Investigation of Salinity Tolerance Related Gene Expression in Rice (Oryza sativa L.)

Abstract

Rice ranks second with the highest consumption rate after corn in world production. As a result of various biotic and abiotic stress factors exposed during production, plants quit normal growth. Under such conditions, plants have developed survival mechanisms at the molecular level in order to maintain their existence. Phenotypic data is widely used to evaluate plant tolerance with assistance of gene expression analysis that interprets the source of tolerance. In this study, Osmancık-97 rice variety which is extensively cultivated in Türkiye was grown under four different salt (NaCl) concentrations (60, 90, 120 mM and control) in in vivo conditions. The study aimed to determine the expression differences of the TPS1, NHX1, SOS1 and HKT2;1 genes under increasing salinity conditions. In the highest applied NaCl concentration (120 mM), TPS1, NHX1, SOS1 and HKT2;1 gene expression decreased 78.2, 74.0, 78.3, and 73.5% compared to the control, respectively. In the same concentration, parameters of photosynthetic pigment content, average plant length, fresh and dry weight, and root length decreased significantly. In contrast, proline accumulation and TBARS content presented significant increases. The difference in ion homeostasis and salt tolerance among species or varieties is related to the expression of regulatory genes. Rice, a moderately salt sensitive crop, has complex responses to salt stress and its sensitivity varies according to species, variety, growth and development stages and the duration of stress to which it is exposed.

Keywords

• Abiotic Stress
• Oryza sativa
• OsHKT2;1
• OsNHX1
• OsSOS1
• OsTPS1
• Salinity

Ethical Statement

There are no ethical issues after the publication of this manuscript.

Thanks

Authors acknowledge the support of Ministry of Agriculture and Forestry, Directorate of Trakya Agricultural Research Institute (Edirne, Türkiye) in providing source of seed materials

References

1. [1]. Jena KK. The Species of the Genus Oryza and Transfer of Useful Genes From Wild Species Into Cultivated Rice, O. sativa. Breeding Science 2010; 60: 518–523.
2. [2]. Chen T., Shabala S., Niu Y., et al. Molecular Mechanisms of Salinity Tolerance in Rice. The Crop Journal 2021; 9: 506–520.
3. [3]. Civan P., Ali S., Batista-Navarro R., et al. Origin of the Aromatic Group of Cultivated Rice (Oryza sativa L.) Traced to the Indian Subcontinent. Genome Biology and Evolution 2019; 11: 832.
4. [4]. Fukagawa NK., Ziska LH. Rice: Importance for Global Nutrition. Journal of Nutritional Science and Vitaminology2019; 65: S2–S3.
5. [5]. Erenstein O., Jaleta M., Sonder K., et al. Global Maize Production, Consumption and Trade: Trends and R&D Implications. Food Security 2022; 145 2022; 14: 1295–1319.
6. [6]. Öztürk D., Akçay Y. Güney Marmara Bölgesinde Çeltik Üretiminin Genel Bir Değerlendirmesi. Journal of Agricultural Faculty of Gaziosmanpaşa University 2010; 2010: 61–71.
7. [7] Taşligi̇l N., Şahi̇n G. Türkiye’de Çeltik (Oryza sativa L.) Yetiştiriciliği ve Coğrafi Dağılımı. Adıyaman Üniversitesi Sosyal Bilimler Enstitüsü Dergisi 2011; 182–203.
8. [8]. Paudel MN. Rice (Oryza sativa L.) Cultivation in the Highest Elevation of the World. Agronomy Journal of Nepal 2011; 2: 31–41.

9. [9]. Bouman BAM., Hengsdijk H., Hardy B., et al. Water-wise Rice Production. IRRI, 2002.
10. [10] Samal P., Babu SC., Mondal B., et al. The Global Rice Agriculture Towards 2050: An Inter-continental Perspective. Outlook on Agriculture 2022; 51: 164–172.
11. [11]. Turkey Rice Area, Yield and Production, https://ipad.fas.usda.gov/countrysummary/Default.aspx?id=TU&crop=Rice (accessed 11 November 2024).
12. [12]. Beşer N., Rice Food Security and Production in Turkey. https://ageconsearch.umn.edu/record/164415/files/AdvancesIn.pdf#page=97 (accessed 1 August 2024).
13. [13]. H.Sürek. Rice Production and Research Activities in Turkey. https://om.ciheam.org/om/pdf/c24-2/CI011101.pdf(accessed 1 August 2024).
14. [14]. van Dijk M., Morley T., Rau ML., et al. A Meta-analysis of Projected Global Food Demand and Population at Risk of Hunger For the Period 2010–2050. Nature Food 2021; 27 2021; 2: 494–501.
15. [15]. Gümüş T., Meriç S., Ayan A., et al. Plant Abiotic Stress Factors: Current Challenges of Last Decades and Future Threats. Plant Abiotic Stress Responses and Tolerance Mechanisms 2023; DOI: 10.5772/intechopen.110367.
16. [16]. Çelik Ö., Meriç S., Ayan A., et al. Epigenetic Analysis of WRKY Transcription Factor Genes in Salt Stressed Rice (Oryza sativa L.) plants. Environmental and Experimental Botany; 2019; 159 DOI: 10.1016/j.envexpbot.2018.12.015.
17. [17]. Sairam R., Physiology and Molecular Biology of Salinity Stress Tolerance in Plants. Current Science 2004 86:3, 407-421.
18. [18]. Zhu JK. Plant Salt Tolerance. Trends Plant Science 2001; 6: 66–71.
19. [19]. Tunç E., Tekin MS., Demir M., et al. Halophytic Species in Natural Areas Close to Agricultural Areas of Araban (Gaziantep, Turkey). Journal of Agricultural Chemistry and Environment 2020; 9: 48–58.
20. [20]. Sadak MS. Physiological Role of Trehalose on Enhancing Salinity Tolerance of Wheat Plant. Bulletin of the National Research Centre. 2019 431 2019; 43: 1–10.
21. [21]. Liang L., Guo L., Zhai Y., et al. Genome-wide Characterization of SOS1 Gene Family in Potato (Solanum tuberosum) and Expression Analyses Under Salt and Hormone Stress. Frontiers in Plant Science. 2023; 14: 1201730.
22. [22]. Solis CA, Yong MT, Zhou M, et al. Evolutionary Significance of NHX Family and NHX1 in Salinity Stress Adaptation in the Genus Oryza. Int J Mol Sci; 23. Epub ahead of print 1 February 2022. DOI: 10.3390/IJMS23042092.
23. [23]. Hamamoto S., Horie T., Hauser F., et al. HKT Transporters Mediate Salt Stress Resistance in Plants: From Structure and Function to the Field. Current Opinion in Biotechnology 2015; 32: 113–120.
24. [24]. Stewart RRC., Bewley JD. Lipid-Peroxidation Associated with Accelerated Aging of Soybean Axes. Plant Physiology. 1980; 65: 245–248.
25. [25]. Bates LS., Waldren RP., Teare ID. Rapid Determination of Free Proline for Water-Stress Studies. Plant and Soil. 1973; 39: 205–207.
26. [26]. Hoagland DR., Arnon DI. The Water-Culture Method for Growing Plants Without Soil. Circular. California Agricultural Experiment Station; 347:39.
27. [27]. Vaidyanathan H., Sivakumar P., Chakrabarty R., et al. Scavenging of Reactive Oxygen Species in NaCl-stressed Rice (Oryza sativa L.) - Differential Response in Salt-Tolerant and Sensitive Varieties. Plant Science. 2003; 165: 1411–1418.
28. [28]. Demiral T., Türkan İ. Comparative Lipid Peroxidation, Antioxidant Defense Systems and Proline Content in Roots of Two Rice Cultivars Differing in Salt Tolerance. Environmental and Experimental Botany. 2005; 53: 247–257.
29. [29]. Chen G., Zheng D., Feng N., et al. Physiological Mechanisms of ABA-induced Salinity Tolerance in Leaves and Roots of Rice. Scientific Reports. 2022 121; 12: 1–26.
30. [30]. Atta K., Mondal S., Gorai S., et al. Impacts of Salinity Stress on Crop Plants: Improving Salt Tolerance Through Genetic and Molecular Dissection. Frontiers in Plant Science. 2023; 14: 1241736.
31. [31]. Hariadi YC., Nurhayati AY., Soeparjono S., et al. Screening Six Varieties of Rice (Oryza sativa) for Salinity Tolerance. Procedia Environmental Sciences. 2015; 28: 78–87.
32. [32]. Harizanova A., Koleva-Valkova L. Effect of Silicon on Photosynthetic Rate and the Chlorophyll Fluorescence Parameters at Hydroponically Grown Cucumber Plants Under Salinity Stress. Journal of Central European Agriculture. 2019; 20: 953–960.
33. [33]. Jamil M., Bashir S., Anwar S., et al. Effect of Salinity on Physiological and Biochemical Characteristics of Different Varieties of Rice. Pakistan Journal of Botany. 2012; 44: 7–13.
34. [34]. Saddiq MS., Iqbal S., Hafeez MB., et al. Effect of Salinity Stress on Physiological Changes in Winter and Spring Wheat. Agronomy. 2021; 11: 1193.
35. [35]. Gadelha CG., Coutinho ÍAC., Pinheiro SK de P., et al. Sodium Uptake and Transport Regulation, and Photosynthetic Efficiency Maintenance as the Basis of Differential Salt Tolerance in Rice Cultivars. Environmental and Experimental Botany. 2021; 192: 104654.
36. [36]. Chen F., Chen S., Guo W., et al. Salt Tolerance Identification of Three Species of Chrysanthemums. Acta Horticulturae 2003; 618: 299–305.
37. [37]. Orcan P. Tuz Stresine Maruz Bırakılan Çeltik (Oryza sativa L.) Çeşitlerinde Radikal Söndürme ve Antioksidan Enzim Aktiviteleri, Dicle Üniversitesi Fen Bilimleri Enstitüsü http://acikerisim.dicle.edu.tr/xmlui/handle/11468/3582 (2017, accessed 1 August 2024).
38. [38]. Alharby HF., Al-Zahrani HS., Hakeem KR., et al. Identification of Physiological and Biochemical Markers for Salt (NaCl) Stress in the Seedlings of Mungbean [Vigna radiata (L.) Wilczek] genotypes. Saudi Journal of Biological Science. 2019; 26: 1053–1060.
39. [39]. Munns R., Tester M. Mechanisms of Salinity Tolerance. Annual Review of Plant Biology 2008; 59: 651–681.
40. [40]. Hu C hong, Zheng Y., Tong C ling, et al. Effects of Exogenous Melatonin on Plant Growth, Root Hormones and Photosynthetic Characteristics of Trifoliate Orange Subjected to Salt Stress. Plant Growth Regulation. 2022; 97: 551–558.
41. [41]. Mohamed HI., Latif HH. Improvement of Drought Tolerance of Soybean Plants by Using Methyl Jasmonate. Physiology and Molecular Biology of Plants. 2017; 23: 545–556.
42. [42]. Meriç S., Ayan A., Atak Ç. Molecular Abiotic Stress Tolerans Strategies: From Genetic Engineering to Genome Editing Era. Abiotic Stress Plants. 2020. DOI: 10.5772/Intechopen.94505.
43. [43]. Chunthaburee S., Dongsansuk A., Sanitchon J., et al. Physiological and Biochemical Parameters for Evaluation and Clustering of Rice Cultivars Differing in Salt Tolerance at Seedling Stage. Saudi Journal of Biological Sciences. 2016; 23: 467–477.
44. [44]. Suzuki N., Koussevitzky S., Mittler R., et al. ROS and Redox Signalling in the Response of Plants to Abiotic Stress. Plant Cell & Environment. 2012; 35: 259–270.
45. [45]. Rasel M., Tahjib-Ul-Arif M., Hossain MA., et al. Discerning of Rice Landraces (Oryza sativa L.) for Morpho-physiological, Antioxidant Enzyme Activity, and Molecular Markers’ Responses to Induced Salt Stress at the Seedling Stage. Journal of Plant Growth Regulation. 2020; 39: 41–59.
46. [46]. Khan MH., Panda SK. Alterations in Root Lipid Peroxidation and Antioxidative Responses in Two Rice Cultivars Under NaCl-salinity Stress. Acta Physiologiae Plantarum. 2008; 30: 81–89.
47. [47]. Singh A., Sengar RS., Shahi UP., et al. Prominent Effects of Zinc Oxide Nanoparticles on Roots of Rice (Oryza sativa L.) Grown under Salinity Stress. Stresses. 2023; 3: 33–46.
48. [48]. Hossen MS., Karim MF., Fujita M., et al. Comparative Physiology of Indica and Japonica Rice under Salinity and Drought Stress: An Intrinsic Study on Osmotic Adjustment, Oxidative Stress, Antioxidant Defense and Methylglyoxal Detoxification. Stresses 2022; 2: 156–178.
49. [49]. Wu J., Yu C., Huang L., et al. A Rice Transcription Factor, OsMADS57, Positively Regulates High Salinity Tolerance in Transgenic Arabidopsis thaliana and Oryza sativa plants. Physiologia Plantarum 2021; 173: 1120–1135.
50. [50]. Çelik Ö., Çakır BC., Atak Ç. Identification of the Antioxidant Defense Genes Which May Provide Enhanced Salt Tolerance in Oryza sativa L. Physiology and Molecular Biology of Plants. 2019; 25: 85–99.
51. [51]. Ramon M., Rolland F., Thevelein JM., et al. ABI4 Mediates the Effects of Exogenous Trehalose on Arabidopsis Growth and Starch Breakdown. Plant Molecular Biology 2007. 63: 195–206.
52. [52]. Saidi A., Hajibarat Z. Computatıonal Analysis and Expression Study of Trehalose 6-Phosphate Synthase (TPS) in Rice (Oryza sativa), http://bar.utoronto.ca/welcome.htm (2021, accessed 5 August 2024).
53. [53]. Lu X., Liu X., Xu J., et al. Strigolactone-Mediated Trehalose Enhances Salt Resistance in Tomato Seedlings. Horticulturae. 2023; 9: 770.
54. [54]. Li HW., Zang BS., Deng XW., et al. Overexpression of the Trehalose-6-Phosphate Synthase Gene OsTPS1 Enhances Abiotic Stress Tolerance in Rice. Planta. 2011; 234: 1007–1018.
55. [55]. Avonce N., Leyman B., Mascorro-Gallardo JO., et al. The Arabidopsis Trehalose-6-P Synthase AtTPS1 Gene is a Regulator of Glucose, Abscisic Acid, and Stress Signaling. Plant Physiol 2004; 136: 3649–3659.
56. [56]. Fukuda A., Nakamura A., Tagiri A., et al. Function, Intracellular Localization and the Importance in Salt Tolerance of a Vacuolar Na+/H+ Antiporter from Rice. Plant and Cell Physiology. 2004; 45: 146–159.
57. [57]. Chen M., Chen QJ., Niu XG., et al. Expression of OsNHX1 Gene in Maize Confers Salt Tolerance and Promotes Plant Growth in the Field. Plant, Soil and Environment. 2007; 53: 490–498.
58. [58]. Yarra R. The Wheat NHX Gene Family: Potential Role in Improving Salinity Stress Tolerance of Plants. Plant Gene 2019; 18: 100178.
59. [59]. Pabuayon ICM., Jiang J., Qian H., et al. Gain-of-function Mutations of AtNHX1 Suppress SOS1 Salt Sensitivity and Improve Salt Tolerance in Arabidopsis. Stress Biology. 2021; 1: 1–19.
60. [60]. Liu M., Song X., Jiang Y. Growth, Ionic Response, and Gene Expression of Shoots and Roots of Perennial Ryegrass Under Salinity Stress. Acta Physiologiae Plantarum. 2018; 40: 1–8.
61. [61]. Silva EN., Silveira JAG., Rodrigues CRF., et al. Physiological Adjustment to Salt Stress in Jatropha curcas is Associated With Accumulation of Salt Ions, Transport and Selectivity of K+, Osmotic Adjustment and K+/Na+ Homeostasis. Plant Biology. 2015; 17: 1023–1029.
62. [62]. Zhang Y., Fang J., Wu X., et al. Na+/K+ Balance and Transport Regulatory Mechanisms in Weedy and Cultivated Rice (Oryza sativa L.) Under Salt Stress. BMC Plant Biology. 2018; 18: 1–14.
63. [63]. Qiu QS., Guo Y., Dietrich MA., et al. Regulation of SOS1, A Plasma Membrane Na+/H+ Exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proceedings of the National Academy of Sciences. 2002; 99: 8436–8441.
64. [64]. Shi H., Quintero FJ., Pardo JM., et al. The Putative Plasma Membrane Na+/H+ Antiporter SOS1 Controls Long-Distance Na+ Transport in Plants. Plant Cell. 2002; 14: 465–477.
65. [65]. Calzone A., Cotrozzi L., Pellegrini E., et al. Can the Transcriptional Regulation of NHX1, SOS1 and HKT1 Genes Handle the Response of Two Pomegranate Cultivars to Moderate Salt Stress?: Salt-tolerance of Two Pomegranate Cultivars. Scientia Horticulturae. 2021; 288: 110309.
66. [66]. Wu H. Plant Salt Tolerance and Na+ Sensing and Transport. Crop Journal. 2018; 6: 215–225.
67. [67]. Omisun T., Sahoo S., Saha B., et al. Relative Salinity Tolerance of Rice Cultivars Native to North East India: A Physiological, Biochemical and Molecular Perspective. Protoplasma. 2018; 255: 193–202.
68. [68]. Theerawitaya C., Tisarum R., Samphumphuang T., et al. Expression Levels of the Na+/K+ Transporter OsHKT2;1 and Vacuolar Na+/H+ Exchanger OsNHX1, Na Enrichment, Maintaining the Photosynthetic Abilities and Growth Performances of Indica Rice Seedlings Under Salt Stress. Physiology and Molecular Biology of Plants. 2020; 26: 513–523.