Skip to main content
SpringerLink
Log in

Isolation and characterization of Panax ginseng geranylgeranyl-diphosphate synthase genes responding to drought stress

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Geranylgeranyl-diphosphate synthases (GGDPS) catalyze branch point enzymatic reactions producing isoprenoid-derived products which are necessary for plant growth and responses to a wide range of biotic and abiotic stresses. In our study, full length geranylgeranyl-diphosphate synthase 1 (PgGGDPS1) and 2 (PgGGDPS2) cDNA were isolated and characterized from the flower of Panax ginseng and 4-year old P. ginseng cv. Gumpoong. The cDNA had open reading frame of 1032 and 1116 bp with a deduced amino acid sequence of 343 and 371 residues for GGDPS1 and GGDPS2, respectively. The calculated molecular mass of GGDPS1 and GGDPS2 were approximately 37.66 and 40.21 kDa with a predicated isoelectric point of 5.32 and 6.23 and predicted localization of plastid. A GenBank Blast X search revealed that the deduced amino acid of PgGGDPS1 shared a high degree of homology with GGDPS from Panax notoginseng. The transcription pattern of GGDPS genes was different at various developmental stages. Both GGDPS genes were highly expressed in aerial parts of the plant, especially in rapidly growing tissues such as 4-year old flower and stem tissues. Transcript level of PgGGDPS1 was differentially induced in ginseng not only during Pseudomonas syringae pv tomato infection but also after exposure to abiotic stresses. Our results suggested that the induction of GGDPS genes specifically PgGGDPS1 by drought stress may affect chlorophyll levels, intracellular GA content and accumulation of carotenoids as the precursor for higher production of ABA and possibly stomatal closure as the barrier for water loss.

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

ABA:

abscisic acid

CLD:

chain length determination

EST:

expressed sequence tags

GA3:

gibberellin

GGDP:

geranylgeranyl diphosphate

GGDPS:

geranylgeranyl-diphosphate synthase

GGR:

geranylgeranyl reductase

MJ:

methyl jasmonates

RT-PCR:

reverse transcriptase-polymerase chain reaction

SA:

salicylic acid

YE:

yeast extract

References

  • Aitken, S. M., Attucci, S., Ibrahim, R. K., & Gulick, P. J. (1995). A cDNA encoding geranylgeranyl pyrophosphate synthase from whitelupin. Plant Physiology, 108, 837–838.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Aliyev, R. Т., Coskuncelebi, K., Beyazoglu, O., & Hacieva, S. I. (2000). Alterations in the genome of wheat seedlings grown under drought stress and the effect of gibberellic acid on these alterations. Review Biology, 93, 183–189.

    CAS  Google Scholar 

  • Ament, K., Van Schie, C. C., Bouwmeester, H. J., Haring, M. A., & Schuurink, R. C. (2006). Induction of a leaf specific geranylgeranyl pyrophosphate synthase and emission of −4, 8, 12-trimethyltrideca-1, 3, 7, 11-tetraene in tomato are dependent on both jasmonic acid and salicylic acid signaling pathways. Planta, 224, 1197–1208.

    Article  CAS  PubMed  Google Scholar 

  • Artimo, P., Jonnalagedda, M., Arnold, K., Baratin, D., Csardi, G., de Castro, E., Duvaud, S., Flegel, V., Fortier, A., Gasteiger, E., et al. (2012). ExPASy: SIB bioinformatics resource portal. Nucleic Acids Research, 40, W597–W603.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Badillo, A., Steppuhn, J., Deruere, J., Camara, B., & Kuntz, M. (1995). Structure of a functional geranylgeranyl pyrophosphate synthase gene from Capsicum annuum. Plant Molecular Biology, 27, 425–428.

    Article  CAS  PubMed  Google Scholar 

  • Bantignies, B., Liboz, T., & Ambid, C. (1995). Nucleotide sequence of a Catharanthus roseus geranylgeranyl pyrophosphate synthase gene. Plant Physiology, 110, 336.

    Google Scholar 

  • Bartley, G. E., & Scolnik, P. A. (1995). Plant carotenoids: pigments for photoprotection, visual attraction, and human health. Plant Cell, 7, 1027–1038.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chen, A. J., Kroon, P. A., & Poulter, C. D. (1994). Isoprenyl diphosphate synthases protein-sequence comparisons, a phylogenetic tree and redictions of secondary structure. Protein Science, 3, 600–607.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • El-Meleigy, E. A., Hassanein, R. A., & Abdel Kader, D. Z. (1999). Improvement of drought tolerance in Araches hypogaea L. plant by some growth substances 1. Growth and productivity. Bulletin Faculty Science Association University, 28, 159–185.

    CAS  Google Scholar 

  • Emanuelson, O., Nielsen, H., Brunak, S., & von Heijne, G. (2000). Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. Journal of Molecular Biology, 300, 1005–1016.

    Article  Google Scholar 

  • Engprasert, S., Taura, F., Kawamukai, M., & Shoyama, Y. (2004). Molecular cloning and functional expression of geranylgeranyl pyrophosphate synthase from Coleus forskohlii Briq. BMC Plant Biology, 4, 18.

    Article  PubMed Central  PubMed  Google Scholar 

  • Ge, X. C., & Wu, J. Y. (2004). Tanshinone production and isoprenoid pathways in Salvia miltiorrhiza hairy roots induced by Ag+ and yeast elicitor. Plant Science, 168, 487–491.

    Article  Google Scholar 

  • Gray, J. C. (1987). Control of isoprenoid biosynthesis in higher plants. Advances in Botanical Research, 14, 25–91.

    CAS  Google Scholar 

  • Hedden, P., & Kamiya, Y. (1997). Gibberellin biosynthesis: enzymes, genes and their regulation. Annual Review of Plant Physiology and Plant Molecular Biology, 48, 431–460.

    Article  CAS  PubMed  Google Scholar 

  • Hefner, J., Ketchum, F. E. B., & Croteau, R. (1998). Cloning and functional expression of a cDNA encoding geranylgeranyl diphosphate synthase from Taxus canadensis and assessment of the role of this prenyltransferase in cells induced for taxol production. Archives of Biochemistry and Biophysics, 360, 62–74.

    Article  CAS  PubMed  Google Scholar 

  • Hua, W., Song, J., Li, C., & Wang, Z. (2012). Molecular cloning and characterization of the promoter of SmGGPPs and its expression pattern in Salvia miltiorrhiza. Molecular Biology Reports, 39, 5775–5783.

    Article  CAS  PubMed  Google Scholar 

  • Kai, G., Liao, P., Zhang, T., Zhou, W., Wang, J., Xu, H., Liu, Y., & Zhang, L. (2010). Characterization, expression profiling, and functional identification of a gene encoding geranylgeranyl diphosphate synthase from Salvia miltiorrhiza. Biotechnology and Bioprocess Engineering, 15, 236–245.

    Article  CAS  Google Scholar 

  • Kelen, M., Çubuk Demìralay, E., Demìralay, E., Sen, S., & özkan, G. (2004). Separation of Abscisic acid, Indole-3-Acetic acid, Gibberellic acid in 99 R (Vitisberlandierix Vitisrupestris) and rose oil (Rosa damascene Mill.) by Reversed Phase Liquid Chromatography. Turkish Journal of Chemistry, 28, 603–610.

    CAS  Google Scholar 

  • Kim, Y. J., Jang, M. G., Noh, H. Y., Lee, H. J., Sukweenadhi, J., Kim, J. H., Kim, S. Y., Kwon, W. S., & Yang, D. C. (2014). Molecular characterization of two glutathione peroxidase genes of Panax ginseng and their expression analysis against environmental stresses. Gene, 535, 33–41.

    Article  CAS  PubMed  Google Scholar 

  • Kirk, J. T. O., & Allen, R. L. (1965). Dependence of chloroplast pigment synthesis on protein synthesis: Effect of actidione. Biochemical Biophysical Research Communications, 21, 523–530.

    Article  CAS  PubMed  Google Scholar 

  • Kleinig, H. (1989). The role of plastids in isoprenoid biosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology, 40, 39–59.

    Article  CAS  Google Scholar 

  • Kuntz, M., Romer, S., Suire, C., Hugueney, P., Weil, J. H., Schantz, R., & Camara, B. (1992). Identification of a cDNA for the plastid-located geranylgeranyl pyrophosphate synthase from Capsicum annuum: correlative increase in enzyme activity and transcript level during fruit ripening. Plant Journal, 2, 25–34.

    CAS  PubMed  Google Scholar 

  • Laferriere, A., & Beyer, P. (1991). Purification of geranylgeranyl diphosphate synthase from Sinapis alba etioplasts. Biochimica et Biophysica Acta, 1077, 167–172.

    Article  CAS  Google Scholar 

  • Lee, C. H., & Kim, J. H. (2014). A review on the medicinal potentials of ginseng and ginsenosides on cardiovascular diseases. Journal of Ginseng Research, 38, 161–166.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liang, P. H., Ko, T. P., & Wang, A. H. J. (2002). Structure, mechanism and function of prenyltransferases. European Journal of Biochemistry, 269, 3339–3354.

    Article  CAS  PubMed  Google Scholar 

  • Lichtenthaler, H. K. (1987). Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology, 148, 350–82.

    CAS  Google Scholar 

  • Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta CT) method. Methods, 25, 402–408.

    Article  CAS  PubMed  Google Scholar 

  • Morris, P. C., Kumar, A., Bowles, D. J., & Cuming, A. C. (1990). Osmotic stress and abscisic acid regulate the expression of the Em gene of wheat. European Journal of Biochemistry, 190, 625–630.

    Article  CAS  PubMed  Google Scholar 

  • Murashige, T., & Skoog, F. (1962). A revised medium for rapid growth and bio assay with tobacco tissue cultures. Plant Physiology, 15, 473–499.

    Article  CAS  Google Scholar 

  • Oh, S. K., Kim, I. J., Shin, D. H., Yang, J., Kang, H., & Han, K. H. (2000). Cloning, characterization, and heterologous expression of a functional geranylgeranyl pyrophosphate synthase from sunflower (Helianthus annuus L.). Journal of Plant Physiology, 157, 535–542.

    Article  CAS  Google Scholar 

  • Okada, K., Saito, T., Nakagawa, T., Kawamukai, M., & Kamiya, Y. (2000). Five geranylgeranyldiphosphate synthases expressed in different organs are localized into three subcellular compartments in Arabidopsis. Plant Physiology, 122, 1045–1056.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Scolnik, P. A., & Bartley, G. E. (1994). Nucleotide sequence of an Arabidopsis cDNA for geranylgeranyl pyrophosphate synthase. Plant Physiology, 104, 1469–1470.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Scolnik, P. A., & Bartley, G. E. (1995). Nucleotide sequence of a putative geranylgeranyl pyrophosphate synthase (GenBank accession no. L40577) from Arabidopsis (PGR 95–018). Plant Physiology, 108, 1343.

    Google Scholar 

  • Scolnik, P. A., & Bartley, G. E. (1996). Two more members of Arabidopsis geranylgeranyl pyrophosphate synthase family (PGR 96–014). Plant Physiology, 110, 1435.

    Google Scholar 

  • Sitthithaworn, W., Kojima, N., Viroonchatapan, E., Suh, D. Y., Iwanami, N., Hayashi, T., Noji, M., Saito, K., Niwa, Y., & Sankawa, U. (2001) Geranylgeranyl diphosphate synthase from Scoparia dulcis and Croton sublyratus. Plastid localization and conversion to a farnesyl diphosphate synthase by mutagenesis. Chem Pharm Bull, 49, 197–292.

  • Song, M. Y., Kim, B. S., & Kim, H. (2014). Influence of Panax ginseng on obesity and gut microbiota in obese middle-aged Korean women. Journal of Ginseng Research, 38, 106–115.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tanimoto, E. (1991). Gibberellin requirement for the normal growth of roots. In N. Takahashi, B. O. Phinney, & J. MacMillan (Eds.), Gibberellins (pp. 229–240). New York: Springer.

    Chapter  Google Scholar 

  • Verslues, P. E., Agarwal, M., Katiyar-Agarwal, S., Zhu, J., & Zhu, J. K. (2006). Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant Journal, 45, 523–539.

    Article  CAS  PubMed  Google Scholar 

  • Wang, K., & Ohnuma, S. I. (1999). Chain-length determination mechanism of isoprenyl diphosphate synthases and implications for molecular evolution. Trends Biochemical Science, 24, 445–451.

    Article  CAS  Google Scholar 

  • Zhu, X. F., Suzuki, K., Okada, K., Tanaka, K., Nakagawa, T., Kawamukai, M., & Matsuda, H. (1997a). Cloning and functional expression of a novel geranylgeranyl pyrophosphate synthase gene from Arabidopsis thaliana in Escherichia coli. Plant Cell Physiology, 38, 357–361.

    Article  CAS  PubMed  Google Scholar 

  • Zhu, X. F., Suzuki, K., Saito, T., Okada, K., Tanaka, K., Nakagawa, T., Matsuda, H., & Kawamukai, M. (1997b). Geranylgeranyl pyrophosphatesynthase encoded by the newly isolated gene GGPS6 from Arabidopsis thaliana is localized in mitochondria. Plant Molecular Biology, 35, 331–341.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by iPET (312064-03-1-HD040), Korea Institute of Planning and Evaluation for Technology in Food, Agriculture, Forestry and Fisheries, Republic of Korea.

Author information

Authors and Affiliations

  1. Department of Oriental Medicinal Biotechnology, College of Life Sciences, Kyung Hee University, Yongin, 446-701, Republic of Korea

    Yu-Jin Kim & Deok-Chun Yang

  2. Graduate School of Biotechnology and Ginseng Bank, College of Life Sciences, Kyung Hee University, Yongin, 446-701, Republic of Korea

    Shadi Rahimi, Yu-Jin Kim, Balusamy Sri Renuka Devi, Altanzul Khorolragchaa, Johan Sukweenadhi & Deok-Chun Yang

Authors
  1. Shadi Rahimi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yu-Jin Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Balusamy Sri Renuka Devi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Altanzul Khorolragchaa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Johan Sukweenadhi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Deok-Chun Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Deok-Chun Yang.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rahimi, S., Kim, YJ., Devi, B.S.R. et al. Isolation and characterization of Panax ginseng geranylgeranyl-diphosphate synthase genes responding to drought stress. Eur J Plant Pathol 142, 747–758 (2015). https://doi.org/10.1007/s10658-015-0648-1

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-015-0648-1

Keywords

Search

Navigation