Salt Stress Effects Physiology Properties, Malondialdehyde and Proline Accumulation in Relation To Osmotic Adjustment Of Soybean [Glycine Max (L) Merrill]

Büşra Küçükkılııç; Öner Canavar; Hatice Kübra Gören

doi:10.18016/ksutarimdoga.vi.1699900

TR EN

Tuz Stresinin Fizyolojik Özellikler, Malondialdehit ve Prolin Birikimi Üzerindeki Etkileri ve Soya Fasulyesi [Glycine Max (L) Merrill]'Nin Ozmotik Ayarlamasi Ile İlişkisi

Öz

Bu çalışma, on adet soya (Glycine max L. Merrill) çeşidinin fide döneminden V4 (üçüncü üç yaprak düğümü) büyüme evresine kadar, üç farklı tuz konsantrasyonuna (0, 3 ve 6 dS m⁻¹) karşı morfolojik, fizyolojik ve biyokimyasal tepkilerini değerlendirmiştir. Artan tuz düzeyleri; bitki boyu, yaş ve kuru ağırlık, yaprak alanı, göreceli su içeriği, klorofil a, klorofil b, SPAD ve karotenoid miktarlarında anlamlı azalmaya yol açarken; göreceli membran geçirgenliği (RMP), prolin ve malondialdehit (MDA) düzeylerinde artışa neden olmuştur. Bu çalışma, tuz stresi ile göreceli membran geçirgenliği (RMP) arasında 0.821 düzeyinde pozitif bir korelasyon olduğunu ortaya koymuştur. Ayrıca, tüm soya çeşitlerinde artan yaprak geçirgenliği, oksidatif zarara bağlı olarak diğer ölçülen özelliklerle anlamlı düzeyde negatif korelasyonlar göstermiştir.Özellikle yüksek MDA ve düşük prolin içeriğine sahip çeşitlerin tuz stresine karşı daha az kuru madde ürettiği görülmüş; bu da oksidatif zararın ve sınırlı osmotik koruyucu birikiminin etkisini ortaya koymuştur. Bulgular, prolin birikiminin tuza dayanıklı genotiplerin belirlenmesinde ve tuzlu koşullarda ürün dayanımının artırılmasında önemli bir gösterge olduğunu göstermektedir. Ayrıca, prolin ve MDA düzeylerinin çeşitler arasında farklılık göstermesi, tuz stresine karşı genotip özgü savunma mekanizmalarının varlığını ortaya koymuştur.

Anahtar Kelimeler

Salt Stress Effects Physiology Properties, Malondialdehyde and Proline Accumulation in Relation To Osmotic Adjustment Of Soybean [Glycine Max (L) Merrill]

Abstract

This study evaluated the morphological, physiological, and biochemical responses of ten soybean (Glycine max L. Merrill) cultivars to three levels of salt stress (0, 3, and 6 dS m⁻¹) from seedling emergence to the V4 growth stage. Increasing salt concentrations significantly reduced plant height, fresh and dry weights, leaf area, relative water content, chlorophyll a, chlorophyll b, SPAD, and carotenoid levels. In contrast, relative membrane permeability (RMP), proline, and malondialdehyde (MDA) levels increased with salt stress. This study showed that there was a 0.821** positive correlation between salt stress and rmp with the increasing salt stress, besides the increasing leaf permeability significantly in the leaves of all cultivars had a negatively significant correlation relationship with other measured traits, because of oxidative membrane damage. Notably, cultivars with higher MDA and lower proline contents produced less biomass under stress, emphasizing the role of oxidative damage and limited osmoprotectant accumulation. These findings underline proline accumulation as a key indicator for selecting salt-tolerant genotypes and improving crop resilience in saline environments. Additionally, the variation in proline and MDA responses among cultivars suggests genotype-specific mechanisms of salt stress tolerance.

Keywords

Project Number

ZRF-21047

References

Acosta-Motos, J. R., Ortuño, M. F., Bernal-Vicente, A., Diaz-Vivancos, P., Sanchez-Blanco, M. J., & Hernandez, J. A. (2017). Plant responses to salt stress: Adaptive mechanisms. Agronomy, 7(1), 18. https://doi.org/10.3390/agronomy7010018.
Antoniou, C., Savvides, A., Christou, A., & Fotopoulos, V. (2016). Unravelling chemical priming machinery in plants: The role of reactive oxygen–nitrogen–sulfur species in abiotic stress tolerance enhancement. Current Opinion in Plant Biology, 33(1), 101–107. https://doi.org/10.1016/j.pbi.2016.06.020.
Arnon, D. I. (1949). Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology, 24(1), 1–15.
Barberon, M. (2017). The Endodermis as a checkpoint for nutrients. New Phytologist, 213(4), 1604–1610. https://doi.org/10.1111/nph.14140.
Bates, L., Waldren, R. P., & Teare, I. D. (1973). Rapid determination of free proline for water-stress studies. Plant and Soil, 39(1), 205–207. https://doi.org/10.1007/BF00018060.
Bharath, P., Gahir, S., & Raghavendra, A. S. (2021). Abscisic acid-induced stomatal closure: An important component of plant defense against abiotic and biotic stress. Frontiers in Plant Science, 12(1), 615114. https://doi.org/10.3389/fpls.2021.615114.
Bryant, C., Fuenzalida, T. I., Brothers, N., Mencuccini, M., Sack, L., Binks, O., & Ball, M. C. (2021). Shifting access to pools of shoot water sustains gas exchange and increases stem hydraulic safety during seasonal atmospheric drought. Plant Cell and Environment, 44(11), 2898–2911. https://doi.org/10.1111/pce.14080.
Burssens, S., Himanen, K., Van de Cotte, B., Beeckman, T., Van Montagu, M., Inzé, D., & Verbruggen, N. (2000). Expression of cell cycle regulatory genes and morphological alterations in response to salt stress in Arabidopsis thaliana. Planta, 211(5), 632–640. https://doi.org/10.1007/s004250000334.

Canavar, Ö., Götz, K. P., Ellmer, F., Chmielewski, F. M., & Kaynak, M. A. (2014). Determination of the relationship between water use efficiency, carbon isotope discrimination and proline in sunflower genotypes under drought stress. Australian Journal of Crop Science, 8(2), 232–242. https://search.informit.org/doi/10.3316/ informit.198767721017085.
Canavar, Ö., Gören, H. K., Tan, U., Yilmaz, O., Kaptan, M. A., & Küçük Kaya, S. (2025). Physiological responses of sunflower (Helianthus annuus L.) to multiple combined prolonged drought stress, salinity stress and boron toxicity: insights from pre‐and post‐recovery stages. Journal of Agronomy and Crop Science, 211(2), e70047. https://doi.org/10.1111/jac.70047
Conn, S., & Gilliham, M. (2010). Comparative physiology of elemental distributions in plants. Annals of Botany, 105(7), 1081–1102. https://doi.org/10.1093/aob/mcq027
Doğan, R., Şahin, U., & Kızılgeçi, F. (2015). Tarımsal üretimde soya fasulyesinin yeri ve önemi. Tarım Bilimleri Dergisi, 21(2), 123–132.
Doğru, A., & Canavar, S. (2020). Bitkilerde tuz toleransının fizyolojik ve biyokimyasal bileşenleri. Academic Platform Journal of Engineering and Science, 8(1), 155–174. https://doi.org/10.21541/apjes.541620
Dos Santos, T. B., Budzinski, I. G., Marur, C. J., Petkowicz, C. L., Pereira, L. F., & Vieira, L. G. (2011). Expression of three galactinol synthase isoforms in Coffea arabica L. and accumulation of raffinose and stachyose in response to abiotic stresses. Plant Physiology and Biochemistry, 49(4), 441–448. https://doi.org/10.1016/ j.plaphy.2011.01.023
Düzgüneş, O., & Akman, H. (1985). Varyasyon Kaynakları. A.Ü. Ziraat Fakültesi Yayınları, 954, 151.
Düzgüneş, O., Kesici, T., Kavuncu, O., & Gürbüz, F. (1987). Araştırma ve Deneme Metodları. A.Ü. Ziraat Fakültesi Yayınları, 1021, 1–381.
Flam-Shepherd, R., Huynh, W. Q., Coskun, D., Hamam, A. M., Britto, D. T., & Kronzucker, H. J. (2018). Membrane fluxes, bypass flows, and sodium stress in rice: The influence of silicon. Journal of Experimental Botany, 69(7), 1679–1692. https://doi.org/10.1093/jxb/erx460.
Frechilla, S., Lasa, B., Ibarretxe, L., Lamsfus, C., & Aparicio-Tejo, P. (2001). Pea responses to saline stress is affected by the source of nitrogen nutrition (Ammonium or Nitrate). Plant Growth Regulation, 35(2), 171–179. https://doi.org/10.1023/A:1014487908495.
Fricke, W., Akhiyarova, G., Wei, W., Alexandersson, E., Miller, A., Kjellbom, P. O., Richardson, A., Wojciechowski, T., Schreiber, L., Veselov, D., Kudoyarova, G., & Volkov, V. (2006). The short-term growth response to salt of the developing barley leaf. Journal of Experimental Botany, 57(5), 1079–1095.
Glenn, E. P., Brown, J. J., & Khan, M. J. (1997). Mechanisms of salt tolerance in higher plants. In: Basra, A. S., & Basra, R. K. (Eds.), Mechanisms of environmental stress resistance in plants (pp. 83–110). Harwood Academic Publishers.
Gong, Z. (2021). Plant abiotic stress: New insights into the factors that activate and modulate plant responses. Journal of Integrative Plant Biology, 63(3), 429–430. https://onlinelibrary.wiley.com/doi/10.1111/jipb.13079
Hayat, S., Hayat, Q., Alyemeni, M.N., Wani, A.S., Pichtel, J. & Ahmad, A. (2012). Role of proline under changing environments: A review. Plant Signaling & Behavior 7(11), 1456–1466. https://doi.org/10.4161/psb.21949.
Hoagland, D.R., & Arnon, D.I. (1950). The water-culture method for growing plants without soil. Circular. California Agricultural Experiment Station, 347, 32.
Hodges, D., DeLong, J., Forney, C. & Prange, R. (1999). Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207(4), 604–611. https://doi.org/10.1007/s004250050524.
Hossain, M.I., Khatun, A., Talukder, M.S.A., Dewan, M.M.R. & Uddin, M.S. (2010). Effect of drought on physiology and yield contributing characters of sunflower. Bangladesh Journal of Agricultural Research 35(1), 113–124. https://doi.org/10.3329/bjar.v35i1.5872.
Hosseinifard, M., Stefaniak, S., Ghorbani, J.M., Soltani, E., Wojtyla, Ł. & Garnczarska, M. (2022). Contribution of exogenous proline to abiotic stresses tolerance in plants: A review. International Journal of Molecular Sciences 23(9), 5186. https://doi.org/10.3390/ijms23095186.
Hussain, M., Malik, M.A., Farooq, M., Ashraf, M.Y., & Cheema, M.A. (2008). Improving drought tolerance by exogenous application of glycinebetaine and salicylic acid in sunflower. J Agron Crop Sci 194(3), 193–199. https://doi.org/10.1111/j.1439-037X.2008.00305.x.
Jaleel, A.C., Manivannan, P., Wahid, A., Farooq, M., AlJuburi, H.J., Somasundaram, R. & Panneerselvam, R. (2009). Drought stress in plants: A review on morphological characteristics and pigments composition. International Journal of Agriculture and Biology 11(1), 100-105.
Juenger, T.E., & Verslues, P.E. (2023). Time for a drought experiment: Do you know your plants’ water status? The Plant Cell 35(1), 10–23. https://doi.org/10.1093/plcell/koac324.
Kesawat, M.S., Satheesh, N., Kherawat, B.S., Kumar, A., Kim, H.U., Chung, S.M. & Kumar, M. (2023). Regulation of reactive oxygen species during salt stress in plants and their crosstalk with other signaling molecules—current perspectives and future directions. Plants (Basel) 12(4), 864. https://doi.org/10.3390/plants12040864.
Kılıçaslan, S., Yıldırım, E., Ekinci, M. & Kul, R. (2020). Kuraklık stresinin fasulyede bitki gelişimi, bazı fizyolojik ve biyokimyasal özellikler üzerine etkisi. Erciyes Üniversitesi Fen Bilimleri Enstitüsü Dergisi 36(2), 264-273.
Kurt, D., Yücel, M., & Okur, B. (2023). Antioxidant enzyme activities and photosynthetic efficiency in soybean under salt stress. Journal of Plant Stress Physiology, 12(3), 201–214.
Lichtenthaler, H.K. (1987). Chlorophylls and carotenoids pigments of photosynthetic biomembranes. Methods in Enzymology 148(1), 350–382.
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.
Ma, Y., Dias, M.C. & Freitas, H. (2020). Drought and salinity stress response and microbe-induced tolerance in plants. Fontiers in Plant Science 11(1), 591911. https://doi.org/10.3389/fpls.2020.591911.
Morales, M. & Munné-Bosch, S. (2019). Malondialdehyde: Facts and artifacts. Plant Physiology 180(3), 1246–1250. https://doi.org/10.1104/pp.19.00405. PMID: 31253746; PMCID: PMC6752910.
Munns, R. (2005). Genes and salt tolerance: Bringing them together. New Phytologist 167(3), 645–663. https://doi.org/10.1111/j.1469-8137.2005.01487.x.
Munns, R., James, R.A. & Läuchli, A. (2006). Approaches to increasing the salt tolerance of wheat and other cereals. Journal of Experimental Botany 57(5), 1025–1043. https://doi.org/10.1093/jxb/erj100.
Munns, R., & Tester, M. (2008). Mechanisms of salinity tolerance. Annual Review of Plant Biology 59(1), 651–681. https://doi.org/10.1146/annurev.arplant.59.032607.092911.
Negrão, S., Schmöckel, S.M., & Tester, M. (2017). Evaluating physiological responses of plants to salinity stress. Annals of Botany 119(1),1–11. https://doi.org/10.1093/aob/mcw191.
Niu, M., Xie, J., Chen, C., Cao, H., Sun, J., Kong, Q., Shabala, S., Shabala, L., Huang, Y. & Bie, Z. (2018). An early ABA-induced stomatal closure, Na+ sequestration in leaf vein and K+ retention in mesophyll confer salt tissue tolerance in Cucurbita species. Journal of Experimental Botany 69(20), 4945–4960. https://doi.org/ 10.1093/jxb/ery251.
Özçınar, A., Arslan, H. & Arslan, D. (2022). Soya (Glycine max L. Merrill)’da tuz uygulamasının fizyolojik ve biyokimyasal özellikler üzerine etkisinin incelenmesi. ISPEC Journal of Agricultural Sciences 6(4),762–776.
Parihar, P., Singh, S.S., Singh, R., Singh, V.P. & Prasad, S.M. (2015). Effect of salinity stress on plants and its tolerance strategies: A review. Environmental Science and Pollution Research 22(6), 4056–4075. https://doi.org/10.1007/s11356-014-3739-1.
Priya, M., Sharma, L., Singh, I., Bains, T., Siddique, K.H., Bindumadhava, H., Nair, R.M. & Nayyar, H. (2019). Securing reproductive function in mungbean grown under high temperature environment with exogenous application of proline. Plant Physiology and Biochemistry 140(1), 136–150. https://doi.org/ 10.1016/j.plaphy.2019.05.009.
Raja, V., Majeed, U., Kang, H., Andrabi, K.I. & John, R. (2017). Abiotic stress: Interplay between ROS, hormones and MAPKs. Environmental and Experimental Botany 137(1), 142–157. https://doi.org/10.1016/ j.envexpbot.2017.02.010.
Rincon, C.A., Raper, C.D. & Patterson, R.P. (2003). Genotypic differences in root anatomy affecting water movement through roots of soybean. International Journal of Plant Sciences 164(4), 543–551. https://doi.org/10.1086/375377.
Rodriguez, P., Torrecillas, A., Morales, M.A., Ortuno, M.F. & Sanchez-Blanco, M.J. (2005). Effects of NaCl salinity and water stress on growth and leaf water relations of Asteriscus maritimus plants. Environmental and Experimental Botany 53(2), 113–123. https://doi.org/10.1016/j.envexpbot.2004.03.005.
Singh, A., Kumar, A., Yadav, S. & Singh, I.K. (2019). Reactive oxygen species-mediated signaling during abiotic stress. Plant Genetic 18(1), 100173. https://doi.org/10.1016/j.plgene.2019.100173
Stavi, I., Thevs, N. & Priori, S. (2021). Soil salinity and sodicity in drylands: A review of causes, effects, monitoring, and restoration measures. Frontiers in Environmental Science 9(1), 712831. https://doi.org/10.3389/ fenvs.2021.712831.
Tagnon, M.D., & Simeon, K.O. (2017). Aldehyde dehydrogenases may modulate signaling by lipid peroxidation-derived bioactive aldehydes. Plant Signal Behav 12(11), e1387707. https://doi.org/10.1080/ 15592324.2017.1387707.
Tan, U., & Gören, H. K. (2024). Comprehensive evaluation of drought stress on medicinal plants: a meta-analysis. PeerJ 12(1), e17801. https://doi.org/10.7717/peerj.17801.
Tanji, K.K. (2002). Toprak ortamında tuzluluk. İçinde: A. Lauchli & U. Luttge (Eds.), Salinity Environment-Plant Molecules (ss. 21–51). Kluwer Academic, Dordrecht.
Xiao, F. & Zhou, H. (2023). Plant salt response: Perception, signaling, and tolerance. Frontiers in Environmental Science 13(1), 1053699. https://doi.org/10.3389/fpls.2022.1053699.
Wang, X., Wang, W., Huang, J., Peng, S. & Xiong, D. (2018). Diffusional conductance to CO2 is the key limitation to photosynthesis in salt-stressed leaves of rice (Oryza sativa). Physiologia Plantarum 163(1), 45–58. https://doi.org/10.1111/ppl.12653.
Yıldırım, E., Ekinci, M., & Turan, M. (2015). Importance of soybean cultivation and its role in food security. Anatolian Journal of Agriculture, 30(1), 45–52.
Zhao, C., Zhang, C.H., Song, J.K., Zhu, J.K. & Shabala, S. (2020). Mechanisms of plant responses and adaptation to soil salinity. Innovation 1(1), 100017. https://doi.org/10.1016/j.xinn.2020.100017.
Zhao, S., Zhang, Q., Liu, M., Zhou, H., Ma, C. & Wang, P. (2021). Regulation of plant responses to salt stress. International Journal of Molecular Sciences 22(9), 4609. https://doi.org/10.3390/ijms22094609.

Details

Primary Language

English

Subjects

Agronomy

Journal Section

Research Article

Authors

Büşra Küçükkılııç
0000-0002-1479-7909
Türkiye

Öner Canavar
0000-0003-4168-953X
Türkiye

Hatice Kübra Gören ^*
0000-0001-7654-1450
Türkiye

Early Pub Date

October 18, 2025

Publication Date

January 1, 2026

Submission Date

May 15, 2025

Acceptance Date

August 15, 2025

Published in Issue

Year 2026 Volume: 29 Number: 1

DOI

https://doi.org/10.18016/ksutarimdoga.vi.1699900

IZ

https://izlik.org/JA54MG84WN

Cite

RIS / Bibtex

APA

Küçükkılııç, B., Canavar, Ö., & Gören, H. K. (2026). Salt Stress Effects Physiology Properties, Malondialdehyde and Proline Accumulation in Relation To Osmotic Adjustment Of Soybean [Glycine Max (L) Merrill]. Kahramanmaraş Sütçü İmam Üniversitesi Tarım Ve Doğa Dergisi, 29(1), 79-97. https://doi.org/10.18016/ksutarimdoga.vi.1699900