Triterpenoid saponins in Aralia elata subjected to combined nutrient availability and light quality

Yuxiang SUN; Mingyang SUN; Huijia QIU; Long TAN; Shenglei GUO

doi:10.15835/nbha51113036

Authors

Yuxiang SUN Jilin University, School of Business and Management, Department of Human Resources Management, Changchun 130021 (CN)
Mingyang SUN Jilin Jianzhu University, College of Art and Design, Changchun, 130118 (CN)
Huijia QIU Jilin University, School of Business and Management, Department of Human Resources Management, Changchun 130021 (CN)
Long TAN Heilongjiang University of Chinese Medicine, College of Pharmacy, Harbin 150040; Heilongjiang University of Chinese Medicine, Key Laboratory of Basic and Application Research of Beiyao, Ministry of Education, Harbin 150040 (CN)
Shenglei GUO Heilongjiang University of Chinese Medicine, College of Pharmacy, Harbin 150040; Heilongjiang University of Chinese Medicine, Key Laboratory of Basic and Application Research of Beiyao, Ministry of Education, Harbin 150040 (CN)

DOI:

https://doi.org/10.15835/nbha51113036

Keywords:

Aralia elata (Miq.) Seem, araloside, fertility, light quality, triterpene saponins

Abstract

Combined light spectra and nitrogen (N) availability may modify contents of triterpenoid saponins (TSs) in leaves of Aralia elata (Miq.) Seem. In this study, A. elata seedlings were raised under light-emitting diode spectra in red- (26.6% red, 59.9% green, and 13.5% blue) and green-colours (12.6% red, 84.6% green, and 2.9% blue) both at a photosynthetic photon flux density of about 77.4 µmol m^-2 s^-1. N availability was employed at low and high rates of 30 and 90 mg kg^-1, respectively. Aralosides-A and -VI did not show any responses to either light or N treatments (ranges of 1.98‒3.75 mg g^-1 and 0.21‒1.41 mg g^-1, respectively). Compared to the green light, the red light resulted in greater growth but lower foliar N assimilation and aralosides-B (~0.7 mg g^-1) and -V concentrations (~16 mg kg^-1). The high N availability resulted in greater growth, biomass, foliar chlorophyl and protein concentrations but lower N assimilation and TS concentrations. We conclude that araloside B can be taken as an objective TS harvested in A. elata food-used leaves as a bioactive compound that can be adjusted by light and N manipulations.

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References

Bartnik M, Facey PC (2017). Glycosides. Chapter 8. In: Badal S, Delgoda R (Eds). Pharmacognosy. Academic Press, Boston, pp 101-161. https://doi.org/B978-0-12-802104-0.00008-1

Bradford MM (1976). Rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72:248-254. https://doi.org/10.1016/0003-2697(76)90527-3

Cheng Y, Liu H, Tong X, Liu Z, Zhang X, Chen Y, Wu F, Jiang X, Yu X (2021a). Effects of shading on triterpene saponin accumulation and related gene expression of Aralia elata (Miq.) Seem. Plant Physiology and Biochemistry 160:166-174. https://doi.org/10.1016/j.plaphy.2021.01.009

Cheng Y, Liu HB, Tong XJ, Liu ZM, Zhang X, Jiang XM, Yu XH (2021b). Somatic embryogenesis and triterpenoid saponin production in Aralia elata (Miq.) Seem. Scientia Horticulturae 285 https://doi.org/10.1016/j.scienta.2021.110162

Du J-R, Long F-Y, Chen C (2014). Research progress on natural triterpenoid saponins in the chemoprevention and chemotherapy of cancer. In: Bathaie SZ, Tamanoi F (Eds). The Enzymes. Academic Press, pp 95-130. https://doi.org/B978-0-12-802215-3.00006-9

Duan J, Xu C, Jacobs DF, Ma L, Wei H, Jiang L, Ren J (2013). Exponential nutrient loading shortens the cultural period of Larix olgensis seedlings. Scandinavian Journal of Forest Research 28(5):409-418. https://doi.org/10.1080/02827581.2013.778328

Duan YD, Guo BT, Zhang L, Li JX, Li S, Zhao WB, … Guo P (2022). Interactive climate-soil forces shape the spatial distribution of foliar N:P stoichiometry in Vaccinium uliginosum planted in agroforests of Northeast China. Frontiers in Ecology and Evolution 10:1065680. https://doi.org/10.3389/fevo.2022.1065680

Gao J, Zhang J, He C, Wang Q (2021). Effects of light spectra and 15N pulses on growth, leaf morphology, physiology, and internal nitrogen cycling in Quercus variabilis Blume seedlings. Plos One 16(7):e0243954. https://doi.org/10.1371/journal.pone.0243954

Gao Z, Khalid M, Jan F, Saeed ur R, Jiang X, Yu X (2019). Effects of light-regulation and intensity on the growth, physiological and biochemical properties of Aralia elata (miq.) seedlings. South African Journal of Botany 121:456-462. https://doi.org/10.1016/j.sajb.2018.12.008

Guo S, Wang H, Sui Y, Liu X, Tan L (2022). Bioactive extracts and association with C and N in Eleutherococcus senticosus subjected to chitosan nanoparticles in contrasting light spectra. Plos One 17(12):e0277233. https://doi.org/10.1371/journal.pone.0277233

Han F, Liang J, Yang BY, Kuang HX, Xia YG (2021). Identification and comparison of triterpene saponins in Aralia elata leaves and buds by the energy-resolved MSAll technique on a liquid chromatography/quadrupole time-of-flight mass spectrometry. Journal of Pharmaceutical and Biomedical Analysis 203:114176. https://doi.org/10.1016/j.jpba.2021.114176

He C, Gao J, Zhao Y, Liu J (2021). Root foraging precision of Pinus pumila (Pall.) Regel subjected to contrasting light spectra. Plants-Basel 10(7):1482. https://doi.org/10.3390/plants10071482

Kuang H-X, Sun H, Zhang N, Okada Y, Okuyama T (1996). Two new saponins, Congmuyenosides A and B, from the leaves of Aralia elata collected in Heilongjiang, China. Chemical & Pharmaceutical Bulletin 44(11):2183-2185. https://doi.org/10.1248/cpb.44.2183

Lavoie S, Pierra J, Legault J, Raminoson D, Lion Q, Mshvildadze V, Pichette A (2021). Isolation and characterization of triterpenoid saponins from leaves of Aralia nudicaulis L. Phytochemistry Letters 43:184-189. https://doi.org/10.1016/j.phytol.2021.04.004

Lee EB, Kim OJ, Kang SS, Jeong C (2005). Araloside A, an antiulcer constituent from the root bark of Aralia elata. Biological & Pharmaceutical Bulletin 28(3):523-526. https://doi.org/10.1248/bpb.28.523

Li HS (2000). Mechanism and Technology for Experiments in Plant Physiology and Biochemistry. Beijing: Higher Education Press.

Li X, Xia H, Wang J, Chen Q (2021a). Nutrient uptake and assimilation in fragrant rosewood (Dalbergia odorifera T.C. Chen) seedlings in growing media with un-composted spent mushroom residue. PLOS One 16(4):e0249534. https://doi.org/10.1371/journal.pone.0249534

Li XW, Chen QX, Lei HQ, Wang JW, Yang S, Wei HX (2018). Nutrient uptake and utilization by fragrant rosewood (Dalbergia odorifera) seedlings cultured with oligosaccharide addition under different lighting spectra. Forests 9(1):29. https://doi.org/10.3390/f9010029

Li XW, Xia HT, Wang JW, Chen QX (2021b). Nutrient uptake and assimilation in fragrant rosewood (Dalbergia odorifera TC Chen) seedlings in growing media with un-composted spent mushroom residue. Plos One 16(4) https://doi.org/10.1371/journal.pone.0249534

Liu P, Cao B, Wang YT, Wei ZP, Ye JF, Wei HX (2021). Spectral effect of streetlamps on urban trees: A simulated study on tissue water, nitrogen, and carbohydrate contents in maple and oak. Plos One 16(3) https://doi.org/10.1371/journal.pone.0248463

Luo Y, Lu S, Ai QD, Zhou P, Qin M, Sun GB, Sun XB (2019). SIRT1/AMPK and Akt/eNOS signaling pathways are involved in endothelial protection of total aralosides of Aralia elata (Miq) Seem against high-fat diet-induced atherosclerosis in ApoE-/- mice. Phytotherapy Research 33(3):768-778. https://doi.org/10.1002/ptr.6269

Luo YQ, Zhao SJ, Tang JY, Zhu H, Wei HX, Cui W, Wang MH, Guo P (2020). White-light emitting diodes' spectrum effect on photosynthesis and nutrient use efficiency in Podocarpus macrophyllus seedlings. Journal of Plant Nutrition 43(19):2876-2884. https://doi.org/10.1080/01904167.2020.1798999

Man S, Gao W, Zhang Y, Huang L, Liu C (2010). Chemical study and medical application of saponins as anti-cancer agents. Fitoterapia 81(7):703-714. https://doi.org/10.1016/j.fitote.2010.06.004

Panossian AG, Efferth T, Shikov AN, Pozharitskaya ON, Kuchta K, Mukherjee PK, … Wagner H (2021). Evolution of the adaptogenic concept from traditional use to medical systems: Pharmacology of stress- and aging-related diseases. Medical Research Reviews 41(1):630-703. https://doi.org/10.1002/med.21743

Ponou BK, Tanaka C, Teponno RB, Tapondjou AL, Miyamoto T (2021). Manniosides B-F, five new triterpenoid saponins from the leaves of Schefflera mannii (Hook.f.) Harms. Carbohydrate Research 502:108279. https://doi.org/10.1016/j.carres.2021.108279

Qin J, Yue X, Shang X, Fang S (2020). Nitrogen forms alter triterpenoid accumulation and related gene expression in Cyclocarya paliurus (Batalin) Iljinsk. seedlings. Forests 11(6):631. https://doi.org/10.3390/f11060631

Saito S, Sumita S, Tamura N, Nagamura Y, Nishida K, Ito M, Ishiguro I (1990). Saponins from the Leaves of Aralia elata SEEM.: Araliaceae. Chemical & Pharmaceutical Bulletin 38(2):411-414. https://doi.org/10.1248/cpb.38.411

Sawai S, Saito K (2011). Triterpenoid biosynthesis and engineering in plants. Frontiers in Plant Science 2(25):25. https://doi.org/10.3389/fpls.2011.00025

Shafiq I, Hussain S, Raza MA, Iqbal N, Ahsan Asghar M, Raza A, … Yang F (2021). Crop photosynthetic response to light quality and light intensity. Journal of Integrative Agriculture 20(1):4-23. https://doi.org/10.1016/s2095-3119(20)63227-0

Song Q, Xu L, Long W, Guo J, Zhang X (2022). Quality assessment and nutrient uptake and utilization in Luohan pine (Podocarpus macrophyllus) seedlings raised by chitosan spraying in varied LED spectra. Plos One 17(4):e0267632. https://doi.org/10.1371/journal.pone.0267632

Sun Y, Li B, Lin X, Xue J, Wang Z, Zhang H, Jiang H, Wang Q, Kuang H (2017a). Simultaneous determination of four triterpenoid saponins in Aralia elata leaves by HPLC-ELSD combined with hierarchical clustering analysis. Phytochemical Analysis 28(3):202-209. https://doi.org/10.1002/pca.2662

Sun YC, Li BM, Lin XT, Xue J, Wang ZB, Zhang HW, Jiang H, Wang QH, Kuang HX (2017b). Simultaneous determination of four triterpenoid saponins in Aralia elata leaves by HPLC-ELSD combined with hierarchical clustering analysis. Phytochemical Analysis 28(3):202-209. https://doi.org/10.1002/pca.2662

Tan L, Fan R, Sun H, Guo S (2021). Root foraging of birch and larch in heterogeneous soil nutrient patches under water deficit. Plos One 16(8):e0255848. https://doi.org/10.1371/journal.pone.0255848

Tang YJ, Liesche J (2017). The molecular mechanism of shade avoidance in crops-How data from Arabidopsis can help to identify targets for increasing yield and biomass production. Journal of Integrative Agriculture 16(6):1244-1255. https://doi.org/10.1016/s2095-3119(16)61434-x

Wang M, Xu XD, Xu HB, Wen FC, Zhang XP, Sun H, Yao F, Sun GB, Sun XB (2014). Effect of the total saponins of Aralia elata (Miq) Seem on cardiac contractile function and intracellular calcium cycling regulation. Journal of Ethnopharmacology 155(1):240-247. https://doi.org/10.1016/j.jep.2014.05.024

Wang R, Wang Y, Su Y, Tan JH, Luo XT, Li JY, He Q (2020). Spectral effect on growth, dry mass, physiology and nutrition in Bletilla striata seedlings: Individual changes and collaborated response. International Journal of Agriculture and Biology 24(1):125-132. https://doi.org/10.17957/ijab/15.1416

Wei HX, Chen GS, Chen X, Zhao HT (2020a). Growth and nutrient uptake in Aralia elata seedlings exposed to exponential fertilization under different illumination spectra. International Journal of Agriculture and Biology 23(3):644-652. https://doi.org/10.17957/ijab/15.1336

Wei HX, Chen GS, Chen X, Zhao HT (2021). Geographical distribution of Aralia elata characteristics correlated with topography and forest structure in Heilongjiang and Jilin Provinces, Northeast China. Journal of Forestry Research 32(3):1115-1125. https://doi.org/10.1007/s11676-020-01100-2

Wei HX, Chen X, Chen GS, Zhao HT (2019a). Foliar nutrient and carbohydrate in Aralia elata can be modified by understory light quality in forests with different structures at Northeast China. Annals of Forest Research 62(2):125-137. https://doi.org/10.15287/afr.2019.1395

Wei HX, Guo P, Zheng HF, He XY, Wang PJ, Ren ZB, Zhai C (2017). Micro-scale heterogeneity in urban forest soils affects fine root foraging by ornamental seedlings of Buddhist pine and Northeast yew. Urban Forestry & Urban Greening 28:63-72. https://doi.org/10.1016/j.ufug.2017.10.006

Wei HX, Hauer RJ, Chen GS, Chen X, He XY (2020b). Growth, nutrient assimilation, and carbohydrate metabolism in Korean Pine (Pinus koraiensis) seedlings in response to light spectra. Forests 11(1):44. https://doi.org/10.3390/f11010044

Wei HX, Ren J, Zhou JH (2013). Effect of exponential fertilization on growth and nutritional status in Buddhist pine (Podocarpus macrophyllus [Thunb.] D. Don) seedlings cultured in natural and prolonged photoperiods. Soil Science and Plant Nutrition 59(6):933-941. https://doi.org/10.1080/00380768.2013.864957

Wei HX, Zhao HT, Chen X (2019b). Foliar N:P stoichiometry in Aralia elata distributed on different slope degrees. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 47(3):887-895. https://doi.org/10.15835/nbha47311390

Wei HX, Zhao HT, Chen X, He XY (2020c). Secondary metabolites, carbohydrate accumulation, and nutrient uptake in Aralia elata (Miq.) Seem seedlings exposed to shoot cutting and different LED spectra. Acta Physiologiae Plantarum 42(11):162. https://doi.org/10.1007/s11738-020-03149-2

Wei W, Ye C, Huang HC, Yang M, Mei XY, Du F, He XH, Zhu SS, Liu YX (2020d). Appropriate nitrogen application enhances saponin synthesis and growth mediated by optimizing root nutrient uptake ability. Journal of Ginseng Research 44(4):627-636. https://doi.org/10.1016/j.jgr.2019.04.003

Xia Y-G, Guo X-D, Song Y, Liang J, Gong F-Q, Wang T-L, Yang B-Y, Kuang H-X (2019). A generic strategy based on gas phase decomposition of protonated and ammoninted precursors producing predictable MRM-MS ion pairs and collision energies for direct analysis of plant triterpene glycosides. Journal of Pharmaceutical and Biomedical Analysis 165:292-303. https://doi.org/10.1016/j.jpba.2018.12.007

Xu L, Zhang X, Zhang D, Wei H, Guo J (2019). Using morphological attributes for the fast assessment of nutritional responses of Buddhist pine (Podocarpus macrophyllus [Thunb.] D. Don) seedlings to exponential fertilization. Plos One 14(12):e0225708. https://doi.org/10.1371/journal.pone.0225708

Yang L, Jiang H, Yan M, Xing X, Guo X, Yang B, Wang Q, Kuang H (2018). UHPLC-MS/MS quantification combined with chemometrics for comparative analysis of different batches of raw, wine-processed, and salt-processed radix Achyranthis Bidentatae. Molecules 23(4):758. https://doi.org/10.3390/molecules23040758

Yu LL, Song CM, Sun LJ, Li LL, Xu ZG, Tang CM (2020). Effects of light-emitting diodes on tissue culture plantlets and seedlings of rice (Oryza sativa L.). Journal of Integrative Agriculture 19(7):1743-1754. https://doi.org/10.1016/s2095-3119(19)62793-0

Zhang JY, Cun Z, Wu HM, Chen JW (2020). Integrated analysis on biochemical profiling and transcriptome revealed nitrogen-driven difference in accumulation of saponins in a medicinal plant Panax notoginseng. Plant Physiology and Biochemistry 154:564-580. https://doi.org/10.1016/j.plaphy.2020.06.049

Zhang M, Liu G, Tang SH, Song SJ, Yamashita K, Manabe M, Kodama H (2006). Effect of five triterpenoid compounds from the buds of Aralia elata on stimulus-induced superoxide generation, tyrosyl phosphorylation and translocation of cytosolic compounds to the cell membrane in human neutrophils. Planta Medica 72(13):1216-1222. https://doi.org/10.1055/s-2006-951679

Zhao J, Chen X, Wei HX, Lv J, Chen C, Liu XY, Wen Q, Jia LM (2019). Nutrient uptake and utilization in Prince Rupprecht's larch (Larix principis-rupprechtii Mayr.) seedlings exposed to a combination of light-emitting diode spectra and exponential fertilization. Soil Science and Plant Nutrition 65(4):358-368. https://doi.org/10.1080/00380768.2019.1631715

Zhao Y, Wang Z, Xu S, Li Y, He C (2020). Nutrient assimilation and utilization in Korean pine (Pinus koraiensis) seedlings exposed to exponential fertilization under contrasting spectra. Communications in Soil Science and Plant Analysis 51(18):2414-2428. https://doi.org/10.1080/00103624.2020.1836210

Zhou C, Cui W, Yuan T, Cheng H, Su Q, Wei H, Guo P (2022). Root foraging behavior of two agronomical herbs subjected to heterogeneous P pattern and high Ca stress. Agronomy-Basel 12(3):624. https://doi.org/10.3390/agronomy12030624