The Metabolite Content of the Post-Culture Medium of the Tree Fern Cyathea delgadii Sternb. Cell Suspension Cultured in the Presence of 2,4-D and BAP
Abstract
:1. Introduction
2. Results
2.1. Description of GC-MS Analysis Results
2.2. Description of LC-MS Analysis Results
3. Discussion
4. Material and Methods
4.1. Callus Induction and Cell Suspension Establishment
4.2. Metabolic Profiling of the Post-Culture Liquid Medium Using LC-MS and GC-MS Analyzes
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
References
- Large, M.F.; Braggins, J.E. Tree Ferns; CSIRO Publishing: Collingwood, VIC, Australia, 2004; pp. 1–123. [Google Scholar]
- Mikuła, A.; Pożoga, M.; Tomiczak, K.; Rybczyński, J.J. Somatic embryogenesis in ferns: A new experimental system. Plant Cell Rep. 2015, 34, 783–794. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Grzyb, M.; Wróbel-Marek, J.; Kurczyńska, E.; Sobczak, M.; Mikuła, A. Symplasmic isolation contributes to somatic embryo induction and development in the tree fern Cyathea delgadii Sternb. Plant Cell Physiol. 2020, 61, 1273–1284. [Google Scholar] [CrossRef]
- Tomaszewicz, W.; Cioć, M.; Dos Santos Szewczyk, K.; Grzyb, M.; Pietrzak, W.; Pawłowska, B.; Mikuła, A. Enhancing in vitro production of the tree fern Cyathea delgadii and modifying secondary metabolite profiles by LED lighting. Cells 2022, 11, 486. [Google Scholar] [CrossRef] [PubMed]
- Rybczynski, J.J.; Kaźmierczak, A.; Dos Santos Szewczyk, K.; Tomaszewicz, W.; Miazga-Karska, M.; Mikuła, A. Biotechnology of the thee fern Cyathea smithii (J.D. Hooker; Soft tree fern, Katote) II Cell suspension culture: Focusing on structure and physiology in the presence of 2,4-D and BAP. Cells 2022, 11, 1396. [Google Scholar] [CrossRef]
- Steward, F.C.; Caplin, S.M.; Millar, F.K. Investigations on growth and metabolism of plant cells. I. New techniques for the investigation of metabolism, nutrition and growth in undifferentiated cells. Ann. Bot. 1952, 16, 57–79. [Google Scholar] [CrossRef]
- Muir, W.; Hildebrand, A.C.; Riker, A.J. Plant tissue cultures produced from single isolated cells. Science 1954, 119, 877–878. [Google Scholar] [CrossRef]
- Yue, W.; Ming, Q.-L.; Lin, B.; Rahman, K.; Zheng, C.-J.; Han, T.; Qin, L.-P. Medicinal plant cell suspension culture: Pharmaceutical applications and high-yielding strategies for the desired secondary metabolites. Crit. Rev. Biotechnol. 2016, 36, 215–232. [Google Scholar] [CrossRef]
- Mir, M.V.; Kamili, A.N.; Hassan, Q.P.; Tyub, S. Effect of light and dark conditions on biomass accumulation and secondary metabolite production in suspension cultures of Artemisia amygdalina Decne. J. Himal. Ecol. Sustain. Dev. 2017, 12, 107–112. [Google Scholar]
- Mikuła, A.; Skierski, J.; Rybczyński, J.J. Somatic embryogenesis of Gentiana genus. III. Characterization of three-year-old embryogenic suspensions of G. pannonica originated from various seedling explants. Acta Physiol. Plant. 2002, 24, 311–322. [Google Scholar] [CrossRef]
- Wójcik, A.; Rybczyński, J.J. Electroporation and morphogenic potential of Gentiana kurroo (Royle) embryogenic cell suspension protoplasts. BioTechnologia 2015, 96, 19–29. [Google Scholar] [CrossRef] [Green Version]
- Rybczyński, J.J.; Wójcik, A.I. The effect of L-glutamine on the genetic transformation of embryogenic cell suspensions of gentian species (Gentiana lutea L., Gentiana cruciata L. and Gentiana kurroo Royle) using Agrobacterium tumefaciens. BioTechnologia 2019, 100, 5–18. [Google Scholar] [CrossRef]
- Vasil, I.K.; Vasil, V. Advances in cereal protoplast research. Physiol. Plant. 1992, 85, 279–283. [Google Scholar] [CrossRef]
- Teramoto, S.; Komamine, A. L-DOPA production in plant cell cultures. In Medicinal and Aromatic Plants, I. Biotechnology in Agriculture and Forestry; Bajaj, Y.P.S., Ed.; Springer: Berlin/Heidelberg, Germany, 1988; pp. 209–224.A. [Google Scholar] [CrossRef]
- Cai, Z.; Kastell, A.; Knorr, D.; Smetanska, I. Exudation: An expanding technique for continuous production and release of secondary metabolites from plant cell suspension and hairy root cultures. Plant Cell Rep. 2012, 31, 461–477. [Google Scholar] [CrossRef]
- Rhodes, M.J.C.; Hilton, M.; Parr, A.J.; Hamill, J.D.; Robis, R.J. Nicotine production by “hairy root” cultures of Nicotiana rustica: Fermentation and product recovery. Biotechnol. Lett. 1986, 8, 415–420. Available online: https://link.springer.com/article/10.1007/BF01026743 (accessed on 1 July 2022). [CrossRef]
- Payne, G.F.; Payne, N.N.; Shuler, M.L.; Asada, M. In situ adsorption for enhanced alkaloid production by Catarnathus roseus. Biotechnol. Lett. 1988, 10, 187–192. [Google Scholar] [CrossRef]
- Almagro, L.; López Perez, A.J.; Pedreño, M.A. New method to enhance ajmalicine production in Catharanthus roseus cell cultures based on the use of cyclodextrins. Biotechnol. Lett. 2011, 33, 381–385. [Google Scholar] [CrossRef] [Green Version]
- Ye, H.; Huang, L.L.; Chen, S.D.; Zhong, J.J. Pulsed electric field stimulates plant secondary metabolism in suspension cultures of Taxus chinensis. Biotechnol. Bioeng. 2004, 88, 788–795. [Google Scholar] [CrossRef]
- Zhang, C.H.; Fevereiro, P.S.; He, G.; Chen, Z. Enhanced paclitaxel productivity and release capacity of Taxus chinensis cell suspension cultures adapted to chitosan. Plant Sci. 2007, 172, 158–163. [Google Scholar] [CrossRef]
- Kajani, A.A.; Mofid, M.R.; Abolfazli, K.; Tafreshi, S.A.H. Encapsulated activated charcoal as a potent agent for improving taxane synthesis and recovery from cultures. Biotechnol. Appl. Biochem. 2010, 56, 71–76. [Google Scholar] [CrossRef]
- Lin, L.D.; Wu, J.Y. Enhancement of shikonin production in single- and two-phase suspension cultures of Lithospermum erythrorhizon cells using low-energy ultrasound. Biotechnol. Bioeng. 2002, 78, 81–88. [Google Scholar] [CrossRef]
- Komaraiah, P.; Ramakrishna, S.V.; Reddanna, P.; Kavi Kishor, P.B. Enhanced production of plumbagin in immobilized cells of Plumbago rosea by elicitation and in situ adsorption. J. Biotechnol. 2003, 101, 181–187. [Google Scholar] [CrossRef]
- Marczak, L.; Kawiak, A.; Lojkowska, E.; Stobiecki, M. Secondary metabolites in in vitro cultured pants of the genus Drosera. Phytochem. Anal. 2005, 16, 143–149. [Google Scholar] [CrossRef] [PubMed]
- Cao, H.; Chai, T.-T.; Wang, X.; Morais-Braga, M.F.B.; Yang, J.-H.; Wong, F.-C.; Wang, R.; Yao, H.; Cao, J.; Cornara, L.; et al. Phytochemicals from fern species: Potential for medicine applications. Phytochem. Rev. 2017, 16, 379–440. [Google Scholar] [CrossRef]
- Huang, Y.C.; Hwang, T.L.; Chang, C.S.; Yang, Y.L.; Shen, C.N.; Liao, W.Y.; Chen, S.C.; Liaw, C.C. Anti-inflammatory flavonoids from the rhizomes of Helminthostachys zeylanica. J. Nat. Prod. 2009, 72, 1273–1278. [Google Scholar] [CrossRef]
- Lafont, R.; Ho, R.; Raharivelomanana, P.; Dinan, L. Ecdysteroids in Ferns: Distribution, Diversity, Biosynthesis, and Functions. In Working with Ferns; Fernández, H., Revilla, M., Kumar, A., Eds.; Springer: New York, NY, USA, 2011; pp. 321–346. [Google Scholar] [CrossRef]
- Fons, F.; Froissard, D.; Bessière, J.-M.; Buatois, B.; Rapior, S. Biodiversity of Volatile Organic Compounds from Five French Ferns. Nat. Prod. Commun. 2010, 5, 1655–1658. [Google Scholar] [CrossRef] [Green Version]
- Baker, C.J.; O’Neill, N.R.; Deahl, K.; Lydon, J. Continuous production of extracellular antioxidants in suspension cells attenuates the oxidative burst detected in plant microbe interactions. Plant Physiol. Biochem. 2002, 40, 641–644. [Google Scholar] [CrossRef] [Green Version]
- Kim, Y.H.; Kim, Y.; Cho, E.; Kwak, S.; Kwon, S.; Bae, J.; Lee, B.; Meen, B.; Huh, G.H. Alterations in intracellular and extracellular activities of antioxidant enzymes during suspension culture of sweetpotato. Phytochemistry 2004, 65, 2471–2476. [Google Scholar] [CrossRef]
- Rybczyński, J.J.; Tomiczak, K.; Grzyb, M.; Mikuła, A. Morphogenic events in ferns: Single and multicellular explants in vitro. In Current Advances in Fern Research; Fernández, H., Ed.; Springer: Berlin/Heidelberg, Germany, 2018; pp. 99–120. [Google Scholar]
- Lutskii, A.E.; Gorokhova, N.I. Intramolecular hydrogen bonds and molecular dipole moments. Theor. Exp. Chem. 1971, 4, 532–534. Available online: https://link.springer.com/article/10.1007/BF00527035 (accessed on 1 July 2022). [CrossRef]
- Xia, X.; Cao, J.; Zheng, Y.; Wang, Q.; Xiao, J. Flavonoid concentrations and bioactivity of flavonoid extracts from 19 species of ferns from China. Ind. Crops Prod. 2014, 58, 91–98. [Google Scholar] [CrossRef]
- Zietz, M.; Weckmüller, A.; Schmidt, S.; Rohn, S.; Schreiner, M.; Krumbein, A.; Kroh, L.W. Genotypic and climatic influence on the antioxidant activity of flavonoids in Kale (Brassica oleracea var. sabellica). J. Agric. Food Chem. 2010, 58, 2123–2130. [Google Scholar] [CrossRef]
- Gullón, B.; Lú-Chau, T.A.; Moreira, M.T.; Lema, J.M.; Eibes, G. Rutin: A review on extraction, identification and purification methods, biological activities and approaches to enhance its bioavailability. Trends Food Sci. Technol. 2017, 67, 220–235. [Google Scholar] [CrossRef]
- Park, J.S.; Rho, H.S.; Kim, D.H.; Chang, I.S. Enzymatic preparation of kaempferol from green tea seed and its antioxidant activity. J. Agric. Food Chem. 2006, 54, 2951–2956. [Google Scholar] [CrossRef]
- Plaxton, W.C. The organization and regulation of plant glycolysis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1996, 47, 185–214. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Agarwal, R.; Mumtaz, H.; Ali, N. Role of inositol polyphosphates in programmed cell death. Mol. Cell Biochem. 2009, 328, 155–165. [Google Scholar] [CrossRef] [PubMed]
- Culbertson, M.C.; Temburnikar, K.W.; Sau, S.P.; Liao, J.-Y.; Bala, S.; Chaput, J.C. Evaluating TNA stability under simulated physiological conditions. Bioorg. Med. Chem. Lett. 2016, 26, 2418–2421. [Google Scholar] [CrossRef] [Green Version]
- Silva, G.B.; Ionashiro, M.; Carrara, T.B.; Crivellari, A.C.; Tiné, M.A.S.; Prado, J.; Carpita, N.C.; Buckeridge, M.S. Cell wall polysaccharides from fern leaves: Evidence for a mannan-rich Type III cell wall in Adiantum raddianum. Phytochemistry 2011, 72, 2352–2360. [Google Scholar] [CrossRef]
- Loewus, F.A.; Murthy, P.P.N. myo-Inositol metabolism in plants. Plant Sci. 2000, 150, 1–19. [Google Scholar] [CrossRef]
- Popper, Z.A.; Fry, S.C. Primary cell wall composition of pteridophytes and spermatophytes. New Phytol. 2004, 164, 165–174. [Google Scholar] [CrossRef] [PubMed]
- Matsunaga, T.; Ishii, T.; Matsumoto, S.; Higuchi, M.; Darvill, A.; Albersheim, P.; O’Neill, M.A. Occurrence of the primary cell wall in polysaccharide rhamnogalacturonan II in Pteridophytes, Lycophytes, and Bryophytes. Implications for the evolution of vascular plants. Plant Physiol. 2004, 134, 339–351. [Google Scholar] [CrossRef]
- Eda, S.; Kodama, H.; Akiyama, Y.; Mori, M.; Kato, K.; Ishizu, A.; Nakano, J. An arabinoxyloglucan from the cell walls of suspension-cultured tobacco cells. Agric. Biol. Chem. 1983, 47, 1791–1979. [Google Scholar] [CrossRef]
- Akiyama, Y.; Eda, S.; Mori, M.; Katō, K. An arabinoglucuromannan from extracellular polysaccharides of suspension-cultured tobacco cells. Agric. Biol. Chem. 1984, 48, 403–407. [Google Scholar] [CrossRef]
- Grembecka, M. Sugar alcohols—Their role in the modern world of sweeteners: A review. Eur. Food Res. Technol. 2015, 241, 1–14. [Google Scholar] [CrossRef] [Green Version]
- Tomiczak, K.; Mikuła, A.; Rybczyński, J.J. Protoplast culture and somatic cell hybridization of Gentians. In The Gentianaceae—Volume 2: Biotechnology and Applications; Rybczyński, J.J., Davey, M.R., Mikuła, A., Eds.; Springer: Berlin/Heidelberg, Germany, 2015; pp. 163–185. [Google Scholar] [CrossRef]
- Murashige, T.; Skoog, F. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 1962, 15, 473–497. [Google Scholar] [CrossRef]
- Moing, A. Sugar alcohols as carbohydrate reserves in some higher plants. Dev. Crop Sci. 2000, 26, 337–358. [Google Scholar] [CrossRef]
- Grembecka, M. Sugar alcohols. In Encyclopedia of Analytical Science, 3rd ed.; Worsfold, P., Poole, C., Townshend, A., Miró, M., Eds.; Elsevier: Amsterdam, The Netherlands, 2019; pp. 290–299. [Google Scholar] [CrossRef]
- Zamil, M.S.; Geitmann, A. The middle lamella-more than a glue. Phys. Biol. 2017, 14, 015004. [Google Scholar] [CrossRef]
- Mikuła, A.; Rybczyński, J.J.; Skierski, J.; Latkowska, M.J.; Fiuk, A. Somatic embryogenesis of Gentiana genus IV: Characterisation of Gentiana cruciata and Gentiana tibetica embryogenic cell suspensions. In Liquid Culture Systems for In Vitro Plant Propagation; Hvoslef-Eide, A.K., Preis, W., Eds.; Springer: Berlin/Heidelberg, Germany, 2005; pp. 345–358. [Google Scholar] [CrossRef]
- Aid, F. Plant Lipid Metabolism. In Advances in Lipid Metabolism; Valenzuela, R., Ed.; IntechOpen: London, UK, 2019. [Google Scholar] [CrossRef]
- Pighin, J.A.; Zheng, H.; Balakshin, L.J.; Goodman, I.P.; Western, T.L.; Jetter, R.; Kunst, L.; Samuels, A.L. Plant cuticular lipid export requires an ABC transporter. Science 2004, 306, 702–704. [Google Scholar] [CrossRef] [Green Version]
- Ishaq, M.S.; Hussain, M.M.; Afridi, M.S.; Ali, G.; Khattak, M.; Ahmad, S.; Shakirullah. In vitro phytochemical, antibacterial, and antifungal activities of leaf, stem, and root extracts of Adiantum capillus-veneris. Sci. World J. 2014, 2014, 269793. Available online: https://www.hindawi.com/journals/tswj/2014/269793 (accessed on 1 July 2022). [CrossRef] [PubMed]
- Salatino, M.L.F.; Prado, J. Flavonoid glycosides of Pteridaceae from Brazil. Biochem. Syst. Ecol. 1998, 26, 761–769. [Google Scholar] [CrossRef]
- Zhao, Z.; Ruan, J.; Jin, J.; Zhu, C.; Yu, Y. Two new flavonoids from the rhizomes of Abacopteris penangiana. Helv. Chim. Acta 2011, 94, 446–452. Available online: https://onlinelibrary.wiley.com/doi/10.1002/hlca.201000223 (accessed on 1 July 2022). [CrossRef]
- Liu, H.; Orjala, J.; Sticher, O.; Rali, T. Acylated flavonol glycosides from leaves of Stenochlaena palustris. J. Nat. Prod. 1999, 62, 70–75. [Google Scholar] [CrossRef]
- Iwashina, T.; Matsumoto, S. Flavonoid glycosides from the fern, Schizaea (Schizaeaceae) in South Pacyfic region, and their distribution pattern. Bull. Natl. Mus. Nat. Sci. Ser. B 2013, 39, 195–201. [Google Scholar]
- Kachlicki, P.; Piasecka, A.; Stobiecki, M.; Marczak, Ł. Structural Characterization of Flavonoid Glycoconjugates and Their Derivatives with Mass Spectrometric Techniques. Molecules 2016, 21, 1494. [Google Scholar] [CrossRef] [Green Version]
- Konieczny, R.; Bohdanowicz, J.; Czaplicki, A.Z.; Przywara, L. Extracellular matrix surface network during plant regeneration in wheat anther culture. Plant Cell Tiss. Org. Cult. 2005, 83, 201–208. [Google Scholar] [CrossRef]
- Popielarska-Konieczna, M.; Kozieradzka-Kiszkurno, M.; Świerczyńska, J.; Góralski, H.; Ślesak, G.; Bohdanowicz, J. Ultrastructure and histochemical analysis of extracellular matrix surface network in kiwifruit endosperm-derived callus culture. Plant Cell Rep. 2008, 27, 1137–1145. [Google Scholar] [CrossRef]
- Joyce, B.L.; Eda, S.; Dunlap, J.; Steward, C.N. Morphology and ploidy level determination of Pteris vittata callus during induction and regeneration. BMC Biotechnol. 2014, 14, 96. [Google Scholar] [CrossRef] [Green Version]
- Ferreyra, M.L.F.; Rius, S.P.; Casati, P. Flavonoids: Biosynthesis, biological functions, and biotechnological applications. Front. Plant Sci. 2012, 3, 222. [Google Scholar] [CrossRef]
Number | Class of Metabolites | Number of Metabolites | Retention Time [min] | |
---|---|---|---|---|
Minimal Value | Maximal Value | |||
1. | Alcohols | 4 | 9.323 | 17.473 |
2. | Amines | 4 | 6.976 | 19.088 |
3. | Amino acids | 10 | 7.344 | 15.272 |
4. | Fatty acids | 12 | 7.854 | 21.806 |
5. | Nucleic acids components | 5 | 7.456 | 12.582 |
6. | Organic acids | 29 | 6.286 | 24.531 |
7. | Phenolics | 6 | 11.850 | 19.143 |
8. | Phosphates | 6 | 6.653 | 21.541 |
9. | Sugars | 27 | 11.708 | 32.775 |
10. | Sugar alcohols | 15 | 12.381 | 25.146 |
11. | Others | 12 | 6.038 | 19.556 |
No. | Compound | Polarity Ion Mode | Molecular Formula | Obtained m/z | Calculated m/z | Error [ppm] | Biological Role /Activity c |
---|---|---|---|---|---|---|---|
1 | aromadendrin 7-O- (hydroxyferuloyl- glucoside) a | - | C31H30O15 | 641.1461 | 641.1512 | −4.6 | Anti-inflammatory, antioxidant, antidiabetic, ROS scavenger |
2 | kaempferol 3-O-rutinoside (rhamnosyl-glucoside) a | - | C27H29O15 | 593.1426 | 593.1512 | −2.55 | In plants ROS scavenger |
3 | aromadendrin 7-O- (hydroxyferuloyl- rhamnoside) a | - | C31H30O14 | 625.1518 | 625.1562 | −3.71 | Anti-HIV-1 activity |
4 | naringenin 7-O- (hydroxyferuloyl- rhamnoside) a | - | C31H30O13 | 609.1626 | 609.1613 | −2.0 | Anti-inflammatory properties, antifibrogenic effects |
5 | quercetin 3-O-rutinoside–(rhamnosyl-glucoside) b | + | C31H30O13 | 633.1967 | 633.1426 | 4.47 | Reduction of the levels of oxidative stress in the colon, ROS scavenger, pharmacological benefits for the treatment of various chronic diseases such as cancer, diabetes, hypertension and hypercholesterolemia |
6 | quercetin rhamnoside | - | C27H30O16 [sodiated ion] | 447.1200 | 447.0932 | 3.08 | Cytotoxic effect on breast cancer, ROS scavenger |
7 | 1,5-dicaffeoylquinic acid (Cynarin) a | - | C25H24O12 | 515.1098 | 515.1195 | 2.07 | Protective role in the control of oxidative damage, ROS scavenger |
8 | chlorogenic acid b | - | C16H18O9 | 353.0859 | 353.0878 | 1.12 | Anti-cancer activity, functioning as an intermediate in lignin biosynthesis |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Rybczyński, J.J.; Marczak, Ł.; Stobiecki, M.; Strugała, A.; Mikuła, A. The Metabolite Content of the Post-Culture Medium of the Tree Fern Cyathea delgadii Sternb. Cell Suspension Cultured in the Presence of 2,4-D and BAP. Int. J. Mol. Sci. 2022, 23, 11783. https://doi.org/10.3390/ijms231911783
Rybczyński JJ, Marczak Ł, Stobiecki M, Strugała A, Mikuła A. The Metabolite Content of the Post-Culture Medium of the Tree Fern Cyathea delgadii Sternb. Cell Suspension Cultured in the Presence of 2,4-D and BAP. International Journal of Molecular Sciences. 2022; 23(19):11783. https://doi.org/10.3390/ijms231911783
Chicago/Turabian StyleRybczyński, Jan J., Łukasz Marczak, Maciej Stobiecki, Aleksander Strugała, and Anna Mikuła. 2022. "The Metabolite Content of the Post-Culture Medium of the Tree Fern Cyathea delgadii Sternb. Cell Suspension Cultured in the Presence of 2,4-D and BAP" International Journal of Molecular Sciences 23, no. 19: 11783. https://doi.org/10.3390/ijms231911783