Proteomics-Based Analysis during Salt Stress in Rice Seedling
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Abstract
Saline soil is one of the major challenges in rice production. Understanding changes in rice proteome in response to salt stress is important to underpin complicated molecular mechanisms underlying this important crop’s growth and yield production. Recent advances in proteomics analysis using mass spectrometry can enhance the study of plant proteins function in a deeper view. In this study, we aimed to explore qualitative and quantitative changes of proteins in rice after salt stress treatment. Pokkali, KDML105, PTT1, RD85, and IR29 were used for the proteomics analysis under salt stress treatment. The experiments were conducted at the seedling stage by gradually increasing the NaCl concentration of the hydroponic solution from 8 dS/m to 12 dS/m within 3 days. After 0, 1, 2, 3, 4, and 7 days under the salinity condition, rice leaf samples were collected for protein extraction and preparation for LC-MS/MS-based shotgun proteomics analysis. Changes in Pokkali’s proteome in response to salt stress since the first day after salt stress treatment revealed several differentially expressed proteins involved in photosynthesis, reactive oxygen species (ROS) scavenging, ion homeostasis, and signal transduction pathway. KDML105, PTT1, and RD85 demonstrated changes in some proteins detected in Pokkali as the up-regulated proteins, although the level of the proteins expressed in these moderate tolerance varieties was slightly lower than in Pokkali which the highly tolerance variety. Our findings lead to the identification of genes encoding for the proteins involved in salt-tolerant mechanisms in rice such as ascorbate peroxidase, superoxide dismutase, glutathione-s-transferases, as well as abiotic stress responsive (ASR) protein. The development of molecular markers associated with the candidate genes identified here can be useful in salt-tolerant rice breeding using marker-assisted selection (MAS) technology.
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กรมพัฒนาที่ดิน. 2558. สภาพทรัพยากรดินและที่ดินของประเทศไทย. กรุงเทพฯ. 340 หน้า.
กรมพัฒนาที่ดิน. 2561. แผนบริหารจัดการทรัพยากรดินปัญหาของประเทศไทยระยะ 20 ปี (2561-2580). กรุงเทพฯ. 266 หน้า.
ดวงใจ สุริยาอรุณโรจน์, อภิชาติ วรรณวิจิตร, สมวงศ์ ตระกูลรุ่ง และธีรยุทธ์ ตู้จินดา. 2550. การปรับปรุงพันธุ์ข้าวให้ทนเค็มและมีคุณภาพหุงต้มดี. วารสารวิชาการข้าว 1(1): 29-43.
Asif, S., E. Kim, Y. Hee. Jang, R. Jan, N. Kim, S. Asaf, L. Muhammad Farooq and K.M. Kim. 2022. Identification of the OsCML4 gene in rice related to salt stress using QTL analysis. Plants 11(19): 2467.
Banerjee, S. 2021. Plant sulfate transporters dealing with drought and salinity stress. pp. 77-87. In: Transporters and Plant Osmotic Stress. Elsevier.
Bradford, M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72: 248-254.
Chaudhry, U.K., Z.N.Ö. Gökçe and A.F. Gökçe. 2021. Drought and salt stress effects on biochemical changes and gene expression of photosystem II and catalase genes in selected onion cultivars. Biologia 76(10): 3107-3121.
Chutimanukul, P., B. Kositsup, K. Plaimas, T. Buaboocha, M. Siangliw, T. Toojinda, L. Comai and S. Chadchawan. 2018. Photosynthetic responses and identification of salt tolerance genes in a chromosome segment substitution line of ‘Khao Dawk Mali 105’ rice. Environmental and Experimental Botany 155: 497-508.
Chutimanukul, P., B. Kositsup, K. Plaimas, M. Siangliw, T. Toojinda and S. Chadchawan. 2019. Effect of salt stress on antioxidant enzyme activity and hydrogen peroxide content in chromosome segment substitution line of ‘Khao Dawk Mali 105’ rice. Agriculture and Natural Resources 53(5): 465-471.
Clarkson, D.T. and J.B. Hanson. 1980. The mineral nutrition of higher plants. Annual Review of Plant Physiology 31(1): 239-298.
Gallardo, K., P.E. Courty, C.L. Signor, D. Wipf and V. Vernoud. 2014. Sulfate transporters in the plant’s response to drought and salinity: regulation and possible functions. Frontiers in Plant Science 5: 1-7.
IRRI. 2002. Standard Evaluation System for Rice (SES). International Rice Research Institute, Los Baños, Manila, Phillippines. 56 p.
Ji, H., J.M. Pardo, G.B., M.J.V. Oosten, R.A. Bressan and X. Li. 2013. The salt overly sensitive (SOS) pathway: established and emerging roles. Molecular Plant 6(2): 275-86.
Karkute, S.G., V. Kumar, M. Tasleem, D.C. Mishra, K.K. Chaturvedi, A. Rai, A.M. Sevanthi, K. Gaikwad, T.R. Sharma and A.U. Solanke. 2022. Genomewide analysis of von Willebrand factor A gene family in rice for its role in imparting biotic stress resistance with emphasis on rice blast disease. Rice Science 29(4): 375-384.
Kim, Y., B. Mun, A.L. Khan, M. Waqas, H.K. Kim, R. Shahzad, M. Imran, B.W. Yun and I.J. Lee. 2018. Regulation of reactive oxygen and nitrogen species by salicylic acid in rice plants under salinity stress conditions. PLoS ONE 13(3): e0192650.
Lekklar, C., D. Suriya-arunroj, M. Pongpanich, L. Comai, K. Kositsup, S. Chadchawan and T. Buaboocha. 2019. Comparative genomic analysis of rice with contrasting photosynthesis and grain production under salt stress. Genes 10(8): 562.
Ma, H. and J. Zhao. 2010. Genome-wide identification, classification, and expression analysis of the arabinogalactan protein gene family in rice (Oryza sativa L.). Journal of Experimental Botany 61(10): 2647-2668.
Macovei, A., B. Garg, S. Raikwar, A. Balestrazzi, D. Carbonera, A. Buttafava, J.F.J. Bremont, S.S. Gill and N. Tuteja. 2014. Synergistic exposure of rice seeds to different doses of γ-ray and salinity stress resulted in increased antioxidant enzyme activities and gene-specific modulation of TC-NER pathway. BioMed Research International 1-15.
Malefo, M.B., E.O. Mathibela, B.G. Crampton and M.E. Makgopa. 2020. Investigating the role of Bowman- Birk serine protease inhibitor in Arabidopsis plants under drought stress. Plant Physiology and Biochemistry 149: 286-293.
Nounjan, N., P. Chansongkrow, V. Charoensawan, J.L. Siangliw, T. Toojinda, S. Chadchawan and P. Theerakulpisut. 2018. High performance of photosynthesis and osmotic adjustment are associated with salt tolerance ability in rice carrying drought tolerance QTL: physiological and co-expression network analysis. Frontiers in Plant Science 9: 1135.
Olmos, E., J.G. Garma, M.C. Gomez-Jimenez and N. Fernandez-Garcia. 2017. Arabinogalactan proteins are involved in salt-adaptation and vesicle trafficking in tobacco by-2 cell cultures. Frontiers in Plant Science 8: 1092.
Parveen, A., S. Ahmar, M. Kamran, Z. Malik, A. Ali, M. Riaz and G.H. Abbasi. 2021. Abscisic acid signaling reduced transpiration flow, regulated Na+ ion homeostasis and antioxidant enzyme activities to induce salinity tolerance in wheat (Triticum Aestivum L.) seedlings. Environmental Technology & Innovation 24: 101808.
Pérez-Díaz, J., T.M. Wu, R. Pérez-Díaz, S. Ruíz-Lara, C.Y. Hong and J.A. Casaretto. 2014. Organ- and stress-specific expression of the ASR genes in rice. Plant Cell Reports 33(1): 61-73.
Quan, R., J. Wang, J. Hui, H. Bai, X. Lyu, Y. Zhu, H. Zhang, Z. Zhang, S. Li and R. Huang. 2018. Improvement of salt tolerance using wild rice genes. Frontiers in Plant Science 8: 2269.
Quinet, M., A. Ndayiragije, I. Lefevre, B. Lambillotte, C.C. Dupont-Gillain and S. Lutts. 2010. Putrescine differently influences the effect of salt stress on polyamine metabolism and ethylene synthesis in rice cultivars differing in salt resistance. Journal of Experimental Botany 61(10): 2719-2733.
R Core Team. 2022. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available source: https://www.R-project.org/. (May 20, 2023)
Razzaque, S., S.M. Elias, T. Haque, S. Biswas, G.M. Nurnabi Azad Jewel, S. Rahman, X. Weng, A.M. Ismail, H. Walai, T.E. Juenger and Z.I. Seraj. 2019. Gene expression analysis associated with salt stress in a reciprocally crossed rice population. Scientific Reports 9(1): 8249.
Rossatto, T., M.N. Amaral, L.C. Benitez, I.L. Vighi, E.J.B. Braga, A.M. Magalhães Júnior, M.A.C. Maia and L.S. Pinto. 2017. Gene expression and activity of antioxidant enzymes in rice plants, Cv. BRS AG, under saline stress. Physiology and Molecular Biology of Plants 23(4): 865-875.
Ruan, S.L., H.S. Ma, S.H. Wang, Y.P. Fu, Y. Xin, W.Z. Liu, F. Wang, J.X. Tong, S.Z. Wang and H.Z. Chen. 2011. Proteomic identification of OsCYP2, a rice cyclophilin that confers salt tolerance in rice (Oryza sativa L.) seedlings when overexpressed. BMC Plant Biology 11(1): 34.
Saha, J. and K. Giri. 2017. Molecular phylogenomic study and the role of exogenous spermidine in the metabolic adjustment of endogenous polyamine in two rice cultivars under salt stress. Gene 609: 88-103.
Sanyal, R.P., V. Prashar, N. Jawali, R. Sunkar, H.S. Misra and A. Saini. 2022. Molecular and biochemical analysis of duplicated cytosolic CuZn superoxide dismutases of rice and in silico analysis in plants. Frontiers in Plant Science 13: 864330.
Shan, L., C. Li, F. Chen, S. Zhao and G. Xia. 2008. A Bowman-Birk type protease inhibitor is involved in the tolerance to salt stress in wheat. Plant, Cell & Environment 31(8): 1128-1137.
Sharma, R., A. Sahoo, R. Devendran and M. Jain. 2014. Over-expression of a rice tau class glutathione s-transferase gene improves tolerance to salinity and oxidative Stresses in Arabidopsis. K. Wu (eds.). PLoS ONE 9(3): e92900.
Sripinyowanich, S., P. Klomsakul, B. Boonburapong, T. Bangyeekhun, T. Asami, H. Gu, T. Buaboocha and S. Chadchawan. 2013. Exogenous ABA induces salt tolerance in indica rice (Oryza sativa L.): the role of OsP5CS1 and OsP5CR gene expression during salt stress. Environmental and Experimental Botany 86: 94-105.
Sudhir, P. and S.D.S. Murthy. 2004. Effects of salt stress on basic processes of photosynthesis. Photosynthetica 42(4): 481-486.
Tester, M. and R. Davenport. 2003. Na+ tolerance and Na+ transport in higher plants. Annals of Botany 91(5): 503-527.
Thomas, D.S.G. and N.J. Middleton. 1993. Salinization: new perspectives on a major desertification issue. Journal of Arid Environments 24(1): 95-105.
Trivedi, D.K., M.W. Ansari and N. Tuteja. 2013. Multiple abiotic stress responsive rice cyclophilin: (OsCYP-25) mediates a wide range of cellular responses. Communicative & Integrative Biology 6(5): e25260.
Tsai, Y.C., C.Y. Hong, L.F. Liu and C.H. Kao. 2005. Expression of ascorbate peroxidase and glutathione reductase in roots of rice seedlings in response to NaCl and H2O2. Journal of Plant Physiology 162(3): 291-299.
Tuteja, N., R. K. Sahoo, B. Garg and R. Tuteja. 2013. OsSUV3 dual helicase functions in salinity stress tolerance by maintaining photosynthesis and antioxidant machinery in rice (Oryza sativa L. Cv. IR64). The Plant Journal 76(1): 115-127.
Udomchalothorn, T., K. Plaimas, S. Sripinyowanich, C. Boonchai, T. Kojonna, P. Chutimanukul, L. Comai, T. Buaboocha and S. Chadchawan. 2017. OsNucleolin1-L expression in Arabidopsis enhances photosynthesis via transcriptome modification under salt stress conditions. Plant and Cell Physiology 58(4): 717-734.
Vengosh, A. 2003. Salinization and saline environments. pp. 1-35. In: Treatise on Geochemistry (eds.). Elsevier.
Wang, Y., J. Wang, X. Zhao, S. Yang, L. Huang, F. Du, Z. Li, X. Zhao, B. Fu and W. Wang. 2020. Overexpression of the transcription factor gene OsSTAP1 increases salt tolerance in rice. Rice 13(1): 50.
Wu, T.M., W.R. Lin, Y.T. Kao, Y.T. Hsu, C.H. Yeh, C.Y. Hong and C.H. Kao. 2013. Identification and characterization of a novel chloroplast/ mitochondria co-localized glutathione reductase 3 involved in salt stress response in rice. Plant Molecular Biology 83(4-5): 379-390.
Yamada, N., C. Theerawitaya, H. Kageyama, S. Cha-um and T. Takabe. 2015. Expression of developmentally regulated plasma membrane polypeptide (DREPP2) in rice root tip and interaction with Ca2+/CaM complex and microtubule. Protoplasma 252(6): 1519-1527.
Yang, Z., J.L. Li, L.N. Liu, Q. Xie and N. Sui. 2020. Photosynthetic regulation under salt stress and salt-tolerance mechanism of sweet sorghum. Frontiers in Plant Science 10: 1722.
Yoshida, S., D.A. Forno, J.H., Cock and K.A. Gome. 1976. Laboratory manual for physiological studies of rice. IRRI, Las Baños, Laguna. 83 p.
Yuenyong, W., A. Chinpongpanich, L. Comai, S. Chadchawan, and T. Buaboocha. 2018. Downstream components of the calmodulin signaling pathway in the rice salt stress response revealed by transcriptome profiling and target identification. BMC Plant Biology 18(335): 1-23.
Zang, A., X. Xu, S. Neill and W. Cai. 2010. Overexpression of OsRAN2 in rice and Arabidopsis renders transgenic plants hypersensitive to salinity and osmotic stress. Journal of Experimental Botany 61(3): 777-789.
Zhang, C.J. and Y. Guo. 2012. OsTRXh1 regulates the redox state of the apoplast and influences stress responses in rice. Plant Signaling & Behavior 7(3): 440-442.
Zhang, Q., Y. Liu, Y. Jiang, A. Li, B. Cheng and J. Wu. 2022a. OsASR6 enhances salt stress tolerance in rice. International Journal of Molecular Sciences 23(16): 9340.
Zhang, Y., Y. Wang, X. Sun, J. Yuan, Z. Zhao, J. Gao, X. Wen, F. Tang, M. Kang, B. Abliz, Z. Zhang, H. Zhang, F. wang, and Z. Li. 2022b. Genome-wide identification of MDH family genes and their association with salt tolerance in rice. Plants 11(11): 1498.
Zhao, Y., W. Dong, N. Zhang, X. Ai, M. Wang, Z. Huang, L. Xiao and G. Xia. 2014. A wheat allene oxide cyclase gene enhances salinity tolerance via jasmonate signaling. Plant Physiology 164(2): 1068.
Zhu, J.K. 2000. Genetic analysis of plant salt tolerance using Arabidopsis. Plant Physiology 124(3): 941.