Skip to main content
SpringerLink
Log in

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

  • Regular Paper
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

COG:

Clusters of orthologous groups

DEGs:

Differentially expressed genes

DPPH:

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

GMO:

Genetically modified organism

GO:

Gene ontology

KEGG:

Kyoto encyclopedia of gene and genome

LEA:

Late embryogenesis abundant

ROS:

Reactive oxygen species

RWC:

Relative water content

SOS:

Salt overly sensitive

TFC:

Total flavonoid content

TPC:

Total phenolic content

References

  • Aronson JA (1989) HALOPH: a data base of salt tolerant plants of the world. Office of Arid Land Studies, University of Arizona, Tuscon, AZ

  • Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216

    Article  CAS  Google Scholar 

  • 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 29:379–387

    Article  CAS  PubMed  Google Scholar 

  • 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 39:295–311

    Article  CAS  Google Scholar 

  • 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 29:676–684

    Article  CAS  Google Scholar 

  • D’Auria JC, Gershenzon J (2005) The secondary metabolism of Arabidopsis thaliana: growing like a weed. Curr Opin Plant Biol 8:308–316

    Article  PubMed  Google Scholar 

  • 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 6:1–15

    Article  Google Scholar 

  • 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 21:69–84

    Article  CAS  PubMed  Google Scholar 

  • 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 19:623–630

    Article  CAS  PubMed  Google Scholar 

  • Golldack D, Li G, Mohan H, Probst N (2014) Tolerance to drought and salt stress in plants: unraveling the signaling networks. Mol Genet Genom 1:15–25

    Google Scholar 

  • Gou JY, Yu XH, Liu CJ (2009) A hydroxycinnamoyltransferase responsible for synthesizing suberin aromatics in Arabidopsis. Proc Natl Acad Sci USA 106:18,855–18,860

    Article  CAS  Google Scholar 

  • 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 92:2,326–2,331

    Article  CAS  Google Scholar 

  • 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 89:103–110

    Article  Google Scholar 

  • Ismail C (2005) The role of potassium in alleviating detrimental effects of abiotic stresses in plants. J Plant Nutr Soil Sci 168:521–530

    Article  Google Scholar 

  • 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 100:1,311–1,320

    Article  CAS  Google Scholar 

  • 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 162:1,733–1,749

    CAS  Google Scholar 

  • 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 34:123–136

    Google Scholar 

  • 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 97:1–3

    Article  CAS  Google Scholar 

  • Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinf 12:323

    Article  CAS  Google Scholar 

  • 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 39:2,821–2,833

    Article  CAS  Google Scholar 

  • 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 13:4,022–4,035

    Article  CAS  Google Scholar 

  • 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 32:95–108

    Article  CAS  PubMed  Google Scholar 

  • Mandhania S, Madan S, Sawhney V (2006) Antioxidant defense mechanism under salt stress in wheat seedlings. Biol Plant 50:227–231

    Article  CAS  Google Scholar 

  • 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 87:17–25

    Article  CAS  PubMed  Google Scholar 

  • 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 16:39–46

    Article  CAS  Google Scholar 

  • Menzel U, Lieth H (2003) HALOPHYTE Database Ver. 2.0 update. In: Cash crop halophytes, pp 221–223

  • Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250

    Article  CAS  PubMed  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  CAS  PubMed  Google Scholar 

  • 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 117:1,083–1,097

    Article  Google Scholar 

  • Ren HY, Wei Q (2015) Isolation and functional analysis of phosphate-responsive gene OsRCI2-9 in Oryza sativa. Zhongguo Nongye Kexue 48:831–840

    CAS  Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1,101–1,108

    Article  CAS  Google Scholar 

  • Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Vitic 16:144–158

    CAS  Google Scholar 

  • Smart RE, Bingham GE (1974) Rapid estimates of relative water content. Plant Physiol 53:258–260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 61:4,449–4,459

    CAS  Google Scholar 

  • Tester M, Davenport R (2003) Sodium ion tolerance and sodium ion transport in higher plants. Ann Bot 91:503–527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomson WW (1975) The structure and function of salt glands. Plants Saline Environ 1:118–146

    Article  Google Scholar 

  • 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 27:1,911–1,928

    Article  Google Scholar 

  • 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 139:822–835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang M, Zheng Q, Shen Q, Guo S (2013) The critical role of potassium in plant stress response. Int J Mol Sci 14:7,370–7,390

    Article  CAS  Google Scholar 

  • Winkel-Shirley B (2002) Biosynthesis of flavonoids and effects of stress. Curr Opin Plant Biol 5:218–223

    Article  CAS  PubMed  Google Scholar 

  • Yeo AR, Flowers TJ (1984) Nonosmotic effects of polyethylene glycols upon sodium transport and sodium-potassium selectivity by rice roots. Plant Physiol 75:298–303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

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

Author information

Authors and Affiliations

  1. Faculty of Engineering, Computing and Science, Swinburne University of Technology Sarawak Campus, Jalan Simpang Tiga, 93350, Kuching, Sarawak, Malaysia

    Brandon Pei Hui Yeo & Siaw San Hwang

  2. Faculty of Science, Engineering and Technology, Swinburne University of Technology, PO Box 218, Hawthorn, VIC, 3122, Australia

    Mrinal Bhave

Authors
  1. Brandon Pei Hui Yeo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mrinal Bhave
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Siaw San Hwang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Siaw San Hwang.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 50 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yeo, B.P.H., Bhave, M. & Hwang, S.S. Effects of acute salt stress on modulation of gene expression in a Malaysian salt-tolerant indigenous rice variety, Bajong. J Plant Res 131, 191–202 (2018). https://doi.org/10.1007/s10265-017-0977-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-017-0977-6

Keywords

Search

Navigation