Journal of Plant Research

, Volume 131, Issue 1, pp 191–202 | Cite as

Effects of acute salt stress on modulation of gene expression in a Malaysian salt-tolerant indigenous rice variety, Bajong

  • Brandon Pei Hui Yeo
  • Mrinal Bhave
  • Siaw San Hwang
Regular Paper


The small genome size of rice relative to wheat and barley, together with its salt sensitivity, make it an ideal candidate for studies of salt stress response. Transcriptomics has emerged as a powerful technique to study salinity responses in many crop species. By identifying a large number of differentially expressed genes (DEGs) simultaneously after the stress induction, it can provide crucial insight into the immediate responses towards the stressor. In this study, a Malaysian salt-tolerant indigenous rice variety named Bajong and one commercial rice variety named MR219 were investigated for their performance in plant growth and ion accumulation properties after salt stress treatment. Bajong was further investigated for the changes in leaf’s transcriptome after 6 h of stress treatment using 100 mM NaCl. Based on the results obtained, Bajong is found to be significantly more salt tolerant than MR219, showing better growth and a lower sodium ion accumulation after the stress treatment. Additionally, Bajong was analysed by transcriptomic sequencing, generating a total of 130 millions reads. The reads were assembled into de novo transcriptome and each transcript was annotated using several pre-existing databases. The transcriptomes of control and salt-stressed samples were then compared, leading to the discovery of 4096 DEGs. Based on the functional annotation results obtained, the enrichment factor of each functional group in DEGs was calculated in relation to the total reads obtained. It was found that the group with the highest gene modulation was involved in the secondary metabolite biosynthesis of plants, with approximately 2.5% increase in relation to the total reads obtained. This suggests an extensive transcriptional reprogramming of the secondary metabolic pathways after stress induction, which could be directly responsible for the salt tolerance capability of Bajong.


mRNA-seq Wild rice variety Antioxidant content Salt stress Plant phytochemicals 



Clusters of orthologous groups


Differentially expressed genes


Di(phenyl)-(2,4,6-trinitrophenyl) iminoazanium


Genetically modified organism


Gene ontology


Kyoto encyclopedia of gene and genome


Late embryogenesis abundant


Reactive oxygen species


Relative water content


Salt overly sensitive


Total flavonoid content


Total phenolic content



We greatly thank Swinburne University of Technology Sarawak Campus for providing the Strategic Research Grant (StraRG 2-5605).

Compliance with ethical standards

Conflict of interest

The authors declare that there is no conflict of interest.

Supplementary material

10265_2017_977_MOESM1_ESM.xlsx (49 kb)
Supplementary material 1 (XLSX 50 KB)


  1. Aronson JA (1989) HALOPH: a data base of salt tolerant plants of the world. Office of Arid Land Studies, University of Arizona, Tuscon, AZGoogle Scholar
  2. Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216CrossRefGoogle Scholar
  3. Bharti N, Yadav D, Barnawal D, Maji D, Kalra A (2013) Exiguobacterium oxidotolerans, a halotolerant plant growth promoting rhizobacteria, improves yield and content of secondary metabolites in Bacopa monnieri (L.) Pennell under primary and secondary salt stress. World J Microbiol Biotechnol 29:379–387CrossRefPubMedGoogle Scholar
  4. Bohnert HJ, Ayoubi P, Borchert C, Bressan RA, Burnap RL, Cushman JC, Cushman MA, Deyholos M, Fischer R, Galbraith DW (2001) A genomics approach towards salt stress tolerance. Plant Physiol Biochem 39:295–311CrossRefGoogle Scholar
  5. Brondani C, Borba TCO, Rangel PHN, Brondani RPV (2006) Determination of genetic variability of traditional varieties of Brazilian rice using microsatellite markers. Genet Mol Biol 29:676–684CrossRefGoogle Scholar
  6. D’Auria JC, Gershenzon J (2005) The secondary metabolism of Arabidopsis thaliana: growing like a weed. Curr Opin Plant Biol 8:308–316CrossRefPubMedGoogle Scholar
  7. Dharmawardhana P, Ren L, Amarasinghe V, Monaco M, Thomason J, Ravenscroft D, McCouch S, Ware D, Jaiswal P (2013) A genome scale metabolic network for rice and accompanying analysis of tryptophan, auxin and serotonin biosynthesis regulation under biotic stress. Rice 6:1–15CrossRefGoogle Scholar
  8. Garg R, Verma M, Agrawal S, Shankar R, Majee M, Jain M (2014) Deep transcriptome sequencing of wild halophyte rice, Porteresia coarctata, provides novel insights into the salinity and submergence tolerance factors. DNA Res 21:69–84CrossRefPubMedGoogle Scholar
  9. Gilroy S, Suzuki N, Miller G, Choi WG, Toyota M, Devireddy AR, Mittler R (2014) A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling. Trends Plant Sci 19:623–630CrossRefPubMedGoogle Scholar
  10. Golldack D, Li G, Mohan H, Probst N (2014) Tolerance to drought and salt stress in plants: unraveling the signaling networks. Mol Genet Genom 1:15–25Google Scholar
  11. Gou JY, Yu XH, Liu CJ (2009) A hydroxycinnamoyltransferase responsible for synthesizing suberin aromatics in Arabidopsis. Proc Natl Acad Sci USA 106:18,855–18,860CrossRefGoogle Scholar
  12. Herald TJ, Gadgil P, Tilley M (2012) High-throughput micro plate assays for screening flavonoid content and DPPH-scavenging activity in sorghum bran and flour. J Sci Food Agric 92:2,326–2,331CrossRefGoogle Scholar
  13. Hernández JA, Corpas FJ, Gomez M, Río LA, Sevilla F (1993) Salt-induced oxidative stress mediated by activated oxygen species in pea leaf mitochondria. Physiol Plant 89:103–110CrossRefGoogle Scholar
  14. Ismail C (2005) The role of potassium in alleviating detrimental effects of abiotic stresses in plants. J Plant Nutr Soil Sci 168:521–530CrossRefGoogle Scholar
  15. Joshi SH, Gupta VS, Aggarwal RK, Ranjekar PK, Brar DS (2000) Genetic diversity and phylogenetic relationship as revealed by inter simple sequence repeat (ISSR) polymorphism in the genus Oryza. Theor Appl Genet 100:1,311–1,320CrossRefGoogle Scholar
  16. Kim JH, Kim WT (2013) The Arabidopsis RING E3 ubiquitin ligase AtAIRP3/LOG2 participates in positive regulation of high-salt and drought stress responses. Plant Physiol Biochem 162:1,733–1,749Google Scholar
  17. Lee HH, Neoh PPN, Bong WST, Puvaneswaran J, Wong SC, Yiu PH, Rajan A (2011) Genotyping of Sarawak rice cultivars using microsatellite markers. Pertan J Trop Agric Sci 34:123–136Google Scholar
  18. Leigh RA, Wyn Jones RG (1984) A hypothesis relating critical potassium concentrations for growth to the distribution and functions of this ion in the plant cell. New Phytol 97:1–3CrossRefGoogle Scholar
  19. Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinf 12:323CrossRefGoogle Scholar
  20. Li T, Li H, Zhang YX, Liu JY (2011) Identification and analysis of seven H2O2-responsive miRNAs and 32 new miRNAs in the seedlings of rice (Oryza sativa L. subsp. indica). Nucleic Acids Res 39:2,821–2,833CrossRefGoogle Scholar
  21. Li L, Li N, Song SF, Li YX, Xia XJ, Fu XQ, Chen GH, Deng HF (2014) Cloning and characterization of the drought-resistance OsRCI2-5 gene in rice (Oryza sativa L.). GMR Genet Mol Res 13:4,022–4,035CrossRefGoogle Scholar
  22. Lugan R, Niogret MF, Kervazo L, Larher FR, Kopka J, Bouchereau A (2009) Metabolome and water status phenotyping of Arabidopsis under abiotic stress cues reveals new insight into ESK1 function. Plant Cell Environ 32:95–108CrossRefPubMedGoogle Scholar
  23. Mandhania S, Madan S, Sawhney V (2006) Antioxidant defense mechanism under salt stress in wheat seedlings. Biol Plant 50:227–231CrossRefGoogle Scholar
  24. Mekawy AM, Assaha DV, Yahagi H, Tada Y, Ueda A, Saneoka H. Growth (2015) Physiological adaptation, and gene expression analysis of two Egyptian rice cultivars under salt stress. Plant Physiol Biochem 87:17–25CrossRefPubMedGoogle Scholar
  25. Meloni DA, Gulotta MR, Martínez CA, Oliva MA (2004) The effects of salt stress on growth, nitrate reduction and proline and glycinebetaine accumulation in Prosopis alba. Braz J Plant Physiol 16:39–46CrossRefGoogle Scholar
  26. Menzel U, Lieth H (2003) HALOPHYTE Database Ver. 2.0 update. In: Cash crop halophytes, pp 221–223Google Scholar
  27. Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250CrossRefPubMedGoogle Scholar
  28. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681CrossRefPubMedGoogle Scholar
  29. Rahman MA, Thomson MJ, Shah-E-Alam M, de Ocampo M, Egdane J, Ismail AM (2016) Exploring novel genetic sources of salinity tolerance in rice through molecular and physiological characterization. Ann Bot 117:1,083–1,097CrossRefGoogle Scholar
  30. Ren HY, Wei Q (2015) Isolation and functional analysis of phosphate-responsive gene OsRCI2-9 in Oryza sativa. Zhongguo Nongye Kexue 48:831–840Google Scholar
  31. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1,101–1,108CrossRefGoogle Scholar
  32. Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Vitic 16:144–158Google Scholar
  33. Smart RE, Bingham GE (1974) Rapid estimates of relative water content. Plant Physiol 53:258–260CrossRefPubMedPubMedCentralGoogle Scholar
  34. Tavakkoli E, Rengasamy P, McDonald GK (2010) High concentrations of Na+ and Cl ions in soil solution have simultaneous detrimental effects on growth of faba bean under salinity stress. J Exp Biol 61:4,449–4,459Google Scholar
  35. Tester M, Davenport R (2003) Sodium ion tolerance and sodium ion transport in higher plants. Ann Bot 91:503–527CrossRefPubMedPubMedCentralGoogle Scholar
  36. Thomson WW (1975) The structure and function of salt glands. Plants Saline Environ 1:118–146CrossRefGoogle Scholar
  37. Van Poecke RM, Posthumus MA, Dicke M (2001) Herbivore-induced volatile production by Arabidopsis thaliana leads to attraction of the parasitoid Cotesia rubecula: chemical, behavioral, and gene-expression analysis. J Chem Ecol 27:1,911–1,928CrossRefGoogle Scholar
  38. Walia H, Wilson C, Condamine P, Liu X, Ismail AM, Zeng L, Wanamaker SI, Mandal J, Xu J, Cui X, Close TJ (2005) Comparative transcriptional profiling of two contrasting rice genotypes under salinity stress during the vegetative growth stage. Plant Physiol 139:822–835CrossRefPubMedPubMedCentralGoogle Scholar
  39. Wang M, Zheng Q, Shen Q, Guo S (2013) The critical role of potassium in plant stress response. Int J Mol Sci 14:7,370–7,390CrossRefGoogle Scholar
  40. Winkel-Shirley B (2002) Biosynthesis of flavonoids and effects of stress. Curr Opin Plant Biol 5:218–223CrossRefPubMedGoogle Scholar
  41. Yeo AR, Flowers TJ (1984) Nonosmotic effects of polyethylene glycols upon sodium transport and sodium-potassium selectivity by rice roots. Plant Physiol 75:298–303CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan KK 2017

Authors and Affiliations

  • Brandon Pei Hui Yeo
    • 1
  • Mrinal Bhave
    • 2
  • Siaw San Hwang
    • 1
  1. 1.Faculty of Engineering, Computing and ScienceSwinburne University of Technology Sarawak CampusKuchingMalaysia
  2. 2.Faculty of Science, Engineering and TechnologySwinburne University of TechnologyHawthornAustralia

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