Effect of far-red light on the production and diversity of ginsenosides in leaves of Panax ginseng Meyer
Applied Biological Chemistry volume 66, Article number: 16 (2023)
Ginsenosides are the most valuable and pharmacologically active triterpenoid saponins found in Panax ginseng. Although light quality affects ginsenoside content, little is known about the underlying genetic and regulatory mechanisms. Additionally, the correlation between the adaptability of ginseng to shade and ginsenoside biosynthesis remains poorly understood. In the present study, transcriptome analysis of ginseng seedlings using RNA sequencing revealed that the expression of ginsenoside biosynthesis genes, including PgHMGR, PgFPS, PgSS, and PgUGT, was enhanced in shade conditions but downregulated by red light, indicating that far-red light might play an essential role in ginsenoside production. Further, gene expression analysis in adventitious roots and 2-year-old plants using qRT-PCR showed that the light quality-mediated expression patterns of ginsenoside genes varied with tissue and age. However, unlike the transcriptome, there was no difference in the total ginsenoside content in seedlings among various light conditions. Nevertheless, the amount of major protopanaxadiol-type ginsenosides increased under shade and red light conditions. Unlike seedlings and adventitious roots, there was a decrease in the expression of PgHMGR, PgFPS, PgSS, and PgDDS in 2-year-old plants, along with an increase in the ginsenoside content, under far-red light. Taken together, our findings suggest that far-red light is an important environmental factor for ginsenoside biosynthesis and diversification and provide information that can improve the quality of ginseng produced for medicinal purposes.
Plants depend on light for various processes during their growth and development, such as germination, photomorphogenesis, photosynthesis, and other metabolic processes [1, 2]. In addition to orchestrating the biosynthesis of primary metabolites (PMs), light also affects the biosynthesis and accumulation of secondary metabolites (SMs) [2, 3]. While PMs are crucial for growth and development, SMs play a vital role in plant fitness under diverse environmental conditions [2, 4, 5]. The biosynthesis of SMs is greatly influenced by environmental factors that include several biotic and abiotic stresses as well as variations in light [6,7,8,9]. Transcriptomic analysis of plants, such as Arabidopsis and rice (Oryza sativa), has shown that light determines morphogenesis and functional metabolite production through changes in gene expression patterns [10,11,12]. In addition, appropriate quality and intensity of light are crucial for the accumulation of secondary metabolites [2, 5, 13,14,15,16,17]. Specific wavelengths in the light spectrum are responsible for the induction of SM biosynthesis along with their composition and content . In the visible light spectrum, blue light (BL; 400–500 nm) and red light (RL; 600–700 nm) affect the accumulation of SMs in medicinal plants .
Panax ginseng is a perennial herbaceous plant of the Araliaceae family widely used in traditional medicine. The pharmacological benefits of ginseng mainly depend on the triterpenoid saponins called ginsenosides [19,20,21,22,23,24], which are mainly produced in the leaves and stored in the roots [25,26,27,28]. They are classified into dammarane-type and oleanolic acid-type ginsenosides. Ginseng mainly consists of the dammarane-type ginsenosides [26, 28, 29], which are further grouped into the protopanaxadiol (PPD) and protopanaxatriol (PPT) types based on the sugar moieties attached to their aglycone structure . The biosynthesis of ginsenosides begins with isoprenoid metabolic pathways involving the cytosolic mevalonate (MVA) pathway and plastid 2-C-Methyl-d-erythritol 4-phosphate (MEP) pathway [27, 30]. Both contribute to ginsenoside biosynthesis by synthesizing isopentenyl diphosphate (IPP) [27, 30, 31]. The backbone for ginsenoside biosynthesis is produced through several condensation and cyclization reactions involving the enzymes farnesyl pyrophosphate synthase (PgFPPS), squalene synthase (PgSS), and squalene epoxidase (PgSE). The first step in ginsenoside biosynthesis is catalyzed by dammarenediol synthase (PgDDS), which converts 2,3-oxidosqualene into a dammarenediol backbone [32, 33]. This backbone is further converted into diverse ginsenosides present in ginseng through numerous cytochrome P450 enzymes and UDP-glucuronosyltransferases (PgUGTs) [34,35,36].
Recent studies have shown that changes in light quality lead to differences in ginsenoside content [37,38,39]. However, studies on gene expression and ginsenoside biosynthesis in ginseng, which is a shade-adapted plant, have not been actively conducted under far-red (FR) enriched shade conditions to date. Therefore, in the present study, we performed transcriptome and ginsenoside analyses on ginseng seedlings exposed to various light conditions, including white light (WL), BL, RL, and shade (R:FR ratio = 0.2). We further analyzed the expression of genes involved in ginsenoside biosynthesis and ginsenoside content in adventitious roots and 2-year-old plants using quantitative real-time PCR (qRT-PCR) and ultra-performance liquid chromatography (UPLC), respectively, to determine whether light quality-mediated ginsenoside production depends on the types of tissue or the age of the ginseng plant.
Materials and methods
The P. ginseng cultivar Yunpoong was used in all the experiments. Stratified seeds were obtained from the Department of Herbal Crop Research, National Institute of Horticultural and Herbal Science, Republic of Korea, and 2-year-old sprouts were obtained from Korea Ginseng Corporation. Adventitious roots derived from the Yunpoong cultivar were divided, transferred into three bioreactors for generating biological replicates, and collected 4 weeks later for light quality studies.
Light treatment and growth conditions
The seeds and 2-year-old sprouts were cultivated in a growth room maintained at 23 °C for 1 month in long-day (16-h light/ 8-h dark) conditions until fully expanded leaves were obtained. For light quality studies, plants were transferred to growth incubators with white light (50 µmol m–2 s–1), blue light (30 µmol m–2 s–1), red light (30 µmol m–2 s–1), far-red light (FRL; 15 µmol m–2 s–1), or shade (50 µmol m–2 s–1, R:FR ratio = 0.2) conditions. Blue, red, and far-red light was generated using blue LEDs (450 nm), red LEDs (660 nm), and far-red LEDs (730 nm), respectively. Light intensity was measured using UPRtek spectral PAR meter (PG200N; UPRtek Corp., Taiwan).
Total RNA extraction, cDNA synthesis, and real-time PCR
The light-treated plants and adventitious roots were harvested in the dark and immediately frozen in liquid nitrogen. For total RNA extraction, TRIzol – RNAeasy hybrid method was followed to avoid contamination with sugars and other secondary metabolites. Frozen ginseng materials were homogenized to a fine powder using a mortar and pestle in the presence of liquid nitrogen, and an appropriate volume of TRI reagent (TR118, Molecular Research Center Inc., Cincinnati, OH, USA) was added according to the manufacturer’s instructions. After mixing and centrifuging, the resulting aqueous phase was transferred to a new tube. Total RNA was precipitated with 70% ethanol and collected using the Qiagen RNAeasy Mini Kit (Qiagen Inc, Hilden, Germany). For cDNA synthesis, 1 µg of total RNA was used as a template in the reverse transcription reactions along with 5X PrimeScript™ RT Master Mix (Takara Bio Inc., Shiga, Japan). Quantitative real-time PCR (qRT-PCR) was performed to analyze the expression of genes involved in ginsenoside biosynthesis using the primers listed in Additional file 1: Table S1. Cyclophilin (PgCYP) or glyceraldehyde 3-phosphate dehydrogenase (GAPDH) expression  was used as an internal control to normalize cDNA levels.
Library construction was performed by the National Instrumentation Center and Environmental Management (NICEM), South Korea and sequencing was performed by PHYZEN, South Korea. Paired-end reads with an average length of 101 base pairs (bp) were generated using the Illumina Hiseq2000 platform. Sequencing quality was examined using FastQC (v0.11.3) before further analysis. Poor-quality reads were removed and clean reads were combined and assembled using the Trinity transcriptome assembler (version r20140717). Nine GB of clean data was generated on average per sample. The final assembly of the light-treated samples contained 59,352 unigenes. Functional annotation revealed 56,968, 50,293, 46,399, 38,819, and 24,905 unigenes with alignments to NR (non-redundant protein database), Protein domains (InterProScan), Gene Ontology (BLAST2GO), and KEGG (Kyoto encyclopedia of genes and genomes) databases, respectively. The selected unigenes were validated according to the P. ginseng draft genome from the Ginseng Genome Database . Differences in the transcript levels of each gene under various light treatments were analyzed using DeSeq2. Differentially expressed genes were defined based on a 2-fold change difference (p < 0.05) in the transcription level of genes between plants treated with white light and plants treated with other light wavelengths, such as blue, red, and shade. A heat map was drawn based on FPKM values using the online program heat mapper .
Total ginsenoside extraction and HPLC analysis
Total ginsenoside content was analyzed in frozen and powdered ginseng samples for qualitative and quantitative analyses. Each sample (0.1 mg) was ground and mixed with methanol (80%; 1:10 wt/vol) used as an extraction solvent. The mixture was sonicated in an ultrasonic bath at 25 kHz for 30 min at 25 °C (Branson ultrasonic cleaner, Emerson Electric, Brookfield, CT, USA) and centrifuged at 3000 rpm for 20 min. The supernatant was sonicated and centrifuged twice. The resultant supernatant was filtered through a 0.2 μm syringe filter and analyzed using UPLC (Shimadzu LCMS-8050 system; Shimadzu Corp., Kyoto, Japan). The sample (1.0 µL) was separated using Cortecs UPLC T3 1.6 μm 2.1 × 150 mm column (Waters Corp., Milford, MA, USA), and the temperature of the column was maintained at 35 °C. Distilled water containing 0.1% formic acid (A) and methanol/acetonitrile (9/1, v/v, 0.1% formic acid, B) was used as the mobile phase with a gradient of 35% A to 95% B for 20 min and a flow rate of 0.45 mL/min. To detect ginsenosides, negative ionization mode of ESI-mass spectrometry (MS)/MS was used.
Light quality dramatically alters the expression patterns of secondary metabolite biosynthetic genes
To investigate the effect of shade and light quality on gene expression and ginsenoside production in ginseng, 1-month-old ginseng seedlings were exposed to WL, BL, RL, or shade and further grown for five days. Transcriptomic analysis revealed a striking number of differentially expressed genes (DEGs) between the light quality treatments. BL had the highest number of upregulated DEGs, whereas RL had a significantly higher number of downregulated genes (Fig. 1A). Interestingly, GO term analysis revealed a dramatic increase in the metabolic activity following BL treatment. Notably, the genes involved in alkaloid and cinnamic acid metabolic processes and sugar transporter activity were upregulated (Fig. 1B). KEGG enrichment analysis revealed that the phenylpropanoid and flavonoid biosynthesis pathway genes were enriched under BL. In contrast, genes involved in most SM pathways were significantly downregulated under RL (Fig. 1C). These genes encode hydroxymethylglutaryl-CoA reductase (HMGCR), farnesyl diphosphate farnesyltransferase and components in terpenoid, sesquiterpenoid, and isoprenoid metabolisms (Fig. 1C). Shade conditions (enriched FR) upregulated 89 DEGs, including genes involved in abiotic stress pathways, and downregulated 97 DEGs, mainly involved in photosystem, photosynthesis, and plastid development (Fig. 1D). Because ginsenoside production is influenced by abiotic stresses, these results suggest that shade conditions may increase ginsenoside content by upregulating ginsenoside biosynthesis genes.
Shade conditions upregulate genes involved in isoprenoid metabolism
Isoprenoids in plants are mainly produced by the MVA and MEP metabolic pathway end products (Fig. 2A), which serve as precursors for many secondary metabolites present in plants [42, 43]. Light has a profound effect on the isoprenoid pathway, especially the MEP pathway. Light-induced changes in isoprenoid metabolic pathways were observed in our transcriptomic analysis (Fig. 1). This led us to analyze the changes in the expression of genes involved in the MVA and MEP pathways. RL treatment tended to reduce the expression levels of MVA and MEP pathway genes compared to BL and shade conditions (Fig. 2B and C). However, the expression of isoprenoid metabolism genes in the MVA and MEP pathways was not altered by RL treatment (Fig. 2B and C). Moreover, in the MVA pathway, the upstream genes encoding acetyl-CoA C-acetyltransferase (PgAACT), hydroxymethylglutaryl-CoA synthase (PgHMGS), and (PgHMGR) were reduced by RL treatment compared to BL and shade conditions (Fig. 2B). Similarly, we observed that most MEP genes were downregulated under RL conditions. Notably, genes that encode 1-deoxy-D-xylulose-5-phosphate synthase (PgDXS) and 1-deoxy-d-xylulose-5-phosphate reductase (PgDXR) synthesizing MEP were downregulated by RL treatment (Fig. 2A and C), resulting in reduced expression of all downstream genes including isopentenyl-diphosphate Delta-isomerase (PgIDI), which its gene product produces a terpenoid precursor, isopentyl-diphosphate (IPP) (Fig. 2A and C). In contrast, we observed the upregulation of MVA and MEP pathway genes under BL and shade conditions (Fig. 2B and C). These results suggested that light quality is important for the regulation of isoprenoid metabolic processes in ginseng and may influence ginsenoside biosynthesis.
Far-red light affects the expression of ginsenoside biosynthetic genes differently according to tissue and age
Ginsenosides, which are ginseng saponins, are derived from the IPP precursor produced by the MVA and MEP pathways and are reportedly synthesized in the leaves . Next, we analyzed the expression profiles of ginsenoside-synthesizing genes in the leaves and found characteristic changes according to light quality. The transcript abundance of ginsenoside biosynthesis genes was the highest under shade conditions (Fig. 3A and B). In particular, PgFPPS (Pg_S8325.1, Pg_S0304.36), PgSS (Pg_S0992.8, Pg_S1678.33, Pg_S2014.27, Pg_S1637.7), PgSE (Pg_S3064.5, Pg_S0129.28, Pg_S1693.31, Pg_S2606.7, Pg_S2606.8, Pg_S2840.6, Pg_S6308.10, Pg_S4651.2), and PgDDS (Pg_S3318.3) genes were highly induced under shade as well as BL conditions (Fig. 3A). All paralogs of these genes were upregulated under shade and BL conditions compared to RL, except PgDDS. Among PgDDS paralogs, only Pg_S3318.3 was expressed in our study (Fig. 3A). These results suggest that ginsenoside biosynthesis is dependent on light quality. Similar to the isoprenoid pathway, the expression of most ginsenoside genes was downregulated under RL conditions, except for one paralog, PgSQE (Pg_S4651.2). Moreover, protopanaxadiol synthase (PgPPDS, Pg_S4733.5, Pg_S3293.6) and one paralog of protopanaxatriol synthase (PgPPTS1, Pg_S1770.12) showed the highest expression under shaded conditions (Fig. 3A), indicating that dammarane-type ginsenosides may accumulate under these conditions. β-amyrin synthase (BAS) catalyzes the cyclization of 2,3-oxidosqualene to produce β-amyrin, which serves as a precursor for the production of oleanolic acid-type ginsenosides (mainly Ro) and plant sterols. Seven PgBAS genes among eight paralogs were expressed in our conditions, and their expression was unaltered by light quality changes (Fig. 3A).
To date, more than 150 ginsenosides have been identified in Panax species, and this diversity is due to many UDP-glycosyltransferases (UGTs) that catalyze glycosylation reactions in the final ginsenoside biosynthesis . We further analyzed whether the expression of UGT genes was dependent on light quality. Among the 12 PgUGTs in our analysis, eight genes were the most enriched under shade conditions (Fig. 3B). In contrast, the expression of Pg_S2390.5 belonging to the UGT74 clade under shade conditions was lower than that under WL and RL conditions (Fig. 3B). Similar to the ginsenoside biosynthesis genes, the expression of all PgUGT genes analyzed was decreased by RL treatment compared to WL conditions (Fig. 3B). These results suggest that light quality may affect the levels of specific ginsenosides.
The level of ginsenoside production varies with tissues and developmental ages [26,27,28]. To examine whether the effect of light quality on the expression of ginsenoside biosynthesis genes was preserved in other tissues and developmental stages, ginseng adventitious roots and 2-year-old plants were grown under WL, BL, RL, and FRL conditions. We used monochromatic FRL instead of shade conditions in order to eliminate the effect of other wavelengths on gene expression. Quantitative real-time PCR analysis showed FRL-specific enrichment in the expression of PgHMGR and PgSS genes in adventitious roots (Fig. 3C). Conversely, RL-specific enrichment of PgHMGR, PgSS, and PgDDS was observed in the leaves of 2-year-old plants (Fig. 3D). These results indicate that light quality may have different effects on ginsenoside production depending on the tissue and age of the ginseng.
Far-red light influences the production and diversity of ginsenosides
Because our data showed that light quality plays an important role in the regulation of ginsenoside biosynthesis gene expression, we analyzed the changes in ginsenoside content under different light regimes. We quantified the total ginsenoside content and individual ginsenosides belonging to the PPD, PPT, or oleanane types in the leaves of seedlings, adventitious roots, and leaves of 2-year-old plants under the same conditions, which the gene expression was analyzed. In seedlings, unlike the transcriptome analysis, the total ginsenoside content was similar among BL, RL, and shade conditions, despite a slight variation compared to WL (Fig. 4A). However, PPD-type ginsenosides, including Rb1, Rc, Rb2, and their malonyl forms such as malonyl-Rc (mRc), malonyl-Rb1 (mRb1), and malonyl-Rb2 (mRb2), and oleanane-type ginsenoside Ro were significantly increased under RL and shade conditions (Fig. 4A). In contrast, the PPT-type ginsenosides Re and Rg1 were enriched following BL treatment. In adventitious roots, the total ginsenoside content under FRL conditions was lower than that under WL conditions (Fig. 4B), which was inconsistent with the enriched transcripts of the canonical ginsenoside genes PgHMGR and PgSS in FRL-treated adventitious roots (Fig. 3C). Moreover, the total ginsenoside content under BL and RL conditions was similar to that under WL conditions (Fig. 4B). Unlike seedlings and adventitious roots, the total amount of ginsenosides in 2-year-old plants was the highest under FRL conditions among all conditions (Fig. 4C), indicating that ginsenoside accumulation may differ from gene expression patterns (Fig. 3D). This asynchronous relationship between gene expression and ginsenoside production may be attributed to unknown feedback and/or compensatory circuits. Additionally, major ginsenosides in the PPD and PPT types, including Rb1, Rb2, Rc, Rd, Re, and Rg1, showed FRL-specific enrichment compared to BL and RL conditions (Fig. 4C). We also found that the ginsenoside content and composition varied among all plant tissues tested (Fig. 4). Taken together, our data suggest the existence of a complicated mechanism by which light quality influences ginsenoside production and diversification of ginsenoside content through the regulation of multiple sets of genes, likely allowing ginseng plants to optimize ginsenoside biosynthesis under a wide range of environmental conditions.
Plants absorb, transmit, and reflect the most photosynthetically active wavelengths. The quality and intensity of light absorbed by leaves play critical roles in the development, morphogenesis, and biosynthesis of different compounds [6, 46]. Our DEG analysis showed that light treatment significantly affected the expression of genes involved in the primary and secondary metabolic pathways. The pairwise comparison between WL- and BL-treated plants showed the upregulation of secondary metabolic pathways, such as alkaloid metabolic pathways and phenylalanine catabolic processes (Fig. 1B–D). The increase in photosynthetic gene expression observed in the BL-treated plants could contribute to active metabolic processes in ginseng. Ginseng possesses chlorophyll A/B binding proteins that are duplicated during evolution, leading to its high photosynthetic capacity . We observed that genes involved in phenylpropanoid biosynthetic pathways, such as Pg_S1239.2, Pg_S2256.14, and Pg_S3606.18, were upregulated in the BL-treated plants in particular. Among the enriched metabolic pathways, products of the cinnamic acid and phenylpropanoid biosynthesis pathways act as precursor pools for secondary metabolites.
Red light is known to contribute to the development of photosynthetic apparatus, thereby enhancing the accumulation of starch in plants [45, 49]. Ginsenoside biosynthesis is regulated during the early growth and developmental stages of ginseng plants, which later leads to the accumulation of ginsenosides in the roots [44, 48,49,50,51]. Thus, we used young seedlings to understand light quality-mediated ginsenoside biosynthesis. Our results showed that upstream pathways, such as the MEP and MVA pathways, were significantly affected by light quality (Fig. 2). Notably, the transcripts of PgDXS, PgDXR, and PgGGPS in the MEP pathway and those of PgAACT, PgHMGS, PgHMGR, and PgPMK in the MVA pathway were significantly downregulated under RL conditions (Fig. 2B and C). In contrast to the plants exposed to WL, BL, and shade conditions, plants exposed to RL displayed downregulation of genes related to the terpenoid and sterol biosynthesis pathways (Fig. 1C).
We found that shade conditions enhanced the expression of genes involved in ginsenoside biosynthesis in seedlings, similar to isoprenoid metabolite pathway genes (Fig. 3A). In particular, canonical genes involved in ginsenoside biosynthesis, such as PgDDS, PgPPDS, and PgPPTS, were prominently expressed. Surprisingly, while the changes in the transcript levels of genes involved in ginsenoside metabolism were striking, the total ginsenoside content did not change significantly (Figs. 3A, B and 4A). However, the concentration of PPD-type ginsenosides was considerably higher under shade conditions than that of PPT-type ginsenosides (Fig. 4A); RL treatment also showed a similar trend. Unlike the seedlings, in 2-year-old plants exposed to FR light, the total ginsenoside content was increased (Fig. 4C) while the ginsenoside gene expression was downregulated (Fig. 3D). The difference in gene expression patterns in response to FR light between seedlings and 2-year-old plants could be explained due to the difference in the duration of light treatment (5 d versus 2 wk). Alternately, it is possible that while the enzymes themselves may be activated by FR light, it might cause a feedback inhibitory effect on the expression of genes that encode key enzymes of ginsenoside biosynthesis. In addition, the post-translational modification or regulation by light quality, such as phosphorylation or stability changes, respectively, can account for discrepancies between gene expression and metabolite profiles . Furthermore, the comparative analysis of transcript levels, enzyme activities, and metabolites revealed that diel changes in transcript levels were rapid, whereas diel changes in activities and metabolites were small or slow .
In conclusion, our transcriptome and ginsenoside analyses suggest that light quality is crucial not only for the production of ginsenosides but also for their diversity, especially highlighting the importance of shade or FR light in the promotion of ginsenoside biosynthesis in ginseng leaves via gene regulation. Our findings provide clues for improving the medicinal quality of ginseng by increasing the pharmacologically valuable PPD-based ginsenoside content in ginseng plants by using shade or FR light during their growth.
Availability of data and materials
The datasets used and/or analyzed in the current study are available from the corresponding author upon reasonable request.
Chen M, Chory J, Fankhauser C (2004) Light signal transduction in higher plants. Annu Rev Genet 38:87–117. https://doi.org/10.1146/annurev.genet.38.072902.092259
Hornyák M, Dziurka M, Kula-Maximenko M, Pastuszak J, Szczerba A, Szklarczyk M, Plazek A (2022) Photosynthetic efficiency, growth and secondary metabolism of common buckwheat (Fagopyrum esculentum Moench) in different controlled-environment production systems. Sci Rep 12(1):257. https://doi.org/10.1038/s41598-021-04134-6
Armbruster U, Correa Galvis V, Kunz HH, Strand DD (2017) The regulation of the chloroplast proton motive force plays a key role for photosynthesis in fluctuating light. Curr Opin Plant Biol 37:56–62. https://doi.org/10.1016/j.pbi.2017.03.012
Sharangi AB (2016) Secondary metabolites in spices and medicinal plants: an overview. In: Siddiqui MW, Prasad K (eds) Plant secondary metabolites, volume 1: Biological and therapeutic significance, 1st edn. Apple Academic Press, New York, pp 145–168
Thoma F, Somborn-Schulz A, Schlehuber D, Keuter V, Deerberg G (2020) Effects of Light on secondary metabolites in selected Leafy Greens: a review. Front Plant Sci 11:497. https://doi.org/10.3389/fpls.2020.00497
Li Y, Kong D, Fu Y, Sussman MR, Wu H (2020) The effect of developmental and environmental factors on secondary metabolites in medicinal plants. Plant Physiol Biochem 148:80–89. https://doi.org/10.1016/j.plaphy.2020.01.006
Shi Y, Yang L, Yu M, Li Z, Ke Z, Qian X, Ruan X, He L, Wei F, Zhao Y, Wang Q (2022) Seasonal variation influences flavonoid biosynthesis path and content, and antioxidant activity of metabolites in Tetrastigma hemsleyanum Diels & Gilg. PLoS ONE 17(4):e0265954
Valletta A, Iozia LM, Leonelli F (2021) Impact of environmental factors on stilbene biosynthesis. Plants 10(1):90. https://doi.org/10.3390/plants10010090
Zhan X, Chen Z, Chen R, Shen C (2022) Environmental and genetic factors involved in plant protection-associated secondary metabolite biosynthesis pathways. Front Plant Sci 13:877304. https://doi.org/10.3389/fpls.2022.877304
Li H, Lyu Y, Chen X, Wang C, Yao D, Ni S, Lin Y, Chen Y, Zhang Z, Lai Z (2019) Exploration of the rffect of blue light on functional metabolite accumulation in longan embryonic calli via RNA sequencing. Int J Mol Sci 20(2):441
Liu L, Lin N, Liu X, Yang S, Wang W, Wan X (2020) From chloroplast biogenesis to chlorophyll accumulation: the interplay of light and hormones on gene expression in Camellia sinensis cv. Shuchazao Leaves Front Plant Sci 11:256
Tian Y, Wang H, Zhang Z, Zhao X, Wang Y, Zhang L (2021) An RNA-seq analysis reveals differential transcriptional responses to different light qualities in leaf color of Camellia sinensis cv. Huangjinya. J Plant Growth Regul 41:612–627. https://doi.org/10.1007/s00344-021-10325-2
Geraldo CC, Marcos FGR, Renato A, Dedecek RA, Curcio GR, Nietsche K, Schenkel EP (2007) Effect of light intensity on methylxanthine contents of Ilex paraguariensis A. St Hil Biochem Syst Ecol 35(2):75–80
Chen Y, Zhou B, Li J, Tang H, Tang J, Yang Z (2018) Formation and change of chloroplast-located plant metabolites in response to light conditions. Int J Mol Sci 19(3):654
Ma Q, Song L, Niu Z, Li J, Wang Y, Sun H, Ren Z, Zhao H, Guo S, Ding Z (2022) Red light regulates the metabolite biosynthesis in the leaves of “Huangjinya” through amino acid and phenylpropanoid metabolisms. Front Plant Sci 12:810888. https://doi.org/10.3389/fpls.2021.810888
Zhang S, Zhang L, Zou H, Qiu L, Zheng Y, Yang D, Wang Y (2021) Effects of light on secondary metabolite biosynthesis in medicinal plants. Front Plant Sci 10:781236. https://doi.org/10.3389/fpls.2021.781236
Dossou SSK, Xu F, Cui X, Sheng C, Zhou R, You J, Tozo K, Wang L (2021) Comparative metabolomics analysis of different sesame (Sesamum indicum L.) tissues reveals a tissue-specific accumulation of metabolites. BMC Plant Biol 21(1):1–14
Siatkowska K, Chraniuk M, Bollin P, Banasiuk R (2021) Light emitting diodes optimisation for secondary metabolites production by Droseraceae plants. J Photochem Photobiol B Biology 224:112308. https://doi.org/10.1016/j.jphotobiol.2021.112308
Li KK, Gong XJ (2015) A review on the medicinal potential of Panax ginseng saponins in diabetes mellitus. RSC Adv 5(59):47353–47366
Wong AST, Che CM, Leung KW (2015) Recent advances in ginseng as cancer therapeutics: a functional and mechanistic overview. Nat Prod Rep 32(2):256–272. https://doi.org/10.1039/c4np00080c
Jakaria M, Kim J, Karthivashan G, Park SY, Ganesan P, Choi DK (2019) Emerging signals modulating potential of ginseng and its active compounds focusing on neurodegenerative diseases. J Ginseng Res 43(2):163–171. https://doi.org/10.1016/j.jgr.2018.01.001
Yi YS (2022) Potential benefits of ginseng against COVID-19 by targeting inflammasomes. J Ginseng Res 46:722–730. https://doi.org/10.1016/j.jgr.2022.03.008
You L, Cha S, Kim MY, Cho JY (2022) Ginsenosides are active ingredients in Panax ginseng with immunomodulatory properties from cellular to organismal levels. J Ginseng Res 46(6):711–721. https://doi.org/10.1016/j.jgr.2021.12.007
Mohanan P, Subramaniyam S, Mathiyalagan R, Yang DC (2018) Molecular signaling of ginsenosides Rb1, Rg1, and Rg3 and their mode of actions. J Ginseng Res 42(2):123–132. https://doi.org/10.1016/j.jgr.2017.01.008
Hou M, Wang R, Zhao S, Wang Z (2021) Ginsenosides in Panax genus and their biosynthesis. Acta Pharm Sin B 11(7):18136–11834. https://doi.org/10.1016/j.apsb.2020.12.017
Chen W, Balan P, Popovich DG (2020) Comparison of ginsenoside components of various tissues of New Zealand forest-grown asian ginseng (Panax ginseng) and American ginseng (Panax quinquefolium L.). Biomolecules 10(3):372. https://doi.org/10.3390/biom10030372
Kim YJ, Zhang D, Yang DC (2015) Biosynthesis and biotechnological production of ginsenosides. Biotechnol Adv 33(6 Pt 1):717–735. https://doi.org/10.1016/j.biotechadv.2015.03.001
Liu J, Liu Y, Wang Y, Abozeid A, Zu YG, Zhang XN, Tang ZH (2017) GC-MS metabolomic analysis to reveal the metabolites and biological pathways involved in the developmental stages and tissue response of Panax ginseng. Molecules 22(3):496. https://doi.org/10.3390/molecules22030496
Shin BK, Kwon SW, Park JH (2015) Chemical diversity of ginseng saponins from Panax ginseng. J Ginseng Res 39:287–298. https://doi.org/10.1016/j.jgr.2014.12.005
Xue L, He Z, Bi X, Xu W, Wei T, Wu S, Hu S (2019) Transcriptomic profiling reveals MEP pathway contributing to ginsenoside biosynthesis in Panax ginseng. BMC Genomics 20(1):383. https://doi.org/10.1186/s12864-019-5718-x
Wang J, Gao W, Zhang J, Zuo BM, Zhang LM, Huang LQ (2012) Advances in study of ginsenoside biosynthesis pathway in Panax ginseng C. A. Meyer. Acta Physiol Plant 34(2):397–403. https://doi.org/10.1007/s11738-011-0844-3
Han JY, Kwon YS, Yang DC, Jung YR, Choi YE (2006) Expression and RNA interference-induced silencing of the dammarenediol synthase gene in Panax ginseng. Plant Cell Physiol 47(12):1653–1662. https://doi.org/10.1093/pcp/pcl032
Kim TD, Han JY, Huh GH, Choi YE (2011) Expression and functional characterization of three squalene synthase genes associated with saponin biosynthesis in Panax ginseng. Plant Cell Physiol 52(1):125–137. https://doi.org/10.1093/pcp/pcq179
Jayakodi M, Choi BS, Lee SC, Kim NH, Park JY, Jang W, Lakshmanan M, Mohan SVG, Lee DY, Yang TJ (2018) Ginseng genome database: an open-access platform for genomics of Panax ginseng. BMC Plant Biol 18(1):62. https://doi.org/10.1186/s12870-018-1282-9
Yang C, Li C, Wei W, Wei Y, Liu Q, Zhao G, Yue J, Yan X, Wang P, Zhou Z (2020) The unprecedented diversity of UGT94-family UDP-glycosyltransferases in Panax plants and their contribution to ginsenoside biosynthesis. Sci Rep 10(1):15394. https://doi.org/10.1038/s41598-020-72278-y
Li C, Yan X, Xu Z, Wang Y, Shen X, Zhang L, Zhou Z, Wang P (2022) Pathway elucidation of bioactive rhamnosylated ginsenosides in Panax ginseng and their de novo high-level production by engineered Saccharomyces cerevisiae. Commun Biol 5(1):775. https://doi.org/10.1038/s42003-022-03740-y
Jang IB, Do GG, Suh SJ, Yu J, Jang IB, Moon JW, Chun CW (2020) Physiological responses and ginsenoside production of Panax ginseng seedlings grown under various ratios of red to blue light-emitting diodes. Hortic Environ Biotechnol 61:663–672. https://doi.org/10.1007/s13580-020-00255-5
Kim YJ, Nguyen TK, Oh MM (2020) Growth and ginsenosides content of ginseng sprouts according to LED-based light quality changes. Agronomy 10(12):1979. https://doi.org/10.3390/agronomy10121979
Choi J, Kim J, Yoon HI, Son JE (2022) Effect of far-red and UV-B light on the growth and ginsenoside content of ginseng (Panax ginseng CA Meyer) sprouts aeroponically grown in plant factories. Hortic Environ Biotechnol 63(1):77–87. https://doi.org/10.1007/s13580-021-00380-9
Liu J, Wang Q, Sun M, Zhu L, Yang M, Zhao Y (2014) Selection of reference genes for quantitative real-time PCR normalization in Panax ginseng at different stages of growth and in different organs. PLoS ONE 9(11):e112177. https://doi.org/10.1371/journal.pone.0112177
Babicki S, Arndt D, Marcu A, Liang Y, Grant JR, Maciejewski A, Wishart DS (2016) Heatmapper: web-enabled heat mapping for all. Nucleic Acids Res 44(W1):147–153. https://doi.org/10.1093/nar/gkw419
Sacchettini JC, Poulter CD (1997) Creating isoprenoid diversity. Science 277(5333):1788–1789
Zeng L, Dehesh K (2021) The eukaryotic MEP-pathway genes are evolutionarily conserved and originated from Chlaymidia and cyanobacteria. BMC Genomics 22(1):137. https://doi.org/10.1186/s12864-021-07448-x
Kim YJ, Joo SC, Shi J, Hu C, Quan S, Hu J, Sukweenadhi J, Mohanan P, Yang DC, Zhang D (2018) Metabolic dynamics and physiological adaptation of Panax ginseng during development. Plant Cell Rep 37(3):393–410. https://doi.org/10.1007/s00299-017-2236-7
Kang KB, Jayakodi M, Lee YS, Nguyen VB, Park HS, Koo HJ, Choi IY, Kim DH, Chung YJ, Ryu B, Lee DY, Sung SH, Yang TJ (2018) Identification of candidate UDP-glycosyltransferases involved in protopanaxadiol-type ginsenoside biosynthesis in Panax ginseng. Sci Rep 8(1):11744. https://doi.org/10.1038/s41598-018-30262-7
Ilić ZS, Fallik E (2017) Light quality manipulation improves vegetable quality at harvest and postharvest: a review. Environ Exp Bot 139:79–90. https://doi.org/10.1016/j.envexpbot.2017.04.006
Kim NH, Jayakodi M, Lee SC, Choi BS, Jang W, Lee J, Kim HH, Waminal NE, Lakshmanan M, van Nguyen B, Lee YS, Park HS, Koo HJ, Park JY, Perumal S, Joh HJ, Lee H, Kim J, Kim IS, Kim K, Koduru L, Kang KB, Sung SH, Yu Y, Park DS, Choi D, Seo E, Kim S, Kim YC, Hyun DY, Park YI, Kim C, Lee TH, Kim HU, Soh MS, Lee Y, In JG, Kim HS, Kim YM, Yang DC, Wing RA, Lee DY, Paterson AH, Yang TJ (2018) Genome and evolution of the shade-requiring medicinal herb Panax ginseng. Plant Biotechnol J 16(11):1904–1917. https://doi.org/10.1111/pbi.12926
Liu Z, Wang CZ, Zhu XY, Wan JY, Zhang J, Li W, Ruan CC, Yuan CS (2017) Dynamic changes in neutral and acidic ginsenosides with different cultivation ages and harvest seasons: identification of chemical characteristics for Panax ginseng quality control. Molecules 22(5):734. https://doi.org/10.3390/molecules22050734
Kim YJ, Jeon JN, Jang MG, Oh JY, Kwon WS, Jung SK, Yang DC (2014) Ginsenoside profiles and related gene expression during foliation in Panax ginseng Meyer. J Ginseng Res 38(1):66–72. https://doi.org/10.1016/j.jgr.2013.11.001
Schramek N, Huber C, Schmidt S, Dvorski SE, Kmispel N, Ostrozhenkova E, Pena-Rodriguez LM, Cusido RM, Wischmann G, Eisenreich W (2014) Biosythesis of ginsenosides in field-grown Panax ginseng. JSM Biotechnol Bioeng 2(1):1033. https://doi.org/10.47739/2333-7117/1033
Xiao D, Yue H, Xiu Y, Sun X, Wang Y, Liu S (2015) Accumulation characteristics and correlation analysis of five ginsenosides with different cultivation ages from different regions. J Ginseng Res 39(4):338–344. https://doi.org/10.1016/j.jgr.2015.03.004
Radomiljac JD, Whelan J, van der Merwe M (2013) Coordinating metabolite changes with our perception of plant abiotic stress responses: emerging views revealed by integrative-omic analyses. Metabolites 3(3):761–786. https://doi.org/10.3390/metabo3030761
Gibon Y, Usadel B, Blaesing OE, Kamlage B, Hoehne M, Trethewey R, Stitt M (2006) Integration of metabolite with transcript and enzyme activity profiling during diurnal cycles in Arabidopsis rosettes. Genome Biol 7(8):R76. https://doi.org/10.1186/gb-2006-7-8-r76
This work was supported by the New Faculty Startup Fund from Seoul National University to Y.H. Song, the Cooperative Research Program for Agriculture Science and Technology Development (Project No. PJ015903) of the Rural Development Administration, Republic of Korea to T-J. Yang and Y.H. Song, and a National Research Foundation (NRF) of Korea grant funded by the Korean government (MSIT) (No. NRF-2021R1A4A1032888) to T-J. Yang and Y. H. Song.
The authors declare that they have no competing interests.
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Mohanan, P., Yang, TJ. & Song, Y.H. Effect of far-red light on the production and diversity of ginsenosides in leaves of Panax ginseng Meyer. Appl Biol Chem 66, 16 (2023). https://doi.org/10.1186/s13765-023-00776-4
- Far-red light
- Secondary metabolites