Skip to main content
Log in

Integration of phenylalanine precursor feeding and elicitor treatment in concert with the cellulase-assisted extraction approach to improve stilbene compound production

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

Abstract

Trans-resveratrol, trans-arachidin-1 (Ara-1), and trans-arachidin-3 (Ara-3) are major stilbene compounds found in elicited peanut hairy root culture and exert diverse potential biological and pharmaceutical activities. The aim of this study was to investigate the various approaches for enhancing the productivity of prenylated stilbene. The fast-growing peanut hairy root K2-K599-C line was elicited with chitosan (CHT), methyl jasmonate (MeJA), and cyclodextrin (CD) (CHT + MeJA + CD) as combined elicitors together with phenylalanine (Phe) as a precursor to feeding at 24, 48, and 72 h. The accumulation of stilbene compounds was investigated in this study as well as stilbene biosynthesis-related genes and plant defense gene expression. Upon an exogenous supply of Phe, elevated amounts of Ara-1 and Ara-3 were detected through the entire 72 h elicitation period while the non-Phe precursor feeding conditions exhibited an increasing amount of Ara-1 and Ara-3 up to 48 h, decreasing at 72 h. In addition, Phe precursor may serve as an early regulator of gene expression for the stilbene biosynthesis pathway, transcription factors, and pathogenesis-related proteins while a delayed response in transcriptional regulation was observed in the elicitation without Phe precursor feeding. Cellulase-assisted extraction was performed prior to solvent extraction of the culture medium. The results indicated a significant 1.73- and 1.57-fold increase in Ara-1 and Ara-3, respectively, compared to the non-cellulase-assisted process. To the best of our knowledge, this is the first study to propose an integrated approach to improving stilbene compound production in peanut hairy root culture.

Key message

An integrated approach of precursor feeding, elicitors, and enzyme-assisted extraction facilitates the improvement of stilbene compound production. Phenylalanine feeding induces early transcriptional regulation of plant response. Cellulase-assisted extraction improves the recovery of stilbene compounds.

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
Fig. 8
Fig. 9

Similar content being viewed by others

Data availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  • Ahlawat S, Saxena P, Alam P, Wajid S, Abdin MZ (2014) Modulation of artemisinin biosynthesis by elicitors, inhibitor, and precursor in hairy root cultures of Artemisia annua L. J Plant Interact 9(1):811–824. https://doi.org/10.1080/17429145.2014.949885

    Article  CAS  Google Scholar 

  • Balasubramani S, Ranjitha Kumari BD, Moola AK, Sathish D, Prem Kumar G, Srimurali S, Babu Rajendran R (2021) Enhanced production of β-caryophyllene by farnesyl diphosphate precursor-treated callus and hairy root cultures of Artemisia vulgaris L. Front Plant Sci. https://doi.org/10.3389/fpls.2021.634178

    Article  PubMed  PubMed Central  Google Scholar 

  • Butaye KMJ, Cammue BPA, Delauré SL, De Bolle MFC (2005) Approaches to minimize variation of transgene expression in plants. Mol Breed 16(1):79–91. https://doi.org/10.1007/s11032-005-4929-9

    Article  Google Scholar 

  • Chayjarung P, Kongbangkerd A, Limmongkon A (2020) Optimization of chitosan concentration for stilbene compound induction in Kalasin 2 peanut hairy root culture. Proceedings of the 50th national graduate research conference. King Mongkut’s Institute of Technology Ladkrabang. pp. 8–15

  • Chayjarung P, Poonsap W, Pankaew C, Inmano O, Kongbangkerd A, Limmongkon A (2021) Using a combination of chitosan, methyl jasmonate, and cyclodextrin as an effective elicitation strategy for prenylated stilbene compound production in Arachis hypogaea L. hairy root culture and their impact on genomic DNA. Plant Cell Tissue Organ Cult (PCTOC). https://doi.org/10.1007/s11240-021-02112-4

    Article  Google Scholar 

  • Chen N, Yang Q, Pan L, Chi X, Chen M, Hu D, Yang Z, Wang T, Wang M, Yu S (2014) Identification of 30 MYB transcription factor genes and analysis of their expression during abiotic stress in peanut (Arachis hypogaea L.). Gene 533(1):332–345. https://doi.org/10.1016/j.gene.2013.08.092

    Article  CAS  PubMed  Google Scholar 

  • Chong J, Poutaraud A, Hugueney P (2009) Metabolism and roles of stilbenes in plants. Plant Sci 177(3):143–155. https://doi.org/10.1016/j.plantsci.2009.05.012

    Article  CAS  Google Scholar 

  • Constabel CP, Brisson N (1992) The defense-related STH—2 gene product of potato shows race-specific accumulation after inoculation with low concentrations of Phytophthora infestans zoospores. Planta 188(3):289–295

    Article  CAS  PubMed  Google Scholar 

  • Cui M, Haider MS, Chai P, Guo J, Du P, Li H, Dong W, Huang B, Zheng Z, Shi L, Zhang X, Han S (2021) Genome-wide identification and expression analysis of AP2/ERF transcription factor related to drought stress in cultivated peanut (Arachis hypogaea L.). Front Genet. https://doi.org/10.3389/fgene.2021.750761

    Article  PubMed  PubMed Central  Google Scholar 

  • Djoko B, Chiou RY, Shee JJ, Liu YW (2007) Characterization of immunological activities of peanut stilbenoids, arachidin-1, piceatannol, and resveratrol on lipopolysaccharide-induced inflammation of RAW 264.7 macrophages. J Agric Food Chem 55(6):2376–2383. https://doi.org/10.1021/jf062741a

    Article  CAS  PubMed  Google Scholar 

  • Ghandahari Yazdi AP, Barzegar M, Sahari MA, Ahmadi Gavlighi H (2019) Optimization of the enzyme-assisted aqueous extraction of phenolic compounds from pistachio green hull. Food Sci Nut 7(1):356–366. https://doi.org/10.1002/fsn3.900

    Article  CAS  Google Scholar 

  • Inyai C, Yusakul G, Komaikul J, Kitisripanya T, Likhitwitayawuid K, Sritularak B, Putalun W (2021) Improvement of stilbene production by mulberry Morus alba root culture via precursor feeding and co-elicitation. Bioprocess Biosyst Eng 44(4):653–660. https://doi.org/10.1007/s00449-020-02474-7

    Article  CAS  PubMed  Google Scholar 

  • Javid A, Gampe N, Gelana F, György Z (2021) Enhancing the accumulation of rosavins in Rhodiola rosea L. plants grown in vitro by precursor feeding. Agronomy 11(12):2531

    Article  CAS  Google Scholar 

  • Jeandet P, Vannozzi A, Sobarzo-Sánchez E, Uddin MS, Bru R, Martínez-Márquez A, Clément C, Cordelier S, Manayi A, Nabavi SF, Rasekhian M, El-Saber Batiha G, Khan H, Morkunas I, Belwal T, Jiang J, Koffas M, Nabavi SM (2021) Phytostilbenes as agrochemicals: biosynthesis, bioactivity, metabolic engineering and biotechnology. Nat Prod Rep 38(7):1282–1329. https://doi.org/10.1039/D0NP00030B

    Article  CAS  PubMed  Google Scholar 

  • Jeandet P, Uddin MS, Clément C, Aziz A, Jacquard C, Khan H, Shah MA, Barka EA, Koffas M, Nabavi SM, Sobarzo-Sánchez E, Renault J-H (2023) Production of high molecular-ordered stilbene oligomers for the study of their biological activity: total synthesis, bio-catalyzed synthesis and production by plant systems electronic supplementary information (ESI). Nat Prod Rep 40(5):1045–1057. https://doi.org/10.1039/d2np00073c. See DOI

    Article  CAS  PubMed  Google Scholar 

  • Kundu S, Salma U, Ali MN, Hazra AK, Mandal N (2018) Development of transgenic hairy roots and augmentation of secondary metabolites by precursor feeding in Sphagneticola calendulacea (L.) Pruski. Ind Crops Prod 121:206–215. https://doi.org/10.1016/j.indcrop.2018.05.009

    Article  CAS  Google Scholar 

  • Li H, Wu WK, Zheng Z, Che CT, Li ZJ, Xu DD, Wong CC, Ye CG, Sung JJ, Cho CH, Wang M (2010) 3,3’,4,5,5’-Pentahydroxy-trans-stilbene, a resveratrol derivative, induces apoptosis in colorectal carcinoma cells via oxidative stress. Eur J Pharmacol 637(1–3):55–61. https://doi.org/10.1016/j.ejphar.2010.04.009

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Osbourn A, Ma P (2015) MYB transcription factors as regulators of phenylpropanoid metabolism in plants. Mol Plant 8(5):689–708. https://doi.org/10.1016/j.molp.2015.03.012

    Article  CAS  PubMed  Google Scholar 

  • Mohammadhosseinpour S, Ho LC, Fang L, Xu J, Medina-Bolivar F (2022) Arachidin-1, a prenylated stilbenoid from peanut, induces apoptosis in triple-negative breast cancer cells. Int J Mol Sci 23(3):1139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pilaisangsuree V, Somboon T, Tonglairoum P, Keawracha P, Wongsa T, Kongbangkerd A, Limmongkon A (2018) Enhancement of stilbene compounds and anti-inflammatory activity of methyl jasmonate and cyclodextrin elicited peanut hairy root culture. Plant Cell Tissue Organ Cult 132(1):165–179. https://doi.org/10.1007/s11240-017-1321-5

    Article  CAS  Google Scholar 

  • Pontillo ARN, Papakosta-Tsigkri L, Lymperopoulou T, Mamma D, Kekos D, Detsi A (2021) Conventional and enzyme-assisted extraction of rosemary leaves (Rosmarinus officinalis L.): toward a greener approach to high added-value extracts. Appl Sci 11(8):3724

    Article  CAS  Google Scholar 

  • Qu J, Zhang W, Yu X (2011) A combination of elicitation and precursor feeding leads to increased anthocyanin synthesis in cell suspension cultures of Vitis vinifera. Plant Cell Tissue Organ Cult (PCTOC) 107(2):261–269. https://doi.org/10.1007/s11240-011-9977-8

    Article  CAS  Google Scholar 

  • Rakesh B, Praveen N (2022) Elicitor and precursor-induced approaches to enhance the in vitro production of L-DOPA from cell cultures of Mucuna pruriens. Ind Crops Prod 188:115735. https://doi.org/10.1016/j.indcrop.2022.115735

    Article  CAS  Google Scholar 

  • Rasool F, Uzair M, Naeem MK, Rehman N, Afroz A, Shah H, Khan MR (2021) Phenylalanine ammonia-lyase (PAL) genes family in wheat (Triticum aestivum L.): genome-wide characterization and expression profiling. Agronomy 11(12):2511

    Article  CAS  Google Scholar 

  • Sharma AR, Gajurel G, Ahmed I, Roedel K, Medina-Bolivar F (2022) Induction of the prenylated stilbenoids arachidin-1 and arachidin-3 and their semi-preparative separation and purification from hairy root cultures of peanut (Arachis hypogaea L.). Molecules 27:6118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sivanandhan G, Selvaraj N, Ganapathi A, Manickavasagam M (2014) Enhanced biosynthesis of withanolides by elicitation and precursor feeding in cell suspension culture of Withania somnifera (L.) dunal in shake-flask culture and bioreactor. PLoS ONE 9(8):e104005. https://doi.org/10.1371/journal.pone.0104005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sobolev VS, Khan SI, Tabanca N, Wedge DE, Manly SP, Cutler SJ, Coy MR, Becnel JJ, Neff SA, Gloer JB (2011) Biological activity of peanut (Arachis hypogaea) phytoalexins and selected natural and synthetic stilbenoids. J Agric Food Chem 59(5):1673–1682. https://doi.org/10.1021/jf104742n

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Somboon T, Chayjarung P, Pilaisangsuree V, Keawracha P, Tonglairoum P, Kongbangkerd A, Wongkrajang K, Limmongkon A (2019) Methyl jasmonate and cyclodextrin-mediated defense mechanism and protective effect in response to paraquat-induced stress in peanut hairy root. Phytochemistry 163:11–22. https://doi.org/10.1016/j.phytochem.2019.03.017

    Article  CAS  PubMed  Google Scholar 

  • Szkudelski T, Szkudelska K (2011) Anti-diabetic effects of resveratrol. Annals of the New York Academy of Sciences 1215(1):34–39. https://doi.org/10.1111/j.1749-6632.2010.05844.x

    Article  CAS  PubMed  Google Scholar 

  • Tothong C, Kongbangkerd A, Limmongkon A (2022) Production of stilbene compounds from peanut hairy root culture elicited with a mixture of chitosan, methyl jasmonate, and cyclodextrin. Proceeding of the 17th international symposium of the protein society of Thailand (PST2022). Chiangmai, Thailand. pp. 1–6

  • Xu Q, Zhou Y, Wu Y, Jia Q, Gao G, Nie F (2016) Enzyme-assisted solvent extraction for extraction of blueberry anthocyanins and separation using resin adsorption combined with extraction technologies. Int J Food Sci Technol 51(12):2567–2573. https://doi.org/10.1111/ijfs.13240

    Article  CAS  Google Scholar 

  • Yang T, Fang L, Nopo-Olazabal C, Condori J, Nopo-Olazabal L, Balmaceda C, Medina-Bolivar F (2015) Enhanced production of resveratrol, piceatannol, arachidin-1, and arachidin-3 in hairy root cultures of peanut co-treated with methyl jasmonate and cyclodextrin. J Agric Food Chem 63(15):3942–3950. https://doi.org/10.1021/jf5050266

    Article  CAS  PubMed  Google Scholar 

  • Zhang LX, Li CX, Kakar MU, Khan MS, Wu PF, Amir RM, Dai DF, Naveed M, Li QY, Saeed M, Shen JQ, Rajput SA, Li JH (2021) Resveratrol (RV): a pharmacological review and call for further research. Biomed Pharmacother 143:112164. https://doi.org/10.1016/j.biopha.2021.112164

    Article  CAS  PubMed  Google Scholar 

  • Zhao N, He M, Li L, Cui S, Hou M, Wang L, Mu G, Liu L, Yang X (2020) Identification and expression analysis of WRKY gene family under drought stress in peanut (Arachis hypogaea L.). PLoS ONE 15(4):e0231396. https://doi.org/10.1371/journal.pone.0231396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zu Y, Wang Y, Fu Y, Li S, Sun R, Liu W, Luo H (2009) Enzyme-assisted extraction of paclitaxel and related taxanes from needles of Taxus chinensis. Sep Purif Technol 68(2):238–243. https://doi.org/10.1016/j.seppur.2009.05.009

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by Agricultural Research Development Agency (Public Organization), Thailand 2022.

Funding

This study was funded by Agricultural Research Development Agency (Public Organization), Thailand 2022.

Author information

Authors and Affiliations

Authors

Contributions

CT: Conceptualization, Methodology, Validation, Formal analysis, Investigation. CP: Investigation, Formal analysis. PC: Validation, Investigation. AK: Resources, Visualization. AL: Conceptualization, Supervision, Visualization, Writing—Review & Editing.

Corresponding author

Correspondence to Apinun Limmongkon.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Christophe Hano.

Publisher’s Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 17.3 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tothong, C., Pankaew, C., Chayjarung, P. et al. Integration of phenylalanine precursor feeding and elicitor treatment in concert with the cellulase-assisted extraction approach to improve stilbene compound production. Plant Cell Tiss Organ Cult 155, 665–679 (2023). https://doi.org/10.1007/s11240-023-02586-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-023-02586-4

Keywords

Navigation