Skip to main content
Log in

Isolation and functional characterization of 3-phosphoglycerate dehydrogenase involved in salt responses in sugar beet

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

Abstract

The present study investigated the significance of serine biosynthetic genes for salt stress in sugar beet (Beta vulgaris). We isolated a total of four genes, two each encoding D-3-phosphoglycerate dehydrogenase (BvPGDHa and BvPGDHb) and serine hydroxymethyl transferase (BvSHMTa and BvSHMTb). mRNA transcriptional expression for BvPGDHa was significantly enhanced under salt stress conditions in both leaves and roots of sugar beet, whereas it was reduced for BvPGDHb. On the other hand, BvSHMTa was expressed transiently in leaves and roots under salt stress, whereas expression level of BvSHMTb was not altered. PGDH activity was high in storage root. After salt stress, PGDH activity was increased in leaf, petiole, and root. Recombinant proteins were expressed in Escherichia coli. The K m values for 3-phosphoglycerate in PGDHa and PGDHb were 1.38 and 2.92 mM, respectively. The findings suggest that BvPGDHa and BvSHMTa play an important role during salt stress in sugar beet.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

BADH:

Betaine aldehyde dehydrogenase

CMO:

Choline monooxygenase

3-PGA:

D-3-phosphoglycerate

PGDH:

D-3-phosphoglycerate dehydrogenase

PHP:

Phosphohydroxypyruvate

PSAT:

Phosphoserine aminotransferase

PSP:

Phosphoserine phosphatase

RuBisCO:

Ribulose-1,5-bisphosphatase carboxylase/oxygenase

SHMT:

Serine hydroxymethyl transferase

References

  • Anderson DD, Stover PJ (2009) SHMT1 and SHMT2 are functionally redundant in nuclear de novo thymidylate biosynthesis. PLOS One 9;4(6):e5839

  • Benstein RM, Ludewig K, Wulfert S, Wittek S, Gigolashvili T, Frerigmann H, Gierth M, Flügge UI, Krueger S (2013) Arabidopsis phosphoglycerate dehydrogenase1 of the phosphoserine pathway is essential for development and required for ammonium assimilation and tryptophan biosynthesis. Plant Cell 25:5011–5029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhuiyan NH, Hamada A, Yamada N, Rai V, Hibino T, Takabe T (2007) Regulation of betaine synthesis by precursor supply and choline monooxygenase expression in Amaranthus tricolor. J Exp Bot 58:4203–4212

    Article  CAS  PubMed  Google Scholar 

  • Cascales-Miñana B, Muñoz-Bertromeu J, Flores-Tornero M, Anoman AD, Pertusa J, Alaiz M, Osorio S, Femie AR, Segura J, Ros R (2013) The phosphorylated pathway of serine biosynthesis is essential both for male gametophyte and embryo development and for root growth in Arabidopsis. Plant Cell 25:2084–2101

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen TH, Murata N (2011) Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. Plant Cell Environ 34:1–20

    Article  PubMed  Google Scholar 

  • Cheng M-C, Ko K, Chang W-L, Kuo W-C, Chen G-H, Lin T-P (2015) Increased glutathione contributes to stress tolerance and global translational changes in Arabidopsis. Plant J 83:926–939

    Article  CAS  PubMed  Google Scholar 

  • Dohm JC, Minoche AE, Holtgräwe D, Capella-Gutiérrez S, Zakrzewski F, Tafer H, Rupp O, Sörensen TR, Stracke R, Reinhardt R, Goesmann A, Kraft T, Schulz B, Stadler PF, Schmidt T, Gabaldón T, Lehrach H, Weisshaar B, Himmelbauer H (2014) The genome of the recently domesticated crop plant sugar beet (Beta vulgaris). Nature 505:546–549

    Article  CAS  PubMed  Google Scholar 

  • Hanson AD, Wise R (1982) Biosynthesis, translocation, and accumulation of betaine in sugar beet and its progenitors in relation to salinity. Plant Physiol 70:1191–1198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hibino T, Waditee R, Araki E, Ishikawa H, Aoki K, Tanaka Y, Takabe T (2002) Functional characterization of choline monooxygenase, an enzyme for betaine synthesis in plants. J Biol Chem 277:41352–41360

    Article  CAS  PubMed  Google Scholar 

  • Ho CL, Saito K (2001) Molecular biology of the plastidic phosphorylated serine biosynthetic pathway in Arabidopsis thaliana. Amino Acids 20:243–259

    Article  CAS  PubMed  Google Scholar 

  • Ho CL, Noji M, Saito M, Saito K (1999) Regulation of serine biosynthesis in Arabidopsis. Crucial role of plastidic 3-phosphoglycerate dehydrogenase in non-photosynthetic tissues. J Biol Chem 274:397–402

    Article  CAS  PubMed  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

  • Nuccio ML, Russell BL, Nolte KD, Rathinasabapathi B, Gage DA, Hanson AD (1998) The endogenous choline supply limits glycine betaine synthesis in transgenic tobacco expressing choline monooxygenase. Plant J 16:487–496

    Article  CAS  PubMed  Google Scholar 

  • Rathinasabapathi B, Burnet M, Russell B, Gage DA, Liao PC, Nye GJ, Scott P, Golbeck JH, Hanson AD (1997) Choline monooxygenase, an unusual iron–sulfur enzyme catalyzing the first step of glycine betaine synthesis in plants: prosthetic group characterization and cDNA cloning. Proc Natl Acad Sci U S A 94:3454–3458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rontein D, Basset G, Hanson AD (2002) Metabolic engineering of osmoprotectant accumulation in plants. Metab Eng 4:49–56

    Article  CAS  PubMed  Google Scholar 

  • Ros R, Muñoz-Bertomeu J, Krueger S (2014) Serine in plants: biosynthesis, metabolism, and functions. Trends Plant Sci 19:564–569

    Article  CAS  PubMed  Google Scholar 

  • Russell BL, Rathinasabapathi B, Hanson AD (1998) Osmotic stress induces expression of choline monooxygenase in sugar beet and amaranth. Plant Physiol 116:859–865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith DD, Summers PS, Weretilnyk EA (2000) Phosphocholine synthesis in spinach: characterization of phosphoethanolamine N-methyltransferase. Physiol Plant 108:286–294

    Article  CAS  Google Scholar 

  • Tabuchi T, Okuda T, Takashima Y, Azuma T, Nanmori T, Yasuda T (2006) Transcriptional response of glycinebetaine-related genes to salt stress and light in leaf beet. Plant Biotechnol 23:317–320

    Article  CAS  Google Scholar 

  • Takabe T, Rai V, Hibino T (2006) Metabolic engineering of glycinebetaine. In: Rai AK, Takabe T (eds) Abiotic stress tolerance in plants. Springer, Berlin, pp 137–151

    Chapter  Google Scholar 

  • Tasseva G, Richard L, Zachowski A (2004) Regulation of phosphatidylcholine biosynthesis under salt stress involves choline kinases in Arabidopsis thaliana. FEBS Lett 566:115–120

    Article  CAS  PubMed  Google Scholar 

  • Toujani W, Muñoz-Bertomeu J, Flores-Tornero M, Rosa-Téllez S, Anoman AD, Alseekh S, Femie AR, Ros R (2013) Functional characterization of the plastidial 3-phosphoglycerate dehydrogenase family in Arabidopsis. Plant Physiol 163:1164–1178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waditee R, Tanaka Y, Aoki K, Hibino T, Jikuya H, Takano J, Takabe T, Takabe T (2003) Isolation and functional characterization of N-methyltransferases that catalyze betaine synthesis from glycine in a halotolerant photosynthetic organism Aphanothece halophytica. J Biol Chem 278:4932–4942

    Article  CAS  PubMed  Google Scholar 

  • Waditee R, Bhuiyan MN, Rai V, Aoki K, Tanaka Y, Hibino T, Suzuki S, Takano J, Jagendorf AT, Takabe T, Takabe T (2005) Genes for direct methylation of glycine provide high levels glycine betaine and abiotic stress tolerance in Synechococcus and Arabidopsis. Proc Natl Acad Sci U S A 102:1318–1323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waditee R, Bhuiyan NH, Hirata E, Hibino T, Tanaka Y, Shikata M, Takabe T (2007) Metabolic engineering for betaine accumulation in microbes and plants. J Biol Chem 282:34185–34193

    Article  CAS  PubMed  Google Scholar 

  • Weretilnyk EA, Hanson AD (1989) Betaine aldehyde dehydrogenase from spinach leaves: purification, in vitro translation of the mRNA and regulation by salinity. Arch Biochem Biophys 271:56–63

    Article  CAS  PubMed  Google Scholar 

  • Weretilnyk EA, Smith DD, Wilch GA, Summers PS (1995) Enzymes of choline synthesis in spinach response of phospho-base N-methyltransferase activities to light and salinity. Plant Physiol 109:1085–1091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamada N, Promden W, Yamane K, Tamagake H, Hibino T, Tanaka Y, Takabe T (2009) Preferential accumulation of betaine uncoupled to choline monooxygenase in young leaves of sugar beet-importance of long-distance translocation of betaine under normal and salt-stressed conditions. J Plant Physiol 166:2058–2070

    Article  CAS  PubMed  Google Scholar 

  • Yamada N, Sakakibara S, Tsutsumi K, Waditee R, Tanaka Y, Takabe T (2011) Expression and substrate specificity of betaine/proline transporters suggest a novel choline transport mechanism in sugar beet. J Plant Physiol 168:1609–1616

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Sun K, Sandoval FJ, Santiago K, Roje S (2010) One-carbon metabolism in plants: characterization of a plastid serine hydroxymethyltranferase. Biochem J 430:97–105

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported in part by Grants-in-Aid for Scientific Research from the Ministry of Education, Science, and Culture of Japan; Salt Science Research Foundation; and the International Center for Natural Environmental Science of Meijo University, Japan.

Author information

Authors and Affiliations

Authors

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: Bhumi Nath Tripathi

Note that nucleotide sequence data for the D-3-phosphoglycerate dehydrogenase genes, BvPGDHa and BvPGDHb, and serine hydroxymethyl transferase genes, BvSHMTa and BvSHMTb, from sugar beet are available in the DDJB database under the accession numbers LC201809, LC201810, LC201811 and LC201812, respectively.

Electronic supplementary material

.

ESM 1

(PDF 207 kb)

.

ESM 2

(PDF 185 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kito, K., Tsutsumi, K., Rai, V. et al. Isolation and functional characterization of 3-phosphoglycerate dehydrogenase involved in salt responses in sugar beet. Protoplasma 254, 2305–2313 (2017). https://doi.org/10.1007/s00709-017-1127-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-017-1127-7

Keywords

Navigation