Abstract
Mirabilis himalaica is a traditional Tibetan medicinal plant in China. However, it has become a class I endangered medicinal plant. Therefore, the utilization of M. himalaica callus to propagate germplasm resources is of great significance. Numerous active compounds have been found in M. himalaica, most of which have been isolated from phenolic acids. In this study, UV-B radiation enhanced the accumulation of phenolic acids effectively in M. himalaica callus. The multi-omics profiles were used to reveal the co-expression regulated patterns of genes related to phenolic acid synthesis in UV-B treated M. himalaica callus. In this way, 8 medicinal metabolites were identified, including rosmarinic acid, sinapic acid, coniferin, salicylic acid, tyrosol, isochlorogenic acid A, isochlorogenic acid B and isochlorogenic acid C. The transcriptome data were divided into 26 modules based on similar expression pattern by using the weighted gene correlation network analysis (WGCNA). It revealed that MEturquoise module correlated with above eight target metabolites. Eventually, 11 structural genes and 31 transcription factors related to phenolic acid biosynthesis were screened. Subsequently, co-expression network was constructed between these genes, transcription factors and metabolites, among which PAL, CAD and CYP73A had strong co-expression relationship with above eight target metabolites. Transcription factors such as MYB, bHLH, bZIP, PLATZ, AP2/ERF-ERF73, WRKY33 and WRKY42 had strong co-expression relationship with eight target metabolites. Consequently, these findings indicated that UV-B treated callus is a cost-efficient alternative to wild M. himalaica, which is valuable for the use of this endangered plant.
Key message
Phenolic acid content in Mirabilis himalaica callus was increased by UV-B treatment and the biosynthesis of phenolic acid is initiated by phenylpropanoid pathway and tyrosine-derived pathway.
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Data availability
Data will be made available on reasonable request.
Abbreviations
- UV-B:
-
UltraViolet B
- WGCNA:
-
Weighted gene correlation network analysis
- DEMs:
-
Differentially expressed metabolites
- DEGs:
-
Differentially expressed genes
- NAA:
-
1-Naphthaleneacetic acid
- TDZ:
-
Thidiazuron
- DPPH:
-
2,2-Diphenyl-1-Picrylhydrazyl
- LC–MS/MS:
-
Liquid chromatography-tandem mass spectrometry
- DW:
-
Dry weight
- KEGG:
-
Kyoto encyclopedia of genes and genomes
- GS:
-
Gene significance
- MM:
-
Module membership
References
Andersen CL, Jensen JL, Ørntoft TF (2004) Approach to identify genes suited for normalization, applied transcription-PCR Data: a model-based variance estimation normalization of real-time quantitative reverse. Cancer Res 64:5245–5250. https://doi.org/10.1158/0008-5472.CAN-04-0496
Cai Y, Luo Q, Sun M, Corke H (2004) Antioxidant activity and phenolic compounds of 112 traditional Chinese medicinal plants associated with anticancer. Life Sci 74(17):2157–2184. https://doi.org/10.1016/j.lfs.2003.09.047
Chen W, Gong L, Guo Z, Wang W, Zhang H, Liu X, Yu S, Xiong L, Luo J (2013) A novel integrated method for large-scale detection, identification, and quantification of widely targeted metabolites: application in the study of rice metabolomics. Mol Plant 6(6):1769–1780. https://doi.org/10.1093/mp/sst080
Chen Y, Zhang L, Lu X, Lan X, Shen M, Lu C (2018) Role of mucilage during achene germination and sprout growth of the endangered Tibetan medicinal herb Mirabilis himalaica (Nyctaginaceae) exposed to abiotic stresses. J Plant Ecol 11(2):328–337. https://doi.org/10.1093/jpe/rtx047
Eichholz I, Huyskens-Keil S, Keller A, Ulrich D, Kroh LW, Rohn S (2011) UV-B-induced changes of volatile metabolites and phenolic compounds in blueberries (Vaccinium corymbosum L). Food Chem 126(1):60–64. https://doi.org/10.1016/j.foodchem.2010.10.071
Gu L, Zheng W, Li M, Quan H, Wang J, Wang F, Huang W, Wu Y, Lan X, Zhang Z (2018) Integrated analysis of transcriptomic and proteomics data reveals the induction effects of rotenoid biosynthesis of Mirabilis himalaica caused by UV-B radiation. Int J Mol Sci 19(11):3324. https://doi.org/10.3390/ijms19113324
Han Y, Lu M, Yue S, Li K, Shang F (2021) Transcriptome and metabolome profiling revealing anthocyanin and phenolic acids biosynthetic mechanisms in sweet osmanthus pericarp. Sci Hortic 289:110489. https://doi.org/10.1016/j.scienta.2021.110489
Huang Q, Zhang L, Lan X, Chen Y, Lu C (2022) Achene mucilage formation process and extrusion from hydrated pericarp of Mirabilis himalaica. Horticultural Plant J 8(2):251–260. https://doi.org/10.1016/j.hpj.2021.10.001
Huyskens-Keil S, Eichholz I, Kroh LW, Rohn S (2007) UV-B induced changes of phenol composition and antioxidant activity in black currant fruit (Ribes nigrum L.). J Appl Bot Food Qual 81:140–144. https://doi.org/10.1086/521686
Jimenez-Lopez C, Pereira AG, Lourenço-Lopes C, Garcia-Oliveira P, Cassani L, Fraga-Corral M, Prieto MA, Simal-Gandara J (2021) Main bioactive phenolic compounds in marine algae and their mechanisms of action supporting potential health benefits. Food Chem 341:128262. https://doi.org/10.1016/j.foodchem.2020.128262
Jin C, Li Z, Li Y, Wang S, Li L, Liu M, Ye J (2020) Transcriptome analysis of terpenoid biosynthetic genes and simple sequence repeat marker screening in Eucommia ulmoides. Mol Biol Rep 47(3):1979–1990. https://doi.org/10.1007/s11033-020-05294-w
Kavya NM, Adil L, Senthilkumar P (2021) A review on saponin biosynthesis and its transcriptomic resources in medicinal plants. Plant Mol Biol Reports 39(4):833–840. https://doi.org/10.1007/s11033-020-05294-w
Kiliç I, Yeşiloğlu Y (2013) Spectroscopic studies on the antioxidant activity of p-coumaric acid. Spectrochim Acta Part A Mol Biomol Spectrosc 115:719–724. https://doi.org/10.1016/j.saa.2013.06.110
Lan X, Quan H, Xia X, Yin W, Zheng W (2016) Molecular cloning and transgenic characterization of the genes encoding chalcone synthase and chalcone isomerase from the Tibetan herbal plantMirabilis himalaica. Biotechnol Appl Biochem 63(3):419–426. https://doi.org/10.1002/bab.1376
Lee JH, Hwang CE, Lee BW, Kim HT, Ko JM, Baek IY, Ahn MJ, Lee HY, Cho KM (2015) Effects of roasting on the phytochemical contents and antioxidant activities of Korean soybean (Glycine max L. Merrill) cultivars. Food Sci Biotechnol 24(5):1573–1582. https://doi.org/10.1007/s10068-015-0203-z
Lee JH, Sun YN, Kim YH (2016) Inhibition of lung inflammation by Acanthopanax divaricatus var. albeofructus and its constituents. Biomol Therapeut 24(1):67–74. https://doi.org/10.4062/biomolther.2015.070
Li Y, Tian Q, Wang Z, Li J, Liu S, Chang R, Chen H, Liu G (2023) Integrated analysis of transcriptomics and metabolomics of peach under cold stress. Front Plant Sci 14 https://doi.org/10.3389/fpls.2023.1153902
Lin W, Li Y, Lu Q, Lu H, Li J (2020) Combined analysis of the metabolome and transcriptome identified candidate genes involved in phenolic acids biosynthesis in the leaves of Cyclocarya paliurus. Int J Mol Sci 21(4):1337. https://doi.org/10.3390/ijms21041337
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
Liu X, Zhang J, Liu H, Shang H, Zhao X, Xu H, Zhang H, Hou D (2022) Comparative transcriptome analysis of MeJA responsive enzymes involved in phillyrin Biosynthesis of Forsythia suspensa. Metabolites 12(11):1143. https://doi.org/10.3390/metabo12111143
Lu C, Guo N, Yang C, Sun H, Cai B (2020) Transcriptome and metabolite profiling reveals the effects of Funneliformis mosseae on the roots of continuously cropped soybeans. BMC Plant Biol 20(1):479. https://doi.org/10.1186/s12870-020-02647-2
Ma L, Gao D, Wang Y, Wang H, Zhang J, Pang X, Hu T, Lü S, Li G, Ye H, Li Y, Wang H (2008) Effects of overexpression of endogenous phenylalanine ammonia-lyase (PALrs1) on accumulation of salidroside in Rhodiola sachalinensis. Plant Biol (Stuttg) 10(3):323–333. https://doi.org/10.1111/j.1438-8677.2007.00024.x
Ma C, Chu J, Shi X, Liu C, Yao X (2016) Effects of enhanced UV-B radiation on the nutritional and active ingredient contents during the floral development of medicinal chrysanthemum. J Photochem Photobiol, B 158:228–234. https://doi.org/10.1016/j.jphotobiol.2016.02.019
Ma S, Hu R, Ma J, Fan J, Wu F, Wang Y, Huang L, Feng G, Li D, Nie G, Zhang X (2022) Integrative analysis of the metabolome and transcriptome provides insights into the mechanisms of anthocyanins and proanthocyanidins biosynthesis in Trifolium repens. Ind Crops Prod 187:115529. https://doi.org/10.1016/j.indcrop.2022.115529
Madureira J, Margaça FMA, Santos Buelga C, Ferreira I, Verde SC, Barros L (2022) Applications of bioactive compounds extracted from olive industry wastes: A review. Comp Rev Food Sci Food Safety 21(1):453–476. https://doi.org/10.1111/1541-4337.12861
Meng X, Wang Y, Li J, Jiao N, Zhang X, Zhang Y, Chen J, Tu Z (2021) RNA sequencing reveals phenylpropanoid biosynthesis genes and transcription factors for Hevea brasiliensis reaction wood formation. Front Gen:12. https://doi.org/10.3389/fgene.2021.763841
Mosadegh H, Trivellini A, Ferrante A, Lucchesini M, Vernieri P, Mensuali A (2018) Applications of UV-B lighting to enhance phenolic accumulation of sweet basil. Sci Hortic 229:107–116. https://doi.org/10.1016/j.scienta.2017.10.043
Nićiforović N, Abramovič H (2014) Sinapic acid and its derivatives: natural sources and bioactivity. Comp Rev Food Sci Food Safety 13(1):34–51. https://doi.org/10.1111/1541-4337.12041
Pfaffl MW, Tichopad A, Prgomet C, Neuvians T (2004) Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper–Excel-based tool using pair-wise correlations. Biotechnol Lett 26(6):509–515. https://doi.org/10.1023/B:BILE.0000019559.84305.47
Rao S, Cong X, Liu H, Hu Y, Yang W, Cheng H, Cheng S, Zhang Y (2022) Revealing the phenolic acids in Cardamine violifolia leaves by transcriptome and metabolome analyses. Metabolites 12(11):1024. https://doi.org/10.3390/metabo12111024
Simić A, Manojlović D, Segan D, Todorović M (2007) Electrochemical behavior and antioxidant and prooxidant activity of natural phenolics. Molecules (basel, Switzerland) 12(10):2327–2340. https://doi.org/10.3390/12102327
Su Z, Jia H, Sun M, Cai Z, Shen Z, Zhao B, Li J, Ma R, Yu M, Yan J (2022) Integrative analysis of the metabolome and transcriptome reveals the molecular mechanism of chlorogenic acid synthesis in peach fruit. Front Nutrition 9. https://doi.org/10.3389/fnut.2022.961626
Surjadinata BB, Jacobo-Velázquez DA, Cisneros-Zevallos L (2021) Physiological role of reactive oxygen species, ethylene, and jasmonic acid on UV light induced phenolic biosynthesis in wounded carrot tissue. Postharvest Biol Technol 172:111388. https://doi.org/10.1016/j.postharvbio.2020.111388
Szajdek A, Borowska EJ (2008) Bioactive compounds and health-promoting properties of berry fruits: A review. Plant Foods Hum Nutr 63(4):147–156. https://doi.org/10.1007/s11130-008-0097-5
Tian C, Wang Y, Yang T, Sun Q, Ma M, Li M (2022) Evolution of physicochemical properties, phenolic acids accumulation, and dough-making quality of whole wheat flour during germination under UV-B radiation. Front Nutrition:9. https://doi.org/10.3389/fnut.2022.877324
Uddin R, Saha MR, Subhan N, Hossain H, Alam A (2014) HPLC-analysis of polyphenolic compounds in Gardenia jasminoides and determination of antioxidant activity by using free radical scavenging assays. Adv Pharma Bull 4(3):273–281. https://doi.org/10.5681/apb.2014.040
Vandesompele J, De Preter K, Pattyn F, Poppe B, Roy NV, Paepe AD, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3(7):H34. https://doi.org/10.1186/gb-2002-3-7-research0034
Wang M, Leng C, Zhu Y, Wang P, Gu Z, Yang R (2022) UV-B treatment enhances phenolic acids accumulation and antioxidant capacity of barley seedlings. LWT 153:112445. https://doi.org/10.1016/j.lwt.2021.112445
Xia J, Lou G, Zhang L, Huang Y, Yang J, Guo J, Qi Z, Li Z, Zhang G, Xu S, Song X, Zhang X, Wei Y, Liang Z, Yang D (2023) Unveiling the spatial distribution and molecular mechanisms of terpenoid biosynthesis inSalvia miltiorrhiza and S. grandifolia using multi-omics and DESI–MSI. Horticulture Res 10 https://doi.org/10.1093/hr/uhad109
Xie F, Xiao P, Chen D, Xu L, Zhang B (2012) miRDeepFinder: a miRNA analysis tool for deep sequencing of plant small RNAs. Plant Mol Biol 80(1):75–84. https://doi.org/10.1007/s11103-012-9885-2
Xiong B, Li Q, Yao J, Wang C, Chen H, Ma Q, Deng T, Liao L, Wang X, Zhang M, Sun G, He S, Zhang X, Wang Z (2023) Combined metabolomic and transcriptomic analysis reveals variation in phenolic acids and regulatory networks in the peel of sweet orange “Newhall” (C sinensis) after grafting onto two different rootstocks. Scientia Horticulturae 323:112461. https://doi.org/10.1016/j.scienta.2023.112461
Yang X, Liao X, Yu L, Rao S, Chen Q, Zhu Z, Cong X, Zhang W, Ye J, Cheng S, Xu F (2022) Combined metabolome and transcriptome analysis reveal the mechanism of selenate influence on the growth and quality of cabbage (Brassica oleracea var. capitata L.). Food Res Int 156:111135. https://doi.org/10.1016/j.foodres.2022.111135
Yildirim AB (2020) Ultraviolet-B-induced changes on phenolic compounds, antioxidant capacity and HPLC profile of in vitro-grown plant materials in Echium orientale L. Ind Crops Prod 153:112584. https://doi.org/10.1016/j.indcrop.2020.112584
Yuan F, Xu Y, Zhao K, Lu Y, Lan X (2020) Characterization of the complete chloroplast genome sequence of the medicinal plant Mirabilis himalaica. Mitochondrial DNA B Resour 5(3):2799–2801. https://doi.org/10.1080/23802359.2020.1788449
Zhang S, Yan Y, Wang B, Liang Z, Liu Y, Liu F, Qi Z (2014) Selective responses of enzymes in the two parallel pathways of rosmarinic acid biosynthetic pathway to elicitors in Salvia miltiorrhiza hairy root cultures. J Biosci Bioeng 117(5):645–651. https://doi.org/10.1016/j.jbiosc.2013.10.013
Zhao W, Peng J, Wang F, Tian M, Li P, Feng B, Yin M, Xu Y, Xue J, Feng X, Chen Y (2022) Integrating metabolomics and transcriptomics to unveil the spatiotemporal distribution of macrocyclic diterpenoids and candidate genes involved in ingenol biosynthesis in the medicinal plant Euphorbia lathyris L. Ind Crops Prod 184:115096. https://doi.org/10.1016/j.indcrop.2022.115096
Zhen W, Tu Y, Lin Z, Xu X, Fu M, Han C (2022) Comparative transcriptome analysis reveals the molecular mechanism of UV-B irradiation in promoting the accumulation of phenolic compounds in wounded carrot. Horticulturae 8(10):896. https://doi.org/10.3390/horticulturae8100896
Funding
This work was financially supported by the National Natural Science Foundation of China (Grant Nos. U20A20401, 31270737), Tibet Autonomous Region Major Special Science and Technology (Grant No. XZ201901-GA-04), and the grant for Beijing Forestry University Outstanding Postgraduate Mentoring Team Building (YJSY-DSTD2022005).
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GJJ, CYZ, and LCF conceived and supervised the project. GJJ, LMY, LRC, GBH, LXJ, performed the research, GJJ and LMY analyzed the data, and GJJ wrote the manuscript. GJJ, LCF, CYZ, LYJ, ZXQ writing, reviewing and editing the manuscript. All authors read and approved the final manuscript.
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Communicated by Ali R. Alan.
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Guo, J., Liu, M., Li, R. et al. Molecular mechanism of phenolic acid biosynthesis in callus of a Tibetan medicinal plant (Mirabilis himalaica) under UV-B treatment. Plant Cell Tiss Organ Cult 156, 82 (2024). https://doi.org/10.1007/s11240-024-02710-y
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DOI: https://doi.org/10.1007/s11240-024-02710-y