GENETIC AND MOLECULAR FOUNDATIONS OF SALT TOLERANCE: TRANSCRIPTOMIC, METABOLOMIC, AND GENOME EDITING APPROACHES

Öz

Salt stress is one of the most critical abiotic factors limiting agricultural productivity worldwide, triggering complex physiological and molecular responses that reduce plant growth, development, and yield. Salt tolerance is a polygenic trait governed by multifaceted processes, including ion homeostasis, osmotic adjustment, antioxidant defense, hormone signaling, and metabolic reprogramming. This review systematically evaluates the genetic and molecular bases of salt tolerance through transcriptomic (Duan et al., 2023a; Liu et al. 2021), metabolomic (Duan et al., 2023b; Zhang, Z., et al., 2023), and genome editing approaches (Zhang, H., et al., 2023; Zhu et al., 2024), offering an integrated perspective on recent advances. Recent progress in CRISPR–Cas systems has enabled precise modification of ion transporters, transcription factors, and stress-responsive regulatory genes, providing significant improvements in plant salt tolerance (Li et al., 2021; Wang et al., 2022a). Additionally, multi-omics integration has facilitated the elucidation of complex regulatory networks activated under salt stress, yielding comprehensive insights into the molecular determinants of tolerance (Wang et al., 2022b; Yu et al., 2025). Overall, this work presents a holistic analysis of molecular responses to salt stress and provides a robust scientific framework to guide future research and genomic breeding strategies aimed at enhancing salt tolerance in crops.

Anahtar Kelimeler

• Salt stress
• Salt tolerance
• Transcriptomics
• Metabolomics
• CRISPR–Cas systems

TUZ TOLERANSININ GENETİK VE MOLEKÜLER TEMELLERİ: TRANSKRİPTOM, METABOLOM VE GEN DÜZENLEME YAKLAŞIMLARI

Öz

Tuz stresi, dünya genelinde tarımsal üretimi sınırlayan başlıca abiyotik stres faktörlerinden biri olup, bitkilerde büyüme, gelişme ve verim kayıplarına yol açmaktadır. Bu derleme çalışması, tuz stresine karşı bitkilerin geliştirdiği tolerans mekanizmalarını fizyolojik, biyokimyasal ve moleküler düzeylerde bütüncül bir yaklaşımla ele almayı amaçlamaktadır. Çalışmada, ozmotik düzenleme, iyon homeostazı, antioksidan savunma sistemleri ve fotosentetik kapasitenin korunması gibi temel fizyolojik süreçler detaylı biçimde değerlendirilmiştir. Ayrıca, tuz stresine yanıtın moleküler boyutları; hücre içi sinyal iletim mekanizmaları, stresle ilişkili transkripsiyon faktörleri ve epigenetik düzenleyiciler bağlamında incelenmiştir. Transkriptomik ve metabolomik yaklaşımlar aracılığıyla elde edilen bulgular, tuz stresine bağlı gen ekspresyonu ve metabolit profillerindeki dinamik değişimlerin toleransın biyokimyasal temelini oluşturduğunu ortaya koymaktadır. Bununla birlikte, genom düzenleme teknolojilerinin, özellikle hedefe yönelik gen modifikasyonları yoluyla tuz toleransının geliştirilmesinde sunduğu potansiyel vurgulanmıştır. Derleme kapsamında, tuz toleransı araştırmalarının yalnızca tarımsal üretimle sınırlı kalmaması gerektiği; elde edilen moleküler ve fizyolojik bilginin, ürün kalitesi, hasat sonrası değerlendirme ve gıda güvenliği gibi alanlarla da ilişkilendirilmesinin önemi ele alınmıştır. Sonuç olarak bu çalışma, tuz stresine karşı bitkisel toleransın çok katmanlı bir yapı sergilediğini ve bu yapının sistem biyolojisi temelli, disiplinler arası yaklaşımlarla değerlendirilmesinin, sürdürülebilir tarımsal üretim ve güvenli gıda sistemlerinin geliştirilmesi açısından kritik bir rol oynadığını ortaya koymaktadır.

Anahtar Kelimeler

• Tuz stresi
• Tuz toleransı
• Transcriptomics
• Metabolomics
• CRISPR–Cas sistemleri

Kaynakça

1. Ajithkumar, V., Soni, K. B., Alex, S., Anuradha, T., Augustine, R., & Manju, R. V. (2025). CRISPR/Cas9-mediated genome editing for abiotic stress tolerance in crops: Current advances and future prospects. Plant Molecular Biology Reporter, 43, 1767–1789. https://doi.org/10.1007/s11105-025-01601-6
2. Ali, Z., Mahas, A., & Mahfouz, M. (2018). CRISPR/Cas13 as a tool for RNA interference. Trends in Plant Science, 23(5), 374–378. https://doi.org/10.1016/j.tplants.2018.03.003
3. Amin, I., Rasheed, A., Jamil, M., & Parveen, A. (2021). Ion homeostasis for salinity tolerance in plants: A molecular perspective. Physiologia Plantarum, 171(3), 578–594.
4. Anzalone, A. V., Randolph, P. B., Davis, J. R., Sousa, A. A., Koblan, L. W., Levy, J. M., Chen, P. J., Wilson, C., Newby, G. A., Raguram, A., & Liu, D. R. (2019). Search-and-replace genome editing without double-strand breaks or donor DNA. Nature, 576(7785), 149-157. https://doi.org/10.1038/s41586-019-1711-4
5. Araus, J. L., & Kefauver, S. C. (2018). Breeding to adapt agriculture to climate change: Affordable phenotyping solutions. Current Opinion in Plant Biology, 45, 237–247.
6. Aryal, J. P., Becerra Lopez-Lavalle, L. A., & El-Naggar, A. H. (2025). Crop loss due to soil salinity and agricultural adaptations to it in the Middle East and North Africa region. Resources, 14(9), 139. https://doi.org/10.3390/resources14090139
7. Ceylan, Z., Çelik, E., & Altay, F. (2025). Gıda biyoteknolojisinde güncel yöntemler ve uygulama alanları: Güvenlikten üretime yeni nesil yaklaşımlar. In Z. Ceylan & R. Meral (Eds.), Biyoteknolojiden konvansiyonel yöntemlere: Gıda muhafaza yöntemleri (pp. 7–32). Efe Akademi.
8. Ceylan, Z., Gürel İnanlı, A., Meral, R., Dalkılıç, S., Kadıoğlu Dalkılıç, L., Karaismailoğlu, M. C., Seven Avuk, H., & Köse, N. (2024). Bioactive nano-scale material approved with HepG2 and MCF-7 cancer cell lines, antimicrobial properties and characterization parameters. Food Bioscience, 61, 104696. https://doi.org/10.1016/j.fbio.2024.104696

9. Crossa, J., Pérez-Rodríguez, P., Cuevas, J., Montesinos-López, O., Jarquín, D., de los Campos, G., Burgueño, J., González-Camacho, J. M., Pérez-Elizalde, S., Beyene, Y., Dreisigacker, S., Singh, R., Zhang, X., Gowda, M., Roorkiwal, M., Rutkoski, J., & Varshney, R. K. (2017). Genomic selection in plant breeding: Methods, models, and perspectives. Trends in Plant Science, 22(11), 961–975.
10. Dai, L., Li, P., Li, Q., Leng, Y., Zeng, D., & Qian, Q. (2022). Integrated multi-omics perspective to strengthen the understanding of salt tolerance in rice. International Journal of Molecular Sciences, 23(9), 5236. https://doi.org/10.3390/ijms23095236
11. Duan, H., Tiika, R. J., Tian, F., Lu, Y., Zhang, Q., Hu, Y., Cui, G., & Yang, H. (2023). Metabolomics analysis unveils important changes involved in the salt tolerance of Salicornia europaea. Frontiers in Plant Science, 13, 1097076. https://doi.org/10.3389/fpls.2022.1097076
12. Fang, X., Mo, J., Zhou, H., Shen, X., Xie, Y., Xu, J., & Yang, S. (2023). Comparative transcriptome analysis of gene responses of salt-tolerant and salt-sensitive rice cultivars to salt stress. Scientific Reports, 13, 19065. https://doi.org/10.1038/s41598-023-46389-1
13. Flowers, T. J., & Colmer, T. D. (2015). Plant salt tolerance: Adaptations in halophytes. Annals of Botany, 115(3), 327–331. https://doi.org/10.1093/aob/mcu267
14. Food and Agriculture Organization of the United Nations (FAO). (2024). The global status of salt-affected soils. FAO. https://doi.org/10.4060/cd3044en
15. Gill, S. S., & Tuteja, N. (2020). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry, 48(12), 909-930. https://doi.org/10.1016/j.plaphy.2010.08.016
16. Gupta, B., & Huang, B. (2014). Mechanism of salinity tolerance in plants: Physiological, biochemical, and molecular characterization. International Journal of Genomics, 2014, 701596. https://doi.org/10.1155/2014/701596
17. Haddadi, B. S., Fang, R., Girija, A., Kattupalli, D., Widdowson, E., Beckmann, M., Yadav, R., & Mur, L. A. J. (2023). Metabolomics targets tissue-specific responses in alleviating the negative effects of salinity in tef (Eragrostis tef) during germination. Planta, 258, 67. https://doi.org/10.1007/s00425-023-04224-x
18. Hasanuzzaman, M., Bhuyan, M. H. M. B., Zulfiqar, F., Raza, A., Mohsin, S. M., Mahmud, J. A., Fujita, M., & Fotopoulos, V. (2020). Reactive oxygen species and antioxidant defense in plants under abiotic stress. Antioxidants, 9(8), 681. https://doi.org/10.3390/antiox9080681
19. He, X., Zhu, J., Gong, X., Zhang, D., Li, Y., Zhang, X., Zhao, X., & Zhou, C. (2025). Advances in deciphering the mechanisms of salt tolerance in maize. Plant Signaling & Behavior, 20(1), 2479513. https://doi.org/10.1080/15592324.2025.2479513
20. Isah, T. (2019). Stress and defense responses in plant secondary metabolites production. Biological Research, 52, 39. https://doi.org/10.1186/s40659-019-0246-3
21. Joshi, S., Nath, J., Singh, A. K., Pareek, A., & Joshi, R. (2022). Ion transporters and their regulatory signal transduction mechanisms for salinity tolerance in plants. Physiologia Plantarum, 174(3), e13702. https://doi.org/10.1111/ppl.13702
22. Julkowska, M. M., & Testerink, C. (2015). Tuning plant signaling and growth to survive salt. Trends in Plant Science, 20(9), 586–594. 10.1016/j.tplants.2015.06.008
23. Kavi Kishor, P. B., & Sreenivasulu, N. (2014). Is proline accumulation per se correlated with stress tolerance or is it a stress indicator? Plant Cell Reports, 37(2), 300-311. https://doi.org/10.1111/pce.12157
24. Kinoshita, T., & Seki, M. (2014). Epigenetic memory for stress response and adaptation in plants. Plant & Cell Physiology, 55(11), 1859–1863. 10.1093/pcp/pcu125
25. Krasensky, J., & Jonak, C. (2012). Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. Journal of Experimental Botany, 63(4), 1593–1608. https://doi.org/10.1093/jxb/err460
26. Ksouri, R., Ksouri, W. M., Jallali, I., Debez, A., Magné, C., Hiroko, I., & Abdelly, C. (2012). Medicinal halophytes: Potent source of health promoting biomolecules with medical, nutraceutical and food applications. Critical Reviews in Biotechnology, 32(4), 289–326. https://doi.org/10.3109/07388551.2011.630647
27. Liu, X., Yang, X., & Zhang, B. (2021). Transcriptome analysis and functional identification of GmMYB46 in soybean seedlings under salt stress. PeerJ, 9, e12492. https://doi.org/10.7717/peerj.12492
28. Munns, R., & Tester, M. (2008). Mechanisms of salinity tolerance. Annual Review of Plant Biology, 59, 651–681. 10.1146/annurev.arplant.59.032607.092911
29. Negacz, K., Malek, Ž., de Vos, A., & Vellinga, P. (2022). Saline soils worldwide: Identifying the most promising areas for saline agriculture. Journal of Arid Environments, 203, 1–9. https://doi.org/10.1016/j.jaridenv.2022.104775
30. Obata, T., & Fernie, A. R. (2012). The use of metabolomics to dissect plant responses to abiotic stresses. Cellular and Molecular Life Sciences, 69(19), 3225–3243.
31. Rai, G. K., Khanday, D. M., Kumar, P., Magotra, I., Choudhary, S. M., Kosser, R., Kalunke, R., Giordano, M., Corrado, G., Rouphael, Y., & Pandey, S. (2023). Enhancing crop resilience to drought stress through CRISPR-Cas9 genome editing. Plants, 12(12), 2306. https://doi.org/10.3390/plants12122306
32. Rai, G. K., Khanday, D. M., Kumar, P., Magotra, I., Choudhary, S. M., Kosser, R., Kalunke, R., Giordano, M., Corrado, G., Rouphael, Y., & Pandey, S. (2023). Enhancing crop resilience to drought stress through CRISPR-Cas9 genome editing. Plants, 12(12), 2306. https://doi.org/10.3390/plants12122306
33. Roy, S. J., Negrão, S., & Tester, M. (2014). Salt resistant crop plants. Current Opinion in Biotechnology, 26, 115–124. https://doi.org/10.1016/j.copbio.2013.12.004
34. Shabala, S., & Munns, R. (2022). Salinity stress: Physiological constraints and adaptive mechanisms. In Plant stress physiology (pp. 59–93). https://doi.org/10.1079/9781845939953.0059
35. Shelake, R. M., Kadam, U. S., Kumar, R., Pramanik, D., Singh, A. K., & Kim, J.-Y. (2022). Engineering drought and salinity tolerance traits in crops. Plant Communications, 3(6), 100417. https://doi.org/10.1016/j.xplc.2022.100417
36. Simarmata, T., Setiawati, M. R., & Fitriatin, B. N. (2025). Integrating metabolomic and transcriptomic approaches to understand plant responses to salinity. Systems Microbiology and Biomanufacturing, 20(1), Article 2567358. https://doi.org/10.1080/17429145.2025.2567358
37. van Zelm, E., Zhang, Y., & Testerink, C. (2020). Salt tolerance mechanisms of plants. Annual Review of Plant Biology, 71, 403–433. 10.1146/annurev-arplant-050718-100005
38. Varshney, R. K., Bohra, A., Roorkiwal, M., Barmukh, R., Cowling, W. A., Chitikineni, A., Lam, H.-M., Hickey, L. T., Croser, J. S., Bayer, P. E., Edwards, D., Crossa, J., Weckwerth, W., Millar, H., Kumar, A., Bevan, M. W., & Siddique, K. H. M. (2021). Fast-forward breeding for a food-secure world. Trends in Genetics, 37(12), 1124–1136. https://doi.org/10.1016/j.tig.2021.08.002
39. Xiao, F., & Zhou, H. (2023). Plant salt response: Perception, signaling, and tolerance. Frontiers in Plant Science, 13, 1053699. https://doi.org/10.3389/fpls.2022.1053699
40. Yu, T., Ma, X., Zhang, J., Cao, S., Li, W., Yang, G., & He, C. (2025). Progress in transcriptomics and metabolomics in plant responses to abiotic stresses. Current Issues in Molecular Biology, 47(6), 421. https://doi.org/10.3390/cimb47060421
41. Zhang, D., Zhang, D., Zhang, Y., Li, G., Sun, D., Zhou, B., & Li, J. (2024). Insights into the epigenetic basis of plant salt tolerance. International Journal of Molecular Sciences, 25(21), 11698. https://doi.org/10.3390/ijms252111698
42. Zhang, H., Yu, C., Zhang, Q., Qiu, Z., Zhang, X., Hou, Y., & Zang, J. (2025). Salinity survival: Molecular mechanisms and adaptive strategies in plants. Frontiers in Plant Science, 16, 1527952. https://doi.org/10.3389/fpls.2025.1527952
43. Zhu, J. K. (2016). Abiotic stress signaling and responses in plants. Cell, 167(2), 313–324.
44. Zörb, C., Geilfus, C. M., & Dietz, K. J. (2018). Salinity and crop yield. Plant Biology, 21(S1), 31–38. https://doi.org/10.1111/plb.12884