Skip to main content
SpringerLink
Log in

Isolation, expression, and functional analysis of developmentally regulated plasma membrane polypeptide 1 (DREPP1) in Sporobolus virginicus grown under alkali salt stress

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

The plant specific DREPP proteins have been shown to bind Ca2+ and regulate the N-myristoylation signaling and microtubule polymerization in Arabidopsis thaliana. The information about DREPP proteins in other plants is, however, scarce. In the present study, we isolated the DREPP gene from a halophytic grass, Sporobolus virginicus, and tested whether the gene was involved in alkaline salt stress responses. The SvDREPP1 was cloned from S. virginicus by RACE methods. The isolated gene showed high homology to DREPP homologs from C4 grasses, Setaria italica, and Panicum hallii as well as rice (OsDREPP1). The encoded protein contained 202 amino acid residues. It was expressed in E. coli, and its biochemical properties were studied. It was observed that SvDREPP1 was not only Ca2+-binding protein, but also bind to calmodulin and microtubules. The SvDREPP1 mRNA expression in plants grown under alkaline salt stress was upregulated by 3.5 times over the control in leaf tissues after 48-h treatment, whereas it was increased for 6.0 times in the root tissues at 36 h. The data suggests the importance of SvDREPP1 in regulating alkali salt stress responses in the leaf tissues.

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
Fig. 6

Similar content being viewed by others

Abbreviations

CaM:

Calmodulin

DREPP:

Developmentally regulated plasma membrane polypeptide

MAP18:

Microtubule-associated protein

MPD25:

Microtubule destabilization protein 25

PCaP:

Plasma membrane-associated Ca2+-binding protein

References

  • Bell H, O’Leary JW (2003) Effects of salinity on growth and cation accumulation of Sporobolus virginicus (Poaceae). Am J Bot 90:1416–1424

    Article  PubMed  Google Scholar 

  • Campbell KP, MacLennan DH, Jorgensen AO (1983) Staining of the Ca2+-binding proteins, calsequestrin, calmodulin, troponin C, and S-100, with the cationic carbocyanine dye “Stains-all”. J Biol Chem 258:11267–11273

    PubMed  CAS  Google Scholar 

  • Cha-um S, Supaibulwatana K, Kirdmanee C (2007) Glycinebetaine accumulation, physiological characterizations, and growth efficiency in salt tolerant and salt sensitive lines of indica rice (Oryza sativa L. ssp. indica) response to salt stress. J Agron Crop Sci 193:157–166

    Article  CAS  Google Scholar 

  • Chen W, Cui P, Sun H, Weiqing Guo W, Yang C, Jin H, Fang B, Shi D (2009) Comparative effects of salt and alkali stresses on organic acid accumulation and ionic balance of seabuckthorn (Hippophae rhamnoides). Ind Crops Prod 30:351–358

    Article  CAS  Google Scholar 

  • Fujita S, Pytela J, Hotta T, Kato T, Hamada T, Akamatsu R, Ishida Y, Kutsuna N, Hasezawa S, Nomura Y, Nakagami H, Hashimoto T (2013) An atypical tubulin kinase mediates stress-induced microtubule depolymerization in Arabidopsis. Curr Biol 23:1969–1978

    Article  PubMed  CAS  Google Scholar 

  • Fukuda A, Chiba K, Maeda M, Nakamura A, Maeshima M, Tanaka Y (2004) Effect of salt and osmotic stresses on the expression of genes for the vacuolar H+-pyrophosphatase, H+-ATPase subunit A, and Na+/H+ antiporter from barley. J Exp Bot 55:585–594

    Article  PubMed  CAS  Google Scholar 

  • Gantet P, Masson F, Domergue O, Marquis-Mention M, Bauw G, Inze D, Rossignol M, Teyssendier de la Serve B (1996) Cloning of a cDNA encoding a developmentally regulated 22 kDa polypeptide from tobacco leaf plasma membrane. Biochem Mol Biol Int 40:469–477

    PubMed  CAS  Google Scholar 

  • Guo LQ, Shi DC, Wang DL (2010) The key physiological response to alkali stress by the alkali-resistant halophyte Puccinellia tenuiflora is the accumulation of large quantities of organic acids and into the rhyzosphere. J Agron Crop Sci 196:123–135

    Article  CAS  Google Scholar 

  • Hossain GS, Waditee R, Hibino T, Tanaka Y, Takabe T (2006) Root specific expression of Na+/H+ antiporter gene from Synechocystis sp. PCC6803 confers salt tolerance of tobacco plant. Plant Biotechnol 23:275–281

    Article  CAS  Google Scholar 

  • Ide Y, Nagasaki N, Tomioka R, Suito M, Kamiya T, Maeshima M (2007) Molecular properties of a novel, hydrophilic cation-binding protein associated with the plasma membrane. J Exp Bot 58:1173–1183

    Article  PubMed  CAS  Google Scholar 

  • Kato M, Nagasaki-Takeuchi N, Ide Y, Maeshima M (2010a) An Arabidopsis hydrophilic Ca2+-binding protein with a PEVK-rich domain, PCaP2, is associated with the plasma membrane and interacts with calmodulin and phosphatidylinositol phosphates. Plant Cell Physiol 51:366–379

    Article  PubMed  Google Scholar 

  • Kato M, Nagasaki-Takeuchi N, Ide Y, Tomioka R, Maeshima M (2010b) PCaPs, possible regulators of PtdInsP signals on plasma membrane. Plant Signal Behav 5:848–850

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kato M, Aoyama T, Maeshima M (2013) The Ca2+-binding protein PCaP2 located on the plasma membrane is involved in root hair development as a possible signal transducer. Plant J 74:690–700

    Article  PubMed  CAS  Google Scholar 

  • Landi S, Hausman J-F, Guerriero G, Esposito S (2017) Poaceae vs. abiotic stress: focus on drought and salt stress, recent insights and perspectives. Front Plant Sci 8:1214

    Article  PubMed  PubMed Central  Google Scholar 

  • Li J, Wang X, Qin T, Zhang Y, Liu X, Sun J, Mao T (2011) MDP25, a novel calcium regulatory protein, mediates hypocotyl cell elongation by destabilizing cortical microtubules in Arabidopsis. Plant Cell 23:4411–4427

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li L, Wang F, Yan P, Jing W, Zhang C, Kudla J, Zhang W (2017) A phosphoinositide-specific phospholipase C pathway elicits stress-induced Ca2+ signals and confers salt tolerance to rice. New Phytol 14:1172–1187

    Article  CAS  Google Scholar 

  • Loggini B, Scartazza A, Brugnoli E, Navari-Izzo F (1999) Antioxidant defense system, pigment composition, and photosynthetic efficiency in two wheat cultivars subjected to drought. Plant Physiol 119:1091–1099

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

    Article  PubMed  CAS  Google Scholar 

  • Nagasaki N, Tomioka R, Maeshima M (2008) A hydrophilic cation-binding protein of Arabidopsis thaliana, AtPCaP1, is localized to plasma membrane via N-myristoylation and interacts with calmodulin and the phosphatidylinositol phosphates PtdIns (3, 4, 5) P3 and PtdIns (3, 5) P2. FEBS J 275:2267–2282

    Article  PubMed  CAS  Google Scholar 

  • Nagata C, Miwa C, Tanaka N, Kato M, Suito M, Tsuchihira A, Sato Y, Segami S, Maeshima M (2016) A novel-type phosphatidylinositol phosphate-interactive, Ca-binding protein PCaP1 in Arabidopsis thaliana: stableassociation with plasma membrane and partial involvementin stomata closure. J Plant Res 129:539–550

    Article  PubMed  CAS  Google Scholar 

  • Naidoo G, Naidoo Y (1998) Salt tolerance in Sporobolus virginicus: the importance of ion relations and salt secretion. Flora 193:337–344

    Article  Google Scholar 

  • Nick P (2013) Microtubules, signalling and abiotic stress. Plant J 75:309–323

    Article  PubMed  CAS  Google Scholar 

  • Qin T, Liu X, Li J, Sun J, Song L, Mao T (2014) Arabidopsis microtubule-destabilizing proteinfunctions in pollen tube growth by severing actin filaments. Plant Cell 26:325–339

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Suh BC, Hille B (2008) PIP2 is a necessary cofactor for ion channel function: how and why? Annu Rev Biophys 37:175–195

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tada Y, Komatsubara S, Kurusu T (2014) Growth and physiological adaptation of whole plants and cultured cells from a halophyte turf grass under salt stress. AoB Plants 6:plu041

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tanaka K, Ohta K, Haddad PR, Fritz JS, Lee KP, Hasebe K, Ieuji A, Miyanaga A (1999) Acid-rain monitoring in East Asia with a portable-type ion-exclusion-cation-exchange chromatographic analyzer. J Chromatogr 850:311–317

    Article  CAS  Google Scholar 

  • Vosolobě S, Petrášek J, Schwarzerová K (2017) Evolutionary plasticity of plasma membrane interaction in DREPP family proteins. Biochim Biophys Acta 1859:686–697

    Article  CAS  Google Scholar 

  • Wang C, Li J, Yuan M (2007a) Salt tolerance requires cortical microtubule reorganization in Arabidopsis. Plant Cell Physiol 48:1534–1547

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Zhu L, Liu B, Wang C, Jin L, Zhao Q, Yuan M (2007b) Arabidopsis MICROTUBULE-ASSOCIATED PROTEIN18 functions in directional cell growth by destabilizing cortical microtubules. Plant Cell 19:877–889

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yamada N, Theerawitaya C, Kageyama H, Cha-um S, Takabe T (2015) Expression of developmentally regulated plasma membrane polypeptide (DREPP2) in rice root tip and interaction with Ca2+/CaM complex and microtubule. Protoplasma 252:1519–1527

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto N, Takano T, Tanaka K, Ishige T, Terashima S, Endo C, Kurusu T, Yajima S, Yano K, Tada Y (2015) Comprehensive analysis of transcriptome response to salinity stress in halophytic turf grass Sporobolus virginicus. Front Plant Sci 6:241

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang C, Shi D, Wang D (2008) Comparative effects of salt and alkali stresses on growth, osmotic adjustment and ionic balance of an alkali-resistant halophyte Sueda glauca (Bge.). Plant Growth Regul 56:179–190

  • Yang CW, Xu HH, Wang LL, Liu J, Shi DC, Wang DL (2009) Comparative effects of salt-stress and alkali-stress on the growth, photosynthesis, solute accumulation, and ion balance of barley plants. Photosynthetica 47:79–86

    Article  CAS  Google Scholar 

  • Zhang JT, Mu CS (2009) Effects of saline and alkaline stresses on the germination, growth, photosynthesis, ionic balance and anti-oxidant system in an alkali-tolerant leguminous forage Lathyrus quinquenervius. Soil Sci Plant Nutr 55:685–697

    Article  CAS  Google Scholar 

  • Zhang GH, Su Q, An LJ, Wu S (2008) Characterization and expression of a vacuolar Na+/H+ antiporter gene from the monocot halophyte Aeluropus littoralis. Plant Physiol Biochem 46:117–126

    Article  PubMed  CAS  Google Scholar 

  • Zhao Q, Suo J, Chen S, Jin Y, Ma X, Yin Z, Zhang Y, Wang T, Luo J, Jin W, Zhang X, Zhou Z, Dai S (2016) Na2CO3-responseive mechanisms in halophyte Puccinellia tenuiflora roots revealed by physiological and proteomic analyses. Sci Rep 6:32717

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Funding

This work was partially granted by Grants-in-Aid for Scientific Research from the Ministry of Education, Science and Culture of Japan and the International Center for Green Biotechnology of Meijo University.

Author information

Authors and Affiliations

  1. National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency (NSTDA), Pathum Thani, 12120, Thailand

    Cattarin Theerawitaya & Suriyan Cha-um

  2. Research Institute, Meijo University, Tenpaku-ku, Nagoya, Aichi, 468-8502, Japan

    Nana Yamada-Kato & Teruhiro Takabe

  3. Department of Environment Studies, Faculty of Science, Panjab University, Chandigarh, 160014, India

    Harminder Pal Singh

  4. Graduate School of Environmental and Human Sciences, Meijo University, Nagoya, 468-8502, Japan

    Teruhiro Takabe

Authors
  1. Cattarin Theerawitaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nana Yamada-Kato
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Harminder Pal Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Suriyan Cha-um
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Teruhiro Takabe
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Teruhiro Takabe.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: Peter Nick

Accession number for SvDREPP1, LC342075

Electronic supplementary material

ESM 1

(DOCX 23 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Theerawitaya, C., Yamada-Kato, N., Singh, H.P. et al. Isolation, expression, and functional analysis of developmentally regulated plasma membrane polypeptide 1 (DREPP1) in Sporobolus virginicus grown under alkali salt stress. Protoplasma 255, 1423–1432 (2018). https://doi.org/10.1007/s00709-018-1242-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-018-1242-0

Keywords

Search

Navigation