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Expression of Bruguiera gymnorhiza BgARP1 enhances salt tolerance in transgenic Arabidopsis plants

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Abstract

We have previously reported that expression of salt-responsive genes, including Bruguiera gymnorhiza ankyrin repeat protein 1 (BgARP1), enhances salt tolerance in both Agrobacterium tumefaciens and Arabidopsis. In this report, we further characterized BgARP1-expressing Arabidopsis to elucidate the role of BgARP1 in salt tolerance. BgARP1-expressing plants exhibited more vigorous growth than wild-type plants on MS plates containing 125–175 mM NaCl. Real-time PCR analysis showed enhanced induction of osmotin34 in the 2-week-old transformants under 125 mM NaCl. It was also showed that induction of typical salt-responsive genes, including RD29A, RD29B, and RD22, was blunted and delayed in the 4-week-old transformants during 24 h after 200 mM NaCl treatment. Ion content analysis showed that transgenic plants contained more K+, Ca2+, and NO3 , and less NH4 +, than wild-type plants grown in 200 mM NaCl. Our results suggest that BgARP1-expressing plants may reduce salt stress by up-regulating osmotin34 gene expression and maintaining K+ homeostasis and regulating Ca2+ content. These results indicate that BgARP1 is functional on a heterogeneous background.

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References

  • Abe H, Yamaguchi-Shinozaki K, Urao T, Iwasaki T, Hosokawa D, Shinozaki K (1997) Role of Arabidopsis MYC and MYB homologs in drought- and abscisic acid-regulated gene expression. Plant Cell 9:1859–1868

    Article  CAS  PubMed  Google Scholar 

  • Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285:1256–1258

    Article  CAS  PubMed  Google Scholar 

  • Blumwald E (2000) Sodium transport and salt tolerance in plants. Curr Opin Cell Biol 12:431–434

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2:953–971

    Article  CAS  PubMed  Google Scholar 

  • Gaxiola RA, Li J, Undurraga S, Dang LM, Allen GJ, Alper SL, Fink GR (2001) Drought- and salt-tolerant plants result from overexpression of the AVP1 H+-pump. Proc Natl Acad Sci USA 98:11444–11449

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann-Sommergruber K (2002) Pathogenesis-related (PR)-proteins identified as allergens. Biochem Soc Trans 30:930–935

    Article  CAS  PubMed  Google Scholar 

  • Jiang Y, Yang B, Harris NS, Deyholos MK (2007) Comparative proteomic analysis of NaCl stress-responsive proteins in Arabidopsis roots. J Exp Bot 58:3591–3607

    Article  CAS  PubMed  Google Scholar 

  • Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17:287–291

    Article  CAS  PubMed  Google Scholar 

  • King GJ, Turner VA, Hussey CE, Wurtele ES, Lee SM (1988) Isolation and characterization of a tomato cDNA clone which codes for a salt-induced protein. Plant Mol Biol 10:821–827

    Article  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 

  • Melchers LS, Sela-Buurlage MB, Vloemans SA, Woloshuk CP, Van Roekel JS, Pen J, van den Elzen PJ, Cornelissen BJ (1993) Extracellular targeting of the vacuolar tobacco proteins AP24, chitinase and beta-1, 3-glucanase in transgenic plants. Plant Mol Biol 21:583–593

    Article  CAS  PubMed  Google Scholar 

  • Miyama M, Hanagata N (2007a) Microarray analysis of 7029 gene expression patterns in burma mangrove under high-salinity stress. Plant Sci 172:948–957

    Article  Google Scholar 

  • Miyama M, Hanagata N (2007b) Microarray gene expression profiling for salt tolerant gene selection. Plant Stress 1:118–122

    Google Scholar 

  • Miyama M, Tada Y (2008) Transcriptional and physiological study of the response of Burma mangrove (Bruguiera gymnorhiza) to salt and osmotic stress. Plant Mol Biol 68:119–129

    Article  CAS  PubMed  Google Scholar 

  • Miyama M, Shimizu H, Sugiyama M, Hanagata N (2006) Sequencing and analysis of 14, 842 expressed sequence tags of burma mangrove, Bruguiera gymnorrhiza. Plant Sci 171:234–241

    Article  Google Scholar 

  • Mosavi LK, Minor DL Jr, Peng ZY (2002) Consensus-derived structural determinants of the ankyrin repeat motif. Proc Natl Acad Sci USA 99:16029–16034

    Article  CAS  PubMed  Google Scholar 

  • Mosavi LK, Cammett TJ, Desrosiers DC, Peng ZY (2004) The ankyrin repeat as molecular architecture for protein recognition. Protein Sci 13:1435–1448

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Neuhaus JM, Sticher L, Meins F Jr, Boller T (1991) A short C-terminal sequence is necessary and sufficient for the targeting of chitinases to the plant vacuole. Proc Natl Acad Sci USA 88:10362–10366

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto H, Matsuda O, Iba K (2008) ITN1, a novel gene encoding an ankyrin-repeat protein that affects the ABA-mediated production of reactive oxygen species and is involved in salt-stress tolerance in Arabidopsis thaliana. Plant J 56:411–422

    Article  CAS  PubMed  Google Scholar 

  • Sánchez-Barrena MJ, Martínez-Ripoll M, Zhu JK, Albert A (2005) The structure of the Arabidopsis thaliana SOS3: molecular mechanism of sensing calcium for salt stress response. J Mol Biol 345:1253–1264

    Article  PubMed  Google Scholar 

  • Sato F, Koiwa H, Sakai Y, Kato N, Yamada Y (1995) Synthesis and secretion of tobacco neutral PR-5 protein by transgenic tobacco and yeast. Biochem Biophys Res Commun 211:909–913

    Article  CAS  PubMed  Google Scholar 

  • Sedgwick SG, Smerdon SJ (1999) The ankyrin repeat: a diversity of interactions on a common structural framework. Trends Biochem Sci 24:311–316

    Article  CAS  PubMed  Google Scholar 

  • Seong ES, Cho HS, Choi D, Joung YH, Lim CK, Hur JH, Wang MH (2007) Tomato plants overexpressing CaKR1 enhanced tolerance to salt and oxidative stress. Biochem Biophys Res Commun 363:983–988

    Article  CAS  PubMed  Google Scholar 

  • Shi H, Lee BH, Wu SJ, Zhu JK (2003) Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat Biotechnol 21:81–85

    Article  CAS  PubMed  Google Scholar 

  • Singh NK, Bracker CA, Hasegawa PM, Handa AK, Buckel S, Hermodson MA, Pfankoch E, Regnier FE, Bressan RA (1987) Characterization of osmotin : a thaumatin-like protein associated with osmotic adaptation in plant cells. Plant Physiol 85:529–536

    Article  CAS  PubMed  Google Scholar 

  • Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci USA 97:11632–11637

    Article  CAS  PubMed  Google Scholar 

  • Xu D, Duan X, Wang B, Hong B, Ho T, Wu R (1996) Expression of a late embryogenesis abundant protein gene, HVA1, from Barley confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiol 110:249–257

    CAS  PubMed  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6:251–264

    Article  CAS  PubMed  Google Scholar 

  • Yamanaka T, Miyama M, Tada Y (2009) Transcriptome profiling of the mangrove plant Bruguiera gymnorhiza and identification of salt tolerance genes by Agrobacterium functional screening. Biosci Biotechnol Biochem 73:304–310

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgment

This work was partially supported by Grant-in Aid for Scientific Research (C) for YT (20580008) and Grant-in Aid for Scientific Research (B) for YT (21380002).

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Correspondence to Yuichi Tada.

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Miyama, M., Tada, Y. Expression of Bruguiera gymnorhiza BgARP1 enhances salt tolerance in transgenic Arabidopsis plants. Euphytica 177, 383–392 (2011). https://doi.org/10.1007/s10681-010-0264-2

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