SavedAdd your journal

Journals / Iğdır Üniversitesi Fen Bilimleri Enstitüsü Dergisi / 2026 / Cilt: 16 Sayı: 3

Identification and Regulation of antiporters in Strawberry (Fragaria x ananassa) under salinity stress

Tuzluluk Stresi Altında Çilekte (Fragaria × ananassa) Antiporterlerin Belirlenmesi ve Düzenlenmesi

Muhammad Sameeullah(BOLU ABANT İZZET BAYSAL ÜNİVERSİTESİ)0000-0001-6767-2539
Vahdettin Çiftçi(Bolu ABANT İZZET BAYSAL ÜNİVERSİTESİ)0000-0002-0440-5959
Pages
1256–1270
Publication Date
2026-09-01
🏛️Bibliographic metadata and full text access for this article are provided via DergiPark.
DergiPark Record ↗
✨

AI Summary & Key Takeaways

AI Insight
⚡ TL;DR(Too Long; Didn't Read)

Future work will focus on the overexpression of selected upregulated antiporters (FaSOS1, FaSOS3, and FaNHX1.2) in Arabidopsis thaliana to further elucidate their functional roles in salinity tolerance.

📌 3 Key Takeaways

🎯
Objective & Hypothesis:Soil salinity is a major abiotic constraint that adversely affects plant growth and yield.
📊
Key Findings & Data:The SOS (Salt Overly Sensitive) family comprised three members (FaSOS1.1, FaSOS1.2, and FaSOS1.3), while SOS2, SOS3, SOS4, and SOS5 were each represented by a single gene (FaSOS2, FaSOS3, FaSOS4, and FaSOS5).
💡
Conclusion & Impact:Future work will focus on the overexpression of selected upregulated antiporters (FaSOS1, FaSOS3, and FaNHX1.2) in Arabidopsis thaliana to further elucidate their functional roles in salinity tolerance.
🔬Design:Araştırma Makalesi
📍Scope:Comprehensive Sample
⚙️Variables:Tuzluluk · Antiporterler · Gen düzenlenmesi

Abstract

Soil salinity is a major abiotic constraint that adversely affects plant growth and yield. The strawberry cultivar Sweet Charlie, previously reported as salt tolerant, was selected to evaluate physiological responses and to identify and characterize the differential regulation of antiporter genes under salinity stress. In total, ten antiporters were identified in cultivated strawberry, belonging to six gene families. The SOS (Salt Overly Sensitive) family comprised three members (FaSOS1.1, FaSOS1.2, and FaSOS1.3), while SOS2, SOS3, SOS4, and SOS5 were each represented by a single gene (FaSOS2, FaSOS3, FaSOS4, and FaSOS5). The NHX (cation/H⁺ exchanger) family included three members (FaNHX1.1, FaNHX1.2, and FaNHX2). The cultivar Sweet Charlie exhibited a high level of salt tolerance, with an LT₅₀ corresponding to 85 mM NaCl after 7 days of stress exposure. Physiological adaptations such as maintenance of leaf area, preservation of relative water content through stomatal regulation, osmotic adjustment, and sustained chlorophyll levels contributed to mitigating the detrimental effects of short-term salinity stress. At the molecular level, increased expression of FaSOS1.2 and FaSOS3 in roots, along with FaNHX1.2 in both roots and shoots, suggests their involvement in alleviating salt-induced toxicity. Short-term salinity stress also induced cellular damage, as evidenced by enhanced reactive oxygen species (ROS) accumulation, elevated malondialdehyde (MDA) levels, and increased electrolyte leakage. Future work will focus on the overexpression of selected upregulated antiporters (FaSOS1, FaSOS3, and FaNHX1.2) in Arabidopsis thaliana to further elucidate their functional roles in salinity tolerance.

Özet

Toprak tuzluluğu, bitki büyümesini ve verimini olumsuz yönde etkileyen başlıca abiyotik stres faktörlerinden biridir. Daha önce tuza toleranslı olduğu bildirilen çilek çeşidi Sweet Charlie, fizyolojik yanıtların değerlendirilmesi ile tuzluluk stresi altında antiporter genlerinin farklı düzenlenmesinin belirlenmesi ve karakterizasyonu amacıyla seçilmiştir. Toplamda, kültür çileğinde altı gen ailesine ait on adet antiporter tanımlanmıştır. SOS (Salt Overly Sensitive) ailesi üç üyeden (FaSOS1.1, FaSOS1.2 ve FaSOS1.3) oluşurken, SOS2, SOS3, SOS4 ve SOS5 aileleri sırasıyla tek bir gen ile temsil edilmiştir (FaSOS2, FaSOS3, FaSOS4 ve FaSOS5). NHX (katyon/H⁺ değiştirici) ailesi ise üç üyeden oluşmuştur (FaNHX1.1, FaNHX1.2 ve FaNHX2). Sweet Charlie çeşidi, 7 günlük stres uygulaması sonrasında 85 mM NaCl’ye karşılık gelen LT₅₀ değeri ile yüksek düzeyde tuz toleransı göstermiştir. Yaprak alanının korunması, stomatal düzenleme yoluyla nispi su içeriğinin sürdürülmesi, ozmotik uyum ve klorofil düzeylerinin devamlılığı gibi fizyolojik adaptasyonlar, kısa süreli tuzluluk stresinin zararlı etkilerinin azaltılmasına katkı sağlamıştır. Moleküler düzeyde ise, köklerde FaSOS1.2 ve FaSOS3 genlerinin yanı sıra hem kök hem de sürgünlerde FaNHX1.2 geninin artan ekspresyonu, bu genlerin tuzluluğun neden olduğu toksisitenin hafifletilmesinde rol oynayabileceğini göstermektedir. Kısa süreli tuzluluk stresi ayrıca hücresel hasara da neden olmuş; bu durum, artmış reaktif oksijen türleri (ROS) birikimi, yükselmiş malondialdehit (MDA) düzeyleri ve artan elektrolit sızıntısı ile ortaya konmuştur. Gelecekte yapılacak çalışmalarda, tuzluluk toleransındaki işlevsel rollerinin daha ayrıntılı olarak aydınlatılması amacıyla, ekspresyonu artış gösteren seçilmiş antiporter genlerinin (FaSOS1, FaSOS3 ve FaNHX1.2) Arabidopsis thaliana’da aşırı ekspresyonu üzerinde durulacaktır.

🔖

Cite This Article

Sameeullah, M., Çiftçi, V. (2026). Identification and Regulation of antiporters in Strawberry (Fragaria x ananassa) under salinity stress. Iğdır Üniversitesi Fen Bilimleri Enstitüsü Dergisi, Cilt: 16 Sayı: 3, 1256–1270. https://doi.org/10.21597/jist.1946021

📄 Full Text PDF Viewer

📄

PDF görüntüleyici hazırlanıyor...

References (54)

  1. Altuğ, C., Saleh, L. Y., Caner, E., Güneş, H., & Sameeullah, M. (2019). Multicomponent synthesis of novel thiazolo[3,2-a]pyridin-8-yl-phosphonates as a model of plant growth regulator. Phosphorus, Sulfur, and Silicon and the Related Elements, 194(1–2), 111–119.
  2. Apse, M. P., Aharon, G. S., Snedden, W. A., & Blumwald, E. (1999). Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science, 285(5431), 1256–1258.
  3. Arora, R., Wisniewski, M. E., & Scorza, R. (1992). Cold acclimation in genetically related (sibling) deciduous and evergreen peach (Prunus persica [L.] Batsch). I. Seasonal changes in cold hardiness and polypeptides of bark and xylem tissues. Plant Physiology, 99(4), 1562–1568.
  4. Hoagland, D. R., & Arnon, D. I. (1950). The water-culture method for growing plants without soil. Circular 347, University of California Agricultural Experiment Station, Berkeley.
  5. Awang, Y. B., & Atherton, J. (1995). Growth and fruiting responses of strawberry plants grown on rockwool to shading and salinity. Scientia Horticulturae, 62(1–2), 25–31.
  6. Barroso, M. M., & Alvarez, C. (1997). Toxicity symptoms and tolerance of strawberry to salinity in the irrigation water. Scientia Horticulturae, 71(3–4), 177–188.
  7. Berardini, T. Z., Reiser, L., Li, D., Mezheritsky, Y., Muller, R., Strait, E., & Huala, E. (2015). The Arabidopsis information resource: Making and mining the “gold standard” annotated reference plant genome. Genesis, 53(8), 474–485.
  8. Bates, L. S., Waldren, R. P., & Teare, I. D. (1973). Rapid determination of free proline for water-stress studies. Plant and Soil, 39, 205–207.
  9. Carvajal, M., Martinez, V., & Cerda, A. (1999). Influence of magnesium and salinity on tomato plants grown in hydroponic culture. Journal of Plant Nutrition, 22, 177–190.
  10. Darley, C. P., Van Wuytswinkel, O. C., Van Der Woude, K., & Mager, W. H. (2000). Arabidopsis thaliana and Saccharomyces cerevisiae NHX1 genes encode amiloride sensitive electroneutral Na+/H+ exchangers. Biochemical Journal, 351(1), 241–249.
  11. Díaz-López, L., Gimeno, V., Lidón, V., Simón, I., Martínez, V., & García-Sánchez, F. (2012). The tolerance of Jatropha curcas seedlings to NaCl: An ecophysiological analysis. Plant Physiology and Biochemistry, 54, 34–42.
  12. Faralli, M., Lektemur, C., Rosellini, D., & Gürel, F. (2015). Effects of heat shock and salinity on barley growth and stress-related gene transcription. Biologia Plantarum, 59(3), 537–546.
  13. Ferreira, J. F. S., Liu, X., & Suarez, D. L. (2014). Salinity tolerance of five commercial cultivars of strawberry (Fragaria × ananassa Duch.). In Proceedings of the 3rd International Salinity Forum (pp. 170–171), Riverside Convention Center, CA, USA.
  14. Fryer, M. J., Oxborough, K., Mullineaux, P. M., & Baker, N. R. (2002). Imaging of photo-oxidative stress responses in leaves. Journal of Experimental Botany, 53(372), 1249–1254.
  15. Gaxiola, R. A., Rao, R., Sherman, A., Grisafi, P., Alper, S. L., & Fink, G. R. (1999). The Arabidopsis thaliana proton transporters, AtNhx1 and Avp1, can function in cation detoxification in yeast. Proceedings of the National Academy of Sciences, 96(4), 1480–1485.
  16. Heath, R., & Packer, L. (1968). Photooxidation in isolated chloroplast. I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics, 125, 189–198.
  17. Hirakawa, H., Shirasawa, K., Kosugi, S., Tashiro, K., Nakayama, S., Yamada, M., Kohara, M., Watanabe, A., Kishida, Y., & Fujishiro, T. (2014). Dissection of the octoploid strawberry genome by deep sequencing of the genomes of Fragaria species. DNA Research, 21(2), 169–181.
  18. Husaini, A. M., & Abdin, M. Z. (2008). Development of transgenic strawberry (Fragaria × ananassa Duch.) plants tolerant to salt stress. Plant Science, 174, 446–455.
  19. Kepenek, K., & Koyuncu, F. (2000). Studies on the salt tolerance of some strawberry cultivars under glasshouse conditions. In International Symposium on Techniques to Control Salination for Horticultural Productivity 573 (pp. 297–304).
  20. Keutgen, A. J., & Pawelzik, E. (2008). Quality and nutritional value of strawberry fruit under long term salt stress. Food Chemistry, 107(4), 1413–1420.
  21. Liu, J., Ishitani, M., Halfter, U., Kim, C. S., & Zhu, J. K. (2000). The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proceedings of the National Academy of Sciences, 97(7), 3730–3734.
  22. Liu, J., & Zhu, J. K. (1997). An Arabidopsis mutant that requires increased calcium for potassium nutrition and salt tolerance. Proceedings of the National Academy of Sciences, 94(26), 14960–14964.
  23. Liu, J., & Zhu, J. K. (1998). A calcium sensor homolog required for plant salt tolerance. Science, 280(5371), 1943–1945.
  24. Loreto, F., & Velikova, V. (2001). Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiology, 127, 1781–1787.
  25. Lutts, S., Kinet, J. M., & Bouharmont, J. (1995). Changes in plant response to NaCl during development of rice (Oryza sativa L.) varieties differing in salinity resistance. Journal of Experimental Botany, 46, 1843–1852.
  26. Maas, E. V., & Hoffman, G. J. (1977). Crop salt tolerance-current assessment. Journal of the Irrigation and Drainage Division, 103(2), 115–134.
  27. Maggio, A., Miyazaki, S., Veronese, P., Fujita, T., Ibeas, J. I., Damsz, B., Narasimhan, M. L., Hasegawa, P. M., Joly, R. J., & Bressan, R. A. (2002). Does proline accumulation play an active role in stress-induced growth reduction? The Plant Journal, 31(6), 699–712.
  28. Miller, G., Shulaev, V., & Mittler, R. (2008). Reactive oxygen signaling and abiotic stress. Physiologia Plantarum, 133(3), 481–489.
  29. Orsini, F., Alnayef, M., Bona, S., Maggio, A., & Gianquinto, G. (2012). Low stomatal density and reduced transpiration facilitate strawberry adaptation to salinity. Environmental and Experimental Botany, 81, 1–10.
  30. Pitzschke, A., Forzani, C., & Hirt, H. (2006). Reactive oxygen species signaling in plants. Antioxidants and Redox Signaling, 8(9–10), 1757–1764.
  31. Quintero, F. J., Blatt, M. R., & Pardo, J. M. (2000). Functional conservation between yeast and plant endosomal Na+/H+ antiporters. FEBS Letters, 471(2–3), 224–228.
  32. Ruggiero, B., Koiwa, H., Manabe, Y., Quist, T., Inan, G., & Saccardo, F. (2004). Uncoupling the effects of ABA on plant growth and water relations: Analysis of sto1/nced3, an ABA-deficient but salt-tolerant mutant in Arabidopsis. Plant Physiology, 136, 3134–3147.
  33. Saied, A. S., Keutgen, A. J., & Noga, G. (2005). The influence of NaCl salinity on growth, yield and fruit quality of strawberry cvs. ‘Elsanta’ and ‘Korona’. Scientia Horticulturae, 103(3), 289–303.
  34. Sameeullah, M., Sasaki, T., & Yamamoto, Y. (2013). Sucrose transporter NtSUT1 confers aluminum tolerance on cultured cells of tobacco (Nicotiana tabacum L.). Soil Science and Plant Nutrition, 59, 756–770. [https://doi.org/10.1080/00380768.2013.830230](https://doi.org/10.1080/00380768.2013.830230)
  35. Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9(7), 671–675.
  36. Shi, H., Ishitani, M., Kim, C., & Zhu, J. K. (2000). The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proceedings of the National Academy of Sciences, 97(12), 6896–6901.
  37. Shi, H., Kim, Y., Guo, Y., Stevenson, B., & Zhu, J. K. (2003). The Arabidopsis SOS5 locus encodes a putative cell surface adhesion protein and is required for normal cell expansion. The Plant Cell, 15(1), 19–32.
  38. Shi, H., Xiong, L., Stevenson, B., Lu, T., & Zhu, J. K. (2002). The Arabidopsis salt overly sensitive 4 mutants uncover a critical role for vitamin B6 in plant salt tolerance. The Plant Cell, 14(3), 575–588.
  39. Shi, H., & Zhu, J. K. (2002). SOS4, a pyridoxal kinase gene, is required for root hair development in Arabidopsis. Plant Physiology, 129(2), 585–593.
  40. Steppuhn, H., van Genuchten, M. T., & Grieve, C. M. (2005). Root-zone salinity: I. Selecting a product-yield index and response function for crop tolerance. Crop Science, 45(1), 209–220.
  41. Topçu, H. (2022). Reference gene selection for RT-qPCR normalization of strawberry at various organs, different growing stages of fruits, and salt-stress treatment. Turkish Journal of Agriculture and Forestry, 46(4), 517–529. https://doi.org/10.55730/1300-011X.3022
  42. Turhan, E., & Eris, A. (2009). Changes of growth, amino acids, and ionic composition in strawberry plants under salt stress conditions. Communications in Soil Science and Plant Analysis, 40(21–22), 3308–3322.
  43. Turhan, E., Gulen, H., & Eris, A. (2008). The activity of antioxidative enzymes in three strawberry cultivars related to salt-stress tolerance. Acta Physiologiae Plantarum, 30(2), 201–208.
  44. Velikova, V., Yordanov, I., & Edreva, A. (2000). Oxidative stress and some antioxidant systems in acid rain-treated bean plants: Protective role of exogenous polyamines. Plant Science, 151, 59–66.
  45. Ward, J. M. (2001). Identification of novel families of membrane proteins from the model plant Arabidopsis thaliana. Bioinformatics, 17(6), 560–563. [https://doi.org/10.1093/bioinformatics/17.6.560](https://doi.org/10.1093/bioinformatics/17.6.560)
  46. Wu, S. J., Ding, L., & Zhu, J. K. (1996). SOS1, a genetic locus essential for salt tolerance and potassium acquisition. The Plant Cell, 8(4), 617–627.
  47. Xue, B., Zhang, A., & Jiang, M. (2009). Involvement of Polyamine Oxidase in Abscisic Acid-induced Cytosolic Antioxidant Defense in Leaves of Maize. Journal of Integrative Plant Biology, 51(3), 225–234.
  48. Yamasaki, S., & Dillemburg, L. R. (1999). Measurements of leaf relative water content in Araucaria angustifolia. Revista Brasileira de Fisiologia Vegetal, 11, 69–75.
  49. Yang, Q., Chen, Z. Z., Zhou, X. F., Yin, H. B., Li, X., Xin, X. F., Hong, X. H., Zhu, J. K., & Gong, Z. (2009). Overexpression of SOS (Salt Overly Sensitive) genes increases salt tolerance in transgenic Arabidopsis. Molecular Plant, 2(1), 22–31. [https://doi.org/10.1093/mp/ssn058](https://doi.org/10.1093/mp/ssn058)
  50. Yildiz, K., Uzal, Ö., & Yilmaz, H. (2008). Consequences of NaCl salinity on growth and ion accumulation in selected strawberry cultivars. European Journal of Horticultural Science, 73(2), 69.
  51. Zhang, H. X., & Blumwald, E. (2001). Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nature Biotechnology, 19(8), 765–768.
  52. Zhang, H. X., Hodson, J. N., Williams, J. P., & Blumwald, E. (2001). Engineering salt-tolerant Brassica plants: Characterization of yield and seed oil quality in transgenic plants with increased vacuolar sodium accumulation. Proceedings of the National Academy of Sciences, 98(22), 12832–12836.
  53. Zhou, F., Mosher, S., Tian, M., Sassi, G., Parker, J., & Klessig, D. F. (2008). The Arabidopsis gain-of-function mutant ssi4 requires RAR1 and SGT1b differentially for defense activation and morphological alterations. Molecular Plant-Microbe Interactions, 21(1), 40–49.
  54. Zhu, J. K., Liu, J., & Xiong, L. (1998). Genetic analysis of salt tolerance in Arabidopsis: Evidence for a critical role of potassium nutrition. The Plant Cell Online, 10(7), 1181–1191.