Skip to main content
SpringerLink
Log in

The linkage between phenylethanoid glycosides biosynthetic pathway and some aromatic amino acids and carbohydrates (rhamnose and glucose) in Scrophularia striata Boiss. cell culture

  • Original Article
  • Published:
Plant Cell, Tissue and Organ Culture (PCTOC) Aims and scope Submit manuscript

Abstract

In the present study, variations in levels of amino acids and carbohydrates in Scrophularia striata Boiss. were investigated at different growth phases in two in-vitro culture systems; namely shake flask and bioreactor by high-performance liquid chromatography (HPLC). The maximum contents of phenylalanine, tyrosine,and rhamnose were determined at 25th day of cell culture in shake flask and 10th day of cell culture in bioreactor while, the maximum content of glucose was observed at 15th day in shake flask and at 25th day in bioreactor. It seems that phenylalanine and tyrosine as precursors of phenylethanoid glycosides were directly related to biosynthetic pathway of phenylethanoid glycosides (PeGs) and also rhamnose and glucose content. In summary, analysis of primary metabolites in two culture systems showed that metabolism and cost of energy of amino acids and carbohydrates during cell culture of S. striata play a critical role in production of PeG compounds. Obtaining high levels of sucrose in S. striata cell culture in bioreactor reflected higher energy demands. It seems that the bioreactor shows higher rates of the produced amino acids as precursors for glycolysis and tricarboxylic cycles. Moreover, metabolism rate of amino acids was increased to supply enough energy and C-skeletons for biosynthesis of N-containing metabolites as well as secondary metabolites. In this study, potential capacity of S. striata cells for synthesis of amino acids and carbohydrates was also compared in both shake flask and bioreactor systems.

Graphic abstract

Key message

Amino acids and carbohydrates metabolism and cost of energy during cell culture of S. striata play a critical role in production of PeGs compounds such as acteoside and echinacoside. Amino acids metabolism to supply enough energy and C-skeletons for the biosynthesis of N-containing metabolites as well as secondary metabolites has been increased. Too, the bioreactor may supply enough energy and C-skeletons for the biosynthesis of N-containing metabolites

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
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Abbreviations

ANOVA:

Analysis of variance

DW:

Dry weight

FLD:

Fluorescence detector

FW:

Fresh weight

Fru:

Fructose

Glc:

Glucose

HCA:

Hierarchical cluster analysis

HPLC:

High performance liquid chromatography

Inv:

Invertase

OPA:

O-phthalaldehyde

PCA:

Principle components analysis

PeGs:

Phenylethanoid glycosides

RID:

Refractive index detector

SUS:

Sucrose synthase

TCA:

Tricarboxylic acid

UDPG:

Uridine diphosphate glucose

References

  • Ahmadi-Sakha S, Sharifi M, Niknam V, Ahmadian-Chashmi N (2018) Phenolic compounds profiling in shake-flask and bioreactor system cell cultures of Scrophularia striata Boiss. Vitro Cell Dev Bio. https://doi.org/10.1007/s11627-018-9899-9

    Article  Google Scholar 

  • Ahmadi-Sakha S, Sharifi M, Niknam V (2016) Bioproduction of phenylethanoid glycosides by plant cell culture of Scrophularia striata Boiss.: from shake-flasks to bioreactor. Plant Cell Tissue Organ Cult 124:275–281

    Article  CAS  Google Scholar 

  • Amir R (2010) Current understanding of the factors regulating methionine content in vegetative tissues of higher plants. Amino Acids 39:917–931

    Article  CAS  PubMed  Google Scholar 

  • Alipieva K, Korkina L, Orhan IE, Georgiev MI (2014) Verbascoside-a review of its pccurrence, (bio)synthesis and pharmacological significance. Biotechnol Adv 32(6):1065–1076

    Article  CAS  PubMed  Google Scholar 

  • Bhandari P, Kumar N, Singh B, Kaul VK (2008) Simultaneous determination of sugars and picrosides in Picrorhiza species using ultrasonic extraction and high-performance liquid chromatography with evaporative light scattering detection. J Chromatogr A 1194:257–261

    Article  CAS  PubMed  Google Scholar 

  • Biermann MB, Vollatadt B, Linnemann S, Knupfer J, Seidel U, Horn U (2013) Simultaneous analysis of the non-canonical amino acids norleucine and norvaline in biopharmaceutical-related fermentation processes by a new ultra-high performance liquid chromatography approach. Amino Acids 44:1225–1231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boundless (2016) General biology 3(1)

  • Causin HF (1996) The central role of amino acids on nitrogen utilization and plant growth. J Plant Physiol 149(3–4):358–362

    Google Scholar 

  • Cheng YC, Sheen JM, Hu WL, Hung YC (2017) Polyphenols and Oxidative Stress in Atherosclerosis-Related Ischemic Heart Disease and Stroke. Oxid Med Cell Longev. https://doi.org/10.1155/2017/8526438

  • Clarkson DT (1986) Regulation of the absorption and release of nitrate by plant cells: a review of current ideas and methodology. In: Fundamental, ecological and agricultural aspects of nitrogen metabolism in higher plants. pp 3–27

  • Dhillon MK, Kumar S, Gujar GT (2014) A common HPLC-PDA method for amino acid analysis in insects and plants. Indian J Exp Biol 52:73–79

    CAS  PubMed  Google Scholar 

  • Di Martino C, Delfine S, Pizzuto R, Loreto F, Fuggi A (2003) Free amino acids and glycine betaine in leaf osmoregulation of spinach responding to increasing salt stress. New Phytol 158:455–463

    Article  CAS  Google Scholar 

  • Dong L, Wang H, Niu J, Zou M, Wu N, Yu D, et al (2015) Echinacoside induces apoptotic cancer cell death by inhibiting the nucleotide pool sanitizing enzyme MTH1. Onco Targets Ther 8:3649–3664

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ellis BE (1983) Production of hydroxyphenylethanol glycosides in suspension cultures of Syringa vulgaris. Phytochem 22:1941–1943

    Article  CAS  Google Scholar 

  • Fan GZ, Wang XD, Li XC, Fan JSh, Zhai QL, Zhan YG (2011) Effect of fungal elicitor on carbon and nitrogen status and triterpenoid production in cell suspension cultures of Betula platyphylla Suk. J Med Plant Res 5(22):5413–5422

    CAS  Google Scholar 

  • Falahia H, Sharifia M, Zare Maivana H, Ahmadian Chashmi N (2017) Phenylethanoid glycosides accumulation in roots of Scrophularia striata as a response to water stress. Environ Exp Bot. https://doi.org/10.1016/j.envexpbot.2017.11.003

    Article  Google Scholar 

  • Flamini R, Rosso MD, Marchi FD, Vedova AD, Panighel A, Gardiman M, Maoz I, Bavaresco L (2013) An innovative approach to grape metabolomics: stilbene profiling by suspect screening analysis. Metabolomics 9:1243–125353

    Article  CAS  Google Scholar 

  • Fu GM, Pang HH, Wong YH (2008) Naturally occurring phenylethanoid glycosides: potential leads for new therapeutics. Curr Med Chem 15:2592–2613

    Article  CAS  PubMed  Google Scholar 

  • Galili G (2011) The aspartate-family pathway of plants: linking production of essential amino acids with energy and stress regulation. Plant Signal Behav 6:192–195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galili G (1995) Regulation of lysine and threonine synthesis. Plant Cell Tiss Organ Cult 7:899–906

    CAS  Google Scholar 

  • Hartig K, Beck E (2006) Crosstalk between auxin, cytokinins, and sugars in the plant cell cycle. Plant Biol 8:389–396

    Article  CAS  PubMed  Google Scholar 

  • Häusler RE, Heinrichs L, Schmitz J, Flugge UI (2014) How sugars might coordinate chloroplast and nuclear gene expression during acclimation to high light intensities. Mol Plant 7(7):1121–1137

    Article  PubMed  CAS  Google Scholar 

  • Heldt HW, Heldt F (2005) Plant Biochemisty. pp 435–454

  • Ingestad T, Kähr M (1985) Nutrition and growth of coniferous seedlings at varied relative nitrogen addition rate. Physiol Plant 65(2):109–116

    Article  Google Scholar 

  • Ingestad T, Lund AB (1979) Nitrogen stress in birch seedlings. Physiol Plant 45(1):137–148

    Article  CAS  Google Scholar 

  • Joshi V, Joung JG, Fei ZJ, Jander G (2010) Interdependence of threonine, methionine and isoleucine metabolism in plants: accumulation and transcriptional regulation under abiotic stress. Amino Acids 39(4):933–947

    Article  CAS  PubMed  Google Scholar 

  • Kamalipourazad M, Sharifia M, Zare Maivana H, Behmaneshb M, Ahmadian Chashmi N (2016) Induction of aromatic amino acids and phenylpropanoid compoundsin Scrophularia striata Boiss. cell culture in response tochitosan-induced oxidative stress. Plant Physiol Biochem 107:374–384

    Article  CAS  PubMed  Google Scholar 

  • Khanpour-Ardestani NS, Sharifi M, Behmanesh M (2015) Establishment of callus and cell suspension culture of Scrophularia striata Boiss: an in vitro approach for acteoside production. Cytotechnology 67(3):475–485

    Article  CAS  PubMed  Google Scholar 

  • Less H, Galili G (2008) Principal transcriptional programs regulating plant amino acid metabolism in response to abiotic stresses. Plant Physiol Biochem 147(1):16–330

    Google Scholar 

  • Mattsson M, Johansson E, Lundborg T, Larsson M, Larsson C-M (1991) Nitrogen Utilization in N-limited Barley during Vegetative and Generative Growth I. growth and nitrate uptake kinetics in vegetative cultures grown at different relative addition rates of nitrate-N. J Exp Bot 42(2):197–205

    Article  CAS  Google Scholar 

  • Moe LA (2013) Amino acids in the rhizosphere: from plants to microbes. Am J Bot 100(9):1692–1705

    Article  CAS  PubMed  Google Scholar 

  • Mooney BP, Miernyk JA, Randall DD (2002) The complex fate of alphaketoacids. Annu Rev Plant Biol 53:357–375

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Nunes-Nesi A, Fernie RA, Stitt M (2010) Metabolic and Signaling Aspects Underpinning the Regulation of Plant Carbon Nitrogen Interactions. Mol Plant 3(6):973–996

    Article  CAS  PubMed  Google Scholar 

  • Raamsdonk LM, Teusink B, Broadhurst D, Zhang N, Hayes A, Walsh MC, Berden JA, Brindle KM, Kell DB, Rowland JJ, Westerhoff HV, Dam KV, Oliver SG (2001) A functional genomics strategy that uses metabolome data to reveal the phenotype of silent mutations. Nat Biotechnol 19:45–50

    Article  CAS  PubMed  Google Scholar 

  • Radwanski ER, Last RL (1995) Tryptophan biosynthesis and metabolism: biochemical and molecular genetics. Plant Cell 7(7):921

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rao SR, Ravishankar GA (2002) Plant cell cultures: Chemical factories of secondary metabolites. Biotechnol Adv 20:101–153

    Article  CAS  PubMed  Google Scholar 

  • Rebeille F, Jabrin S, Bligny R, Loizeau K, Gambonnet B, Van Wilder V (2006) Methionine catabolism in Arabidopsis cells is initiated by a gamma-cleavage process and leads to S-methylcysteine and isoleucine syntheses. Proc Natl Acad Sci USA 103:15687–15692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodgers C, Barneix A (1989) The effect of N-deprivation on nitrate uptake and growth rate of two wheat cultivars selected for different fertility levels. Plant Physiol Biochem 27:387–392

    Google Scholar 

  • Roessner-Tunali U, Hegemann B, Lytovchenko A, Carrari F, Bruedigam C (2003) Metabolic profiling of transgenic tomato plants overexpressing hexokinase reveals that the influence of hexose phosphorylation diminishes during fruit development. Plant Physiol 133:84–99

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rolland F, Moore B, Sheen J (2002) Sugar sensing and signaling in plants. Plant Cell 14:S185–S205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruan YL (2012) Signaling roles of sucrose metabolism in plant development. Mol Plant 5:763–765

    Article  CAS  PubMed  Google Scholar 

  • Sadeghnezhad E, Sharifi M, Zare-Maivan H (2016) Profiling of acidic (amino and phenolic acids) and phenylpropanoids production in response to methyl jasmonate-induced oxidative stress in Scrophularia striata suspension cells. Planta 244:75–85

    Article  CAS  PubMed  Google Scholar 

  • Sakano K, Tazawa M (1984) Intracellular distribution of free amino acids between the vacuolar and extravacuolar compartments in internodal cells of Chara australis. Plant Cell Physiol 25(8):1477–1486

    Article  CAS  Google Scholar 

  • Saimaru H, Orihara Y (2010) Biosynthesis of acteoside in cultured cells of Olea europaea. J Nat Med 64:139–145

    Article  CAS  PubMed  Google Scholar 

  • Schlegel HG (1956) Die verwertung organischer säuren durch Chlorella im licht. Planta 47(5):510–526

    Article  CAS  Google Scholar 

  • Slocum RD (2005) Genes, enzymes and regulation of arginine biosynthesisin plants. Plant Physiol Biochem 43:729–745

    Article  CAS  PubMed  Google Scholar 

  • Steuer R, Kurths J, Fiehn O, Weckwerth W (2003) Interpreting correlations in metabolomic networks. Biochem Soc Trans 31:1476–1478

    Article  CAS  PubMed  Google Scholar 

  • Timm S, Florian A, Arrivault S, Stitt M, Fernie AR, Bauwe H (2012) Glycine decarboxylase controls photosynthesis and plant growth. FEBS Lett 586:3692–3697

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Ruan YL (2013) Regulation of cell division and expansion by sugar and auxin signaling. Front Plant Sci 4:163

    PubMed  PubMed Central  Google Scholar 

  • Weckwerth W, Loureiro M, Wenzel K, Fiehn O (2004) Differential metabolic networks unravel the effects of silent plant phenotypes. Proc Natl Acad Sci 101:7809–7814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Widhalm JR, Gutensohn M, Yoo H, Adebesin F, Qian Y, Guo L, Jaini R, Lynch JH, McCot RM, Shreve T, Thimmapuram J, Rhodes D, Morgan JA, Dudareva N (2015) Identification of a plastidial phenylalanine exporter that influences flux distribution through the phenylalanine biosynthetic network. Nat Commun. https://doi.org/10.1038/ncomms9142

    Article  PubMed  Google Scholar 

  • Winter G, Todd CD, Trovato M, Forlani G, Funck D (2015) Physiological implications of arginine metabolism in plants. Front Plant Sci. https://doi.org/10.3389/fpls.2015.00534

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao Y, Zhao J, Zhou C, Zhao C, Zhou H, LI Y, Zhang J, Li L, Hu C, Li W, Peng X, Lu X, Lin F, Xu G (2015) A metabolomics study delineating geographical location-associated primary metabolic changes in the leaves of growing tobacco plants by GC-MS and CE-MS. Scientific Reports 2015 5(1). https://doi.org/10.1038/srep16346

Download references

Author information

Authors and Affiliations

  1. Department of Plant Biology, Faculty of Biological Sciences, Tarbiat Modares University, Tehran, Iran

    Sedigheh Ahmadi-Sakha & Mohsen Sharifi

  2. School of Biology, College of Science, University of Tehran, Tehran, Iran

    Vahid Niknam

  3. Center of Excellence in Medicinal Plant Metabolites, Tarbiat Modares University, Tehran, Iran

    Mohsen Sharifi & Vahid Niknam

Authors
  1. Sedigheh Ahmadi-Sakha
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mohsen Sharifi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vahid Niknam
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mohsen Sharifi.

Additional information

Communicated by KX Tang.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ahmadi-Sakha, S., Sharifi, M. & Niknam, V. The linkage between phenylethanoid glycosides biosynthetic pathway and some aromatic amino acids and carbohydrates (rhamnose and glucose) in Scrophularia striata Boiss. cell culture. Plant Cell Tiss Organ Cult 147, 131–145 (2021). https://doi.org/10.1007/s11240-021-02113-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-021-02113-3

Keywords

Search

Navigation