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.
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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.
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.
About this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11240-023-02586-4