Skip to main content
SpringerLink
Log in

Over-expression of a DUF1644 protein gene, SIDP361, enhances tolerance to salt stress in transgenic rice

  • Original Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

Salt stress has adverse effects on the growth and production of rice crops. In this study, we isolated and characterized SIDP361, which encodes a DUF1644 family protein. This gene was expressed in various rice tissues and was induced by high salt (200 mM NaCl), dehydration, and abscisic acid (100 µM ABA) treatments. Stable expression of SIDP361-GFP in rice cells suggested that SIDP361 is a cytoplasmic protein. When compared with the untransformed wild-type (WT) control, transgenic plants over-expressing SIDP361 exhibited significantly improved tolerance to salt stress at both the seedling and heading stages. Under salinity conditions, the transgenics also had elevated amounts of free proline. Moreover, transcript levels for genes encoding proline synthetase enzymes were significantly higher in transformants than in the WT. The transgenic lines were also hypersensitive to exogenous ABA. Quantitative real-time PCR analysis showed that transcription of several stressrelated genes was greater in SIDP361-overexpressing plants than in the WT under both normal and salt-stressed conditions. These results demonstrate that SIDP361 has high potential as a tool for genetically improving salt tolerance in rice.

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

Similar content being viewed by others

References

  • Abraham E, Rigo G, Szekely G, Nagy R, Koncz C, Szabados L (2003) Light-dependent induction of proline biosynthesis by abscisic acid and salt stress is inhibited by brassinosteroid in Arabidopsis. Plant Mol Biol 51:363–372

    Article  CAS  PubMed  Google Scholar 

  • Bateman A, Birney E, Cerruti L, Durbin R, Etwiller L, Eddy SR, Griffiths-Jones S, Howe KL, Marshall M, Sonnhammer EL (2002) The Pfam protein families database. Nucleic Acids Res 30:276–280

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bates L, Waldren R, Teare I (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Bohnert HJ, Shen B (1998) Transformation and compatible solutes. Scientia Hort 78:237–260

    Article  Google Scholar 

  • Boyer JS (1982) Plant productivity and environment. Science 218:443–448

    Article  CAS  PubMed  Google Scholar 

  • Bray EA (1997) Plant responses to water deficit. Trends Plant Sci 2:48–54

    Article  Google Scholar 

  • Cantrell RP, Reeves TG (2002) The rice genome. The cereal of the world's poor takes center stage. Science 296:53

    Article  CAS  PubMed  Google Scholar 

  • Chen WJ, Zhu T (2004) Networks of transcription factors with roles in environmental stress response. Trends Plant Sci 9:591–596

    Article  CAS  PubMed  Google Scholar 

  • Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451

    Article  CAS  PubMed  Google Scholar 

  • Cushman JC, Bohnert HJ (2000) Genomic approaches to plant stress tolerance. Curr Opin Plant Biol 3:117–124

    Article  CAS  PubMed  Google Scholar 

  • Diamant S, Eliahu N, Rosenthal D, Goloubinoff P (2001) Chemical chaperones regulate molecular chaperones in vitro and in cells under combined salt and heat stresses. J Biol Chem 276:39586–39591

    Article  CAS  PubMed  Google Scholar 

  • Du H, Wang N, Cui F, Li X, Xiao J, Xiong L (2010) Characterization of the beta-carotene hydroxylase gene DSM2 conferring drought and oxidative stress resistance by increasing xanthophylls and abscisic acid synthesis in rice. Plant Physiol 154:1304–1318

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, Miura S, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt-and cold-responsive gene expression. Plant J 33:751–763

    Article  CAS  PubMed  Google Scholar 

  • Finkelstein RR, Gampala SS, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14 Suppl:S15–45

    PubMed Central  CAS  PubMed  Google Scholar 

  • Gao J-P, Chao D-Y, Lin H-X (2008) Toward understanding molecular mechanisms of abiotic stress responses in rice. Rice 1:36–51

    Article  Google Scholar 

  • Hare P, Cress W, van Staden J (1998) Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ 21:535–553

    Article  CAS  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499

    Article  CAS  PubMed  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27:297–300

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Himmelbach A, Yang Y, Grill E (2003) Relay and control of abscisic acid signaling. Curr Opin Plant Biol 6:470–479

    Article  CAS  PubMed  Google Scholar 

  • Hofgen R, Willmitzer L (1988) Storage of competent cells for Agrobacterium transformation. Nucleic Acids Res 16:9877

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hong Z, Lakkineni K, Zhang Z, Verma DP (2000) Removal of feedback inhibition of delta(1)-pyrroline-5-carboxylate synthetase results in increased proline accumulation and protection of plants from osmotic stress. Plant Physiol 122:1129–1136

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hu H, Dai M, Yao J, Xiao B, Li X, Zhang Q, Xiong L (2006) Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci USA 103:12987–12992

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hu H, You J, Fang Y, Zhu X, Qi Z, Xiong L (2008) Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice. Plant Mol Biol 67:169–181

    Article  CAS  PubMed  Google Scholar 

  • Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47:377–403

    Article  CAS  PubMed  Google Scholar 

  • Iuchi S, Kobayashi M, Taji T, Naramoto M, Seki M, Kato T, Tabata S, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K (2001) Regulation of drought tolerance by gene manipulation of 9-cisepoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J 27:325–333

    Article  CAS  PubMed  Google Scholar 

  • Jan A, Maruyama K, Todaka D, Kidokoro S, Abo M, Yoshimura E, Shinozaki K, Nakashima K, Yamaguchi-Shinozaki K (2013) OsTZF1, a CCCH-tandem zinc finger protein, confers delayed senescence and stress tolerance in rice by regulating stressrelated genes. Plant Physiol 161:1202–1216

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Karimi M, Inze D, Depicker A (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7:193–195

    Article  CAS  PubMed  Google Scholar 

  • Khush GS (1997) Origin, dispersal, cultivation and variation of rice. Plant Mol Biol 35:25–34

    Article  CAS  PubMed  Google Scholar 

  • Kim SJ, Ryu MY, Kim WT (2012) Suppression of Arabidopsis RING-DUF1117 E3 ubiquitin ligases, AtRDUF1 and AtRDUF2, reduces tolerance to ABA-mediated drought stress. Biochem Biophys Res Comm 420:141–147

    Article  CAS  PubMed  Google Scholar 

  • Knight H, Knight MR (2001) Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci 6:262–267

    Article  CAS  PubMed  Google Scholar 

  • Leung J, Giraudat J (1998) Abscisic acid signal transduction. Annu Rev Plant Physiol Plant Mol Biol 49:199–222

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Martinez-Atienza J, Jiang X, Garciadeblas B, Mendoza I, Zhu JK, Pardo JM, Quintero FJ (2007) Conservation of the salt overly sensitive pathway in rice. Plant Physiol 143:1001–1012

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Matsukura S, Mizoi J, Yoshida T, Todaka D, Ito Y, Maruyama K, Shinozaki K, Yamaguchi-Shinozaki K (2010) Comprehensive analysis of rice DREB2-type genes that encode transcription factors involved in the expression of abiotic stress-responsive genes. Mol Genet Genom 283:185–196

    Article  CAS  Google Scholar 

  • McNeil SD, Nuccio ML, Hanson AD (1999) Betaines and related osmoprotectants. Targets for metabolic engineering of stress resistance. Plant Physiol 120:945–950

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Medina J, Bargues M, Terol J, Pérez-Alonso M, Salinas J (1999) The Arabidopsis CBF gene family is composed of three genes encoding AP2 domain-containing proteins whose expression is regulated by low temperature but not by abscisic acid or dehydration. Plant Physiol 119:463–470

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mundy J, Chua NH (1988) Abscisic acid and water-stress induce the expression of a novel rice gene. EMBO J 7:2279–2286

    PubMed Central  CAS  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56:165–185

    Article  CAS  PubMed  Google Scholar 

  • Nishimura A, Aichi I, Matsuoka M (2006) A protocol for Agrobacterium-mediated transformation in rice. Nat Protoc 1:2796–2802

    Article  CAS  PubMed  Google Scholar 

  • Prasad S, Bagali P, Hittalmani S, Shashidhar H (2000) Molecular mapping of quantitative trait loci associated with seedling tolerance to salt stress in rice (Oryza sativa L.). Curr Sci 78:162–164

    CAS  Google Scholar 

  • Sakuma Y, Maruyama K, Osakabe Y, Qin F, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in droughtresponsive gene expression. Plant Cell 18:1292–1309

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3:217–223

    Article  CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227

    Article  CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417

    Article  CAS  PubMed  Google Scholar 

  • Skriver K, Mundy J (1990) Gene expression in response to abscisic acid and osmotic stress. Plant Cell 2:503–512

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Song SY, Chen Y, Chen J, Dai XY, Zhang WH (2011) Physiological mechanisms underlying OsNAC5-dependent tolerance of rice plants to abiotic stress. Planta 234:331–345

    Article  CAS  PubMed  Google Scholar 

  • Sperotto RA, Ricachenevsky FK, Duarte GL, Boff T, Lopes KL, Sperb ER, Grusak MA, Fett JP (2009) Identification of upregulated genes in flag leaves during rice grain filling and characterization of OsNAC5, a new ABA-dependent transcription factor. Planta 230:985–1002

    Article  CAS  PubMed  Google Scholar 

  • Takasaki H, Maruyama K, Kidokoro S, Ito Y, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K, Nakashima K (2010) The abiotic stress-responsive NAC-type transcription factor OsNAC5 regulates stress-inducible genes and stress tolerance in rice. Mol Genet Genom 284:173–183

    Article  CAS  Google Scholar 

  • Thomashow MF (1998) Role of cold-responsive genes in plant freezing tolerance. Plant Physiol 118:1–8

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Troll W, Lindsley J (1955) A photometric method for the determination of proline. J Biol Chem 215:655–660

    CAS  PubMed  Google Scholar 

  • Tyagi AK, Mohanty A (2000) Rice transformation for crop improvement and functional genomics. Plant Sci 158:1–18

    Article  CAS  PubMed  Google Scholar 

  • Tyagi AK, Mohanty A, Bajaj S, Chaudhury A, Maheshwari SC (1999) Transgenic rice: A valuable monocot system for crop improvement and gene research. Crit Rev Biotechnol 19:41–79

    Article  CAS  Google Scholar 

  • Vierling E, Kimpel JA (1992) Plant responses to environmental stress. Curr Opin Biotechnol 3:164–170

    Article  CAS  PubMed  Google Scholar 

  • Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14

    Article  CAS  PubMed  Google Scholar 

  • Wrzaczek M, Brosché M, Salojärvi J, Kangasjärvi S, Idänheimo N, Mersmann S, Robatzek S, Karpiñski S, Karpiñska B, Kangasjärvi J (2010) Transcriptional regulation of the CRK/DUF26 group of receptor-like protein kinases by ozone and plant hormones in Arabidopsis. BMC Plant Biol 10:95

    Article  PubMed Central  PubMed  Google Scholar 

  • Xiao B, Huang Y, Tang N, Xiong L (2007) Over-expression of a LEA gene in rice improves drought resistance under the field conditions. Theor Appl Genet 115:35–46

    Article  CAS  PubMed  Google Scholar 

  • Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14 Suppl:S165–183

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cisacting regulatory elements in osmotic-and cold-stress-responsive promoters. Trends Plant Sci 10:88–94

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Klueva N, Wang Z, Wu R, Ho T-H, Nguyen H (2000) Genetic engineering for abiotic stress resistance in crop plants. In Vitro Cell Dev Biol-Plant 36:108–114

    Article  CAS  Google Scholar 

  • Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71

    Article  CAS  PubMed  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Xiamen Key Laboratory for Plant Genetics, School of Life Sciences, Xiamen University, Xiamen, 361005, China

    Min Li, Chiming Guo & Liang Chen

  2. Key Laboratory of Integrated Pest Management on Tropical Crops, Ministry of Agriculture, Environment and Plant Protection Institute, Chinese Academy of Tropical Agricultural Sciences, Danzhou, Hainan, 571737, China

    Lijia Guo

  3. Department of Genetics and Biochemistry, Clemson University, Clemson, SC, 29634, USA

    Liangjiang Wang

Authors
  1. Min Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lijia Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chiming Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Liangjiang Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Liang Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Liang Chen.

Additional information

These authors contributed equally to the paper.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, M., Guo, L., Guo, C. et al. Over-expression of a DUF1644 protein gene, SIDP361, enhances tolerance to salt stress in transgenic rice. J. Plant Biol. 59, 62–73 (2016). https://doi.org/10.1007/s12374-016-0180-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-016-0180-7

Key words

Search

Navigation