Comparative Profiles of Primary Metabolites of Suaeda salsa under Different Salt Stress Conditions

Document Type : Research Paper

Authors

1 Ph.D. Student, Department of Plant Breeding and Biotechnology (PBB), Faculty of Agriculture, Zanjan University, Zanjan, Iran

2 Assistant Professor, Department of Plant Breeding and Biotechnology (PBB), Faculty of Agriculture, Zanjan University, Zanjan, Iran

3 Department of Molecular Physiology, Agricultural Biotechnology Research Institute of Iran. (ABRII), Karaj, Iran

4 Assistant Professor, Department of System Biology, Agricultural Biotechnology Research Institute of Iran (ABRII), Karaj, Iran

Abstract

Suaeda salsa is an annual halophyte with nutritional value and high salt tolerance, making it crucial as an oil, medicinal, and edible plant. Currently, there is limited research in the field investigating metabolic diversity in S. salsa. In this study, our aim was to understand the salinity tolerance mechanism by examining metabolic diversity, specifically the amino acids profile, in S. salsa exposed to 0 mM, 200 mM, and 800 mM NaCl. The results of the physiological study indicated that salinity significantly affected the sodium (Na+) content in the aerial parts of the plant, with a significant increase compared to the control. Principal component analysis (PCA) revealed that differences in metabolic diversity can explain 96% of the phenotypic variation in S. salsa under salinity stress. Comparison of amino acids profiles at different salinity levels showed the highest accumulation of proline, methionine, citrulline, and lysine under 800 mM salt stress. Given the crucial role of these amino acids in S. Salsa,further studies are necessary to uncover the mechanisms behind the adaptation response.

Keywords

Main Subjects


Abrahám, E. Rigó, G. Székely, G. Nagy, R. Koncz, C. et al. (2003). Light-dependent induction of proline biosynthesis by abscisic acid and salt stress is inhibited by brassinosteroid in Arabidopsis. Plant Mol Biol, 51 (3): 363-372. Ahmad, P. Satyawati, S. (2008). Salt stress and phyto-biochemical responses of plants - A review. Plant, Soil and Environment, 54(3): 89-99. Arbelet-Bonnin, D. Blasselle, C. Rose Palm, E. Redwan, M. PonnaiaH. M. et al. (2020). Metabolism regulation during salt exposure in the halophyte Cakile maritima. Environmental and Experimental Botany, 177: 104075. Arbona, V. Manzi, M. Ollas, C. D. Gómez-Cadenas, A. (2013). Metabolomics as a tool to investigate abiotic stress tolerance in plants. International journal of molecular sciences, 14(3):: 4885-4911. Ashraf, M. Harris, P. J. C. (2004). Potential biochemical indicators of salinity tolerance in plants. Plant Science, 166: 3-16. Bates, L. S. Waldren, R. Teare, I. D. (1973). Rapid determination of free proline for water-stress studies. Plant and Soil, 39: 205-207. Bohnert, H. J. Jensen, R. G. (1996). Strategies for engineering water-stress tolerance in plants. Trends Biotechnol,. 14: 89–97. Bueno, M. Cordovilla, M. P. (2019). Polyamines in Halophytes. Front. Plant Sci. 9:10: 439. Cheng, Y. Yang, P. Zhao, L. Priyadarshani, S. Zhou, Q. et al. (2019). Studies on genome size estimation, chromosome number, gametophyte development and plant morphology of salt-tolerant halophyte Suaeda salsa. BMC Plant Biol, 19(1): 473. Cuin, T. A. Shabala, S. (2007). Amino acids regulate salinity-induced potassium efflux in barley root epidermis. Planta, 225(3): 753-761. Di Martino, C. Delfine, S. Pizzuto, R. Loreto, F. Fuggi, A. (2003). Free amino acids and glycine betaine in leaf osmoregulation of spinach responding to increasing salt stress. New Phytologist, 158(3): 455-463. Diray-Arce, J. Clement, M. Gul, B. Khan, M. A, Nielsen, B. L. (2015). Transcriptome assemblY. profiling and differential gene expression analysis of the halophyte Suaeda fruticosa provides insights into salt tolerance. BMC Genomics, 16(1): 353. El Moukhtari, A. Cabassa-Hourton, C. Farissi, M. Savouré, A. (2020). How Does Proline Treatment Promote Salt Stress Tolerance During Crop Plant Development. Frontiers in Plant Science, 23;11:1127. El-Samad, H. M. A. Shadad, M. A. K. Barak, N. (2011). Improvement of plants salt tolerance by exogenous application of amino acids. Journal of Medicinal Plants, 5: 5692-5699. Flowers, T. J. Galal, H. K. Bromham, L. (2010). Evolution of halophytes: multiple origins of salt tolerance in land plants. Functional Plant Biology, 37: 604-612. Fukusaki, E. Kobayashi, A. (2005). Plant metabolomics: potential for practical operation. J Biosci Bioeng, 100(4): 347-354. Guo, S. M. Tan, Y. Chu, H. J. Sun, M. X. Xing J. C. (2019). Transcriptome sequencing revealed molecular mechanisms underlying tolerance of Suaeda salsa to saline stress. PLOS ONE, 14(7): e219979. Hartzendorf, T. Rolletschek, H. (2001). Effects of NaCl-salinity on amino acid and carbohydrate contents of Phragmites australis. Aquatic Botany, 69: 195-208. Hong, J. Yang, L. Zhang, D. Shi, J .(2016). Plant Metabolomics: An Indispensable System Biology Tool for Plant Science. Int J Mol Sci, 17(6):767.Huang, Z. Zhao, L. Chen, D. Liang, M. Liu, Z. et al. (2013). Salt stress encourages proline accumulation by regulating proline biosynthesis and degradation in Jerusalem artichoke plantlets. PLoS One, 8(4): e62085. Khedr, A. H. A. Abbas, M. A. Wahid, A. A. A. Quick, W. P. Abogadallah, G. M. (2003). Proline induces the expression of salt‐stress‐responsive proteins and may improve the adaptation of Pancratium maritimum L. to salt‐stress. Journal of Experimental Botany, 54(392): 2553-2562. Kord, H. Fakheri, B. Ghabooli, M. Solouki, M. Emamjomeh, A. Khatabi, B. Sepehri, M. Salekdeh, G. H. Ghaffari, M. R. (2019). Salinity-associated microRNAs and their potential roles in mediating salt tolerance in rice colonized by the endophytic root fungus Piriformospora indica. Funct Integr Genomics, 19(4): 659-672. Koyro, H. W. C, Z. R. Debez, A. Huchzermeyer, B. (2013). The effect of hyper-osmotic salinity on protein pattern and enzyme activities of halophytes. Funct Plant Biol, 40(9): 787-804. Kusano, T. Berberich, T. Tateda, C. Takahashi, Y. (2008). Polyamines: essential factors for growth and survival. Planta, 228(3): 367-381. Li, Q. Song, J. (2019). Analysis of widely targeted metabolites of the euhalophyte Suaeda salsa under saline conditions provides new insights into salt tolerance and nutritional value in halophytic species. BMC plant biology, 19: 388-388. Lu, X. Liu, J. Liu, Y. Zhang, Z. Tang, Z. (2022). Suaeda glauca and Suaeda salsa Employ Different Adaptive Strategies to Cope with Saline–Alkali Environments. Agronomy, 12:10: 2496. Maggio, A. Miyazaki, S. Veronese, P. Fujita, T. Ibeas, J. I. et al. (2002). Does proline accumulation play an active role in stress-induced growth reduction. Plant J , 31(6): 699-712. Mansour, M. M. F. (1998). Protection of plasma membrane of onion epidermal cells by glycinebetaine and proline against NaCl stress. Plant Physiology and Biochemistry, 36: 767-772. Meng, X. Zhou, J. Sui, N. (2018). Mechanisms of salt tolerance in halophytes: Current understanding and recent advances. Open Life Sciences, 13: 149-154. Nasir, F. A. Batarseh, M. Abdel-Ghani, A. H. Jiries, A. (2010). Free Amino Acids Content in Some Halophytes under Salinity Stress in Arid Environment, Jordan. CLEAN – Soil, Air, Water, 38: 592-600. Nerd, A. Pasternak, D. (1992). GrowtH. ion accumulation, and nitrogen fractioning in Atriplex barclayana grown at various salinities. Society for Range Management, pp. 164-166. Obata, T. Fernie, A. R. (2012). The use of metabolomics to dissect plant responses to abiotic stresses. Cell Mol Life Sci, 69(19): 3225-3243. Panta, S. Flowers, T. Lane, P. Doyle, R. Haros, G. Shabala, S. (2014). Halophyte agriculture: success stories. Exp. Bot, 107: 71–83. Parida, A. K Veerabathini, S. K. Kumari, A. Agarwal, P. K. (2016). Physiological, Anatomical and Metabolic Implications of Salt Tolerance in the Halophyte Salvadora persica under Hydroponic Culture Condition. Front. Plant Sci, 22;7: 351. Ramanjulu, S. Sudhakar, C. (2000). Proline metabolism during dehydration in two mulberry genotypes with contrasting drought tolerance. Plant Physiology, 157: 81-85. Ray, S. Dansana, P. K. Giri, J. Deveshwar, P. Arora, R. et al. (2011). Modulation of transcription factor and metabolic pathway genes in response to water-deficit stress in rice. Funct Integr Genomics, 11(1): 157-178. Shahid, S. Kausar, A. Zahra, N. et al. (2023). Methionine-Induced Regulation of Secondary Metabolites and Antioxidants in Maize (Zea mays L.) Subjected to Salinity Stress. Gesunde Pflanzen, 75: 1143–1155. Shulaev, V, Cortes, D, Miller, G, Mittler, R (2008). Metabolomics for plant stress response. Physiol Plant, 132(2): 199-208. Song, J. Wang, B. (2015). Using euhalophytes to understand salt tolerance and to develop saline agriculture: Suaeda salsa as a promising model. Ann Bot, 115(3): 541-553. Thomas, J. C. De Armond, R. L. Bohnert, H. J. (1992). Influence of NaCl on GrowtH. Proline, and Phosphoenolpyruvate Carboxylase Levels in Mesembryanthemum crystallinum Suspension Cultures. Plant Physiology, 98(2): 626-631. Vicente, O. Boscaiu, M. Naranjo, M. Á. Estrelles, E. Bellés, J. M. A. et al. (2004). Responses to salt stress in the halophyte Plantago crassifolia (Plantaginaceae). Journal of Arid Environments, 58: 463-481. Xie, E. Wei, X. Ding, A. Zheng, L. Wu, X. et al. (2020). Short-Term Effects of Salt Stress on the Amino Acids of Phragmites australis Root Exudates in Constructed Wetlands. Water, 12: 569. Xu, Y. Zhao, Y. Duan, H. Sui, N. Yuan, F. et al. (2017). Transcriptomic profiling of genes in matured dimorphic seeds of euhalophyte Suaeda salsa. BMC Genomics, 18: 727. Yang, Z. Xie, T. Liu Q. (2014). Physiological responses of Phragmites australis to the combined effects of water and salinity stress. Ecohydrology, 7: 420-426. Yazdanpanah, P. Jonoubi, P. Zeinalabedini, M. Rajaei, H. Ghaffari, M. R. Vazifeshenas, M. R. Abdirad, S. (2021). Seasonal Metabolic Investigation in Pomegranate (Punica granatum L.) Highlights the Role of Amino Acids in Genotype- and Organ-Specific Adaptive Responses to Freezing Stress. Front Plant Sci, 12;12:699139. Narita,Y. Taguchi H. Nakamura T. Ueda A. Shi W. Takabe, T. (2004). Characterization of the salt-inducible methionine synthase from barley leaves. Plant Science, 167:1009–1016. Zhang, X. Yao, Y. Li, X. Zhang, L. Fan, S. (2020). Transcriptomic analysis identifies novel genes and pathways for salt stress responses in Suaeda salsa leaves. Sci Rep, 10(1): 4236. Zhao, L. Yang, Z. Guo, Q. Mao, S. Li, S. et al. (2017). Transcriptomic Profiling and Physiological Responses of Halophyte Kochia sieversiana Provide Insights into Salt Tolerance. Front. Plant Sci, 24;8:1985. Zhao, Y. Ma, Y. Li, Q. Yang, Y. Guo, J. et al. (2018). Utilisation of stored lipids during germination in dimorphic seeds of euhalophyte Suaeda salsa. Functional Plant Biology, 45(10): 1009-1016. Zhao, Y. Q. Ma, Y. C. Duan, H. M. Liu, R. R. Song, J. (2019). Traits of fatty acid accumulation in dimorphic seeds of the euhalophyte Suaeda salsa in saline conditions. Plant Biosystems - An International Journal Dealing with all Aspects of Plant Biology, 153: 514-520.