ağır metallerin toprak, bitki, su ve insan sağlığına etkileri. Türk Doğa ve Fen Dergisi, 9(Özel Sayı): 103-114.
• Yuan, G., Wang, X., Guo, R. and Wang, Q. 2010. Effect of salt stress on phenolic compounds, glucosinolates, myrosinase and antioxidant activity in radish sprouts. Food Chemistry, 121: 1014-1019.
• Zanganeh, R., Jamei, R. and Rahmani, F. 2019. Modulation of growth and oxidative stress by seed priming with salicylic acid in Zea mays L. under lead stress. Journal of Plant Interactions, 14: 369-375.
• Zengin, F.K. and Munzuroğlu, Ö. 2004. Effect of lead (Pb+2) and copper (Cu+2) on the growth of root, shoot and leaf of bean (Phaseolus vulgaris L.) seedlings. Gazi University Journal of Science, 17(3): 1-10.
• Zengin, K.F. ve Munzuroğlu, Ö. 2005. Fasulye fidelerinin (Phaseolus vulgaris L. Strike) klorofil ve karotenoid miktarı üzerine bazı ağır metallerin (Ni+2, Co+2, Cr+3, Zn+2) etkileri. Fırat Üniversitesi Fen ve Mühendislik Bilimleri Dergisi, 17(1): 164-172.