Integration of the metabolome and transcriptome reveals the metabolites and genes related to nutritional and medicinal value in Coriandrum sativum

doi:10.1016/S2095-3119(20)63358-5

摘要/Abstract

摘要：

芫荽或胡荽是一种具有多种药效的药膳，广泛用于烹饪和传统医药。它富含精油和抗氧化剂化合物，但其意义不明。为了发掘这些尚未开发的营养或药用丰富的化合物，我们对芫荽三个发育阶段的转录组学和代谢组学数据进行研究。在此，我们鉴定了10个酪氨酸代谢途径相关基因，6个卟啉和叶绿素代谢途径相关基因，5个维生素E代谢途径相关基因。这些基因与芫荽早期发育相关。我们的分析表明，这些途径参与关键酚类代谢物的产生。此外，我们还构建了这些途径相关基因与转录因子之间的相互作用网络，支持了酚类代谢物的调控通路。有趣的是，我们鉴定到了一些营养或药用成分代谢物，包括59种酚类，2种多胺，12种生物碱和1种萜类。较高含量的代谢物来自于咖啡酸、胍丁胺及其衍生物。我们发现咖啡酸和胍丁胺在30天时的浓度高于60天或90天时的浓度。本研究为进一步研究这些化合物在医学和营养学研究中的作用提供了线索。

Abstract:

Coriandrum sativum (Coriander) or Chinese parsley is a culinary herb with multiple medicinal effects, which is widely used in cooking and traditional medicine. It is enriched with essential oils and anti-oxidant compounds with unknown significance. To explore the untapped reservoir of Coriander, we studied the transcriptome and metabolic profiles from three developmental stages. Here, we identified 10 tyrosine metabolic pathway-related genes (TMPRGs), six porphyrins and chlorophyll metabolic pathway-related genes (PCMPRGs), and five Vitamin E metabolic pathway-related genes (VEMPRGs). These genes were associated with the early development of Coriander. Our analysis suggests that these pathways are involved in the production of critical phenolic metabolites. Furthermore, we constructed the interaction network between these pathway-related genes and transcription factors (TFs), which supported the regulatory pathways for phenolic metabolites. Interestingly, we identified several nutritional or medicinally relevant metabolites, including 59 phenols, two polyamines, 12 alkaloids, and one terpenoid. The higher concentrations of metabolites were from caffeic acid, agmatine, and its derivatives. We found higher levels of caffeic acid and agmatine at 30 days compared to 60 or 90 days. This study provides evidence to stimulate further investigation of the role of these metabolites in medicinal and nutritional research.

Key words: metabolomics , transcriptome , regulatory network , phenolic compounds , Coriander

. [J]. Journal of Integrative Agriculture, 2021, 20(7): 1807-1818.

WU Tong, FENG Shu-yan, YANG Qi-hang, Preetida J BHETARIYA, GONG Ke, CUI Chun-lin, SONG Jie, PING Xiao-rui, PEI Qiao-ying, YU Tong, SONG Xiao-ming. Integration of the metabolome and transcriptome reveals the metabolites and genes related to nutritional and medicinal value in Coriandrum sativum[J]. Journal of Integrative Agriculture, 2021, 20(7): 1807-1818.

参考文献

Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biology, 11, R106.
Anders S, Pyl P T, Huber W. 2015. HTSeq - A Python framework to work with high-throughput sequencing data. Bioinformatics, 31, 166–169.
Artati A, Prehn C, Adamski J. 2019. LC-MS/MS-based metabolomics for cell cultures. Methods in Molecular Biology, 1994, 119–130.
Ben Salah N, Bejar D, Snène H, Ouahchi Y, Mehiri N, Louzir B. 2017. The Z-score: A new tool in the interpretation of spirometric data. La Tunisie Medicale, 95, 767–771.
Beshir W F, Tohge T, Watanabe M, Hertog M, Hoefgen R, Fernie A R, Nicolaï B M. 2019. Non-aqueous fractionation revealed changing subcellular metabolite distribution during apple fruit development. Horticulture Research, 6, 98.
Bhat W F, Ahmed A, Abbass S, Afsar M, Bano B, Masood A. 2020. Deciphering the nature of caffeic acid to inhibit the HSA aggregation induced by glyoxal. Protein and Peptide Letters, 27, 725–735.
BIG Data Center Members. 2019. Database resources of the BIG data center in 2019. Nucleic Acids Research, 47, D8–D14.
Cho H W, Kim S B, Jeong M K, Park Y, Miller N G, Ziegler T R, Jones D P. 2008. Discovery of metabolite features for the modelling and analysis of high-resolution NMR spectra. International Journal of Data Mining and Bioinformatics, 2, 176–192.
Choudhary S, Naika M B N, Sharma R, Meena R D, Singh R, Lal G. 2019. Transcriptome profiling of Coriander: A dual purpose crop unravels stem gall resistance genes. Journal of Genetics, 98, 19.
Cory H, Passarelli S, Szeto J, Tamez M, Mattei J. 2018. The role of polyphenols in human health and food systems: A mini-review. Frontiers in Nutrition, 5, 87.
David C C, Jacobs D J. 2014. Principal component analysis: A method for determining the essential dynamics of proteins. Methods in Molecular Biology, 1084, 193–226.
DellaPenna D. 2005. A decade of progress in understanding vitamin E synthesis in plants. Journal of Plant Physiology, 162, 729–737.
Ferlazzo N, Curro M, Giunta M L, Longo D, Rizzo V, Caccamo D, Ientile R. 2020. Up-regulation of HIF-1α is associated with neuroprotective effects of agmatine against rotenone-induced toxicity in differentiated SH-SY5Y cells. Amino Acids, 52, 171–179.
Freitas A E, Neis V B, Rodrigues A L S. 2016. Agmatine, a potential novel therapeutic strategy for depression. European Neuropsychopharmacology, 26, 1885–1899.
Gromski P S, Muhamadali H, Ellis D I, Xu Y, Correa E, Turner M L, Goodacre R. 2015. A tutorial review: Metabolomics and partial least squares-discriminant analysis - a marriage of convenience or a shotgun wedding. Analytica Chimica Acta, 879, 10–23.
Grusak M A, DellaPenna D. 1999. Improving the nutrient composition of plants to enhance human nutrition and health. Annual Review of Plant Physiology and Plant Molecular Biology, 50, 133–161.
Habtemariam S. 2017. Protective effects of caffeic acid and the Alzheimer’s brain: An update. Mini Reviews in Medicinal Chemistry, 17, 667–674.
Ivanov B N. 2014. Role of ascorbic acid in photosynthesis. Biochemistry Biokhimiia, 79, 282–289.
Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y. 2008. KEGG for linking genomes to life and the environment. Nucleic Acids Research, 36, D480–D484.
Karunanandaa B, Qi Q, Hao M, Baszis S R, Jensen P K, Wong Y H, Jiang J, Venkatramesh M, Gruys K J, Moshiri F, Post-Beittenmiller D, Weiss J D, Valentin H E. 2005. Metabolically engineered oilseed crops with enhanced seed tocopherol. Metabolic Engineering, 5–6, 384–400.
Kim D, Langmead B, Salzberg S L. 2015. HISAT: A fast spliced aligner with low memory requirements. Nature Methods, 12, 357–360.
Kotagale N R, Ali M T, Chopde C T, Umekar M J, Taksande B G. 2018. Agmatine inhibits nicotine withdrawal induced cognitive deficits in inhibitory avoidance task in rats: Contribution of α(2)-adrenoceptors. Pharmacology Biochemistry and Behavior, 167, 42–49.
Krautler B. 2016. Breakdown of chlorophyll in higher plants - phyllobilins as abundant, yet hardly visible signs of ripening, senescence, and cell death. Angewandte Chemie International Edition, 55, 4882–4907.
Laribi B, Kouki K, M’Hamdi M, Bettaieb T. 2015. Coriander (Coriandrum sativum L.) and its bioactive constituents. Fitoterapia, 103, 9–26.
Laube G, Bernstein H G. 2017. Agmatine: Multifunctional arginine metabolite and magic bullet in clinical neuroscience? The Biochemical Journal, 474, 2619–2640.
Li X F, Zhu J Y, Tian L X, Ma X Y, Fan X, Luo L, Yu J, Sun Y, Yang X, Tang W Q, Ma W, Yan J, Xu X, Liang H P. 2020. Agmatine protects against the progression of sepsis through the imidazoline I2 receptor-ribosomal S6 kinase 2-nuclear factor-κB signaling pathway. Critical Care Medicine, 48, e40–e47.
Li X L, Zhang X P, Ye L, Kang Z J, Jia D H, Yang L F, Zhang B. 2019. LC-MS-based metabolomic approach revealed the significantly different metabolic profiles of five commercial truffle species. Frontiers in Microbiology, 10, 2227.
Li X Y, Wang L H, Wang S M, Yang Q, Zhou Q, Huang X H. 2018. A preliminary analysis of the effects of bisphenol A on the plant root growth via changes in endogenous plant hormones. Ecotoxicology and Environmental Safety, 150, 152–158.
Liu Q Q, Luo L, Zheng L Q. 2018. Lignins: Biosynthesis and biological functions in plants. International Journal of Molecular Sciences, 19, 335.
Love M I, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15, 550.
Matejczyk M, Swislocka R, Kalinowska M, Swidersk G, Lewandowsk W, Jablonska-Trypuo A. 2017. Monitoring of synergistic enhancement of caffeic acid on Escherichia coli K-12 reca::GFP strain treated with dacarbazine. Acta Poloniae Pharmaceutica, 74, 809–816.
Munir N, Cheng C Z, Xia C S, Xu X M, Nawaz M A, Iftikhar J, Chen Y K, Lin Y L, Lai Z X. 2019. RNA-seq analysis reveals an essential role of tyrosine metabolism pathway in response to root-rot infection in Gerbera hybrida. PLoS ONE, 14, e0223519.
Munne-Bosch S. 2005. Linking tocopherols with cellular signaling in plants. The New Phytologist, 166, 363–366.
Munne-Bosch S, Weiler E W, Alegre L, Muller M, Duchting P, Falk J. 2007. Alpha-tocopherol may influence cellular signaling by modulating jasmonic acid levels in plants. Planta, 225, 681–691.
Neis V B, Rosa P B, Olescowicz G, Rodrigues A L S. 2017. Therapeutic potential of agmatine for CNS disorders. Neurochemistry International, 108, 318–331.
Ning X H, Ren X B, Xie X F, Yan P, Wang D H, Huang X S. 2020. A caffeic acid phenethyl ester analog inhibits the proliferation of nasopharyngeal carcinoma cells via targeting epidermal growth factor receptor. Journal of Biochemical and Molecular Toxicology, 34, e22491.
Schenck C A, Maeda H A. 2018. Tyrosine biosynthesis, metabolism, and catabolism in plants. Phytochemistry, 149, 82–102.
Smirnoff N, Wheeler G L. 2000. Ascorbic acid in plants: Biosynthesis and function. Critical Reviews in Biochemistry and Molecular Biology, 35, 291–314.
Soll J, Schultz G, Joyard J, Douce R, Block M A. 1985. Localization and synthesis of prenylquinones in isolated outer and inner envelope membranes from spinach chloroplasts. Archives of Biochemistry and Biophysics, 238, 290–299.
Song X M, Liu G F, Duan W K, Liu T K, Huang Z N, Ren J, Li Y, Hou X L. 2014. Genome-wide identification, classification and expression analysis of the heat shock transcription factor family in Chinese cabbage. Molecular Genetics and Genomics, 289, 541–551.
Song X M, Liu G F, Huang Z N, Duan W K, Tan H W, Li Y, Hou X L. 2016. Temperature expression patterns of genes and their coexpression with LncRNAs revealed by RNA-Seq in non-heading Chinese cabbage. BMC Genomics, 17, 297.
Song X M, Nie F L, Chen W, Ma X, Gong K, Yang Q H, Wang J P, Li N, Sun P C, Pei Q Y, Yu T, Hu J J, Li X Y, Wu T, Feng S Y, Li X Q, Wang X Y. 2020. Coriander Genomics Database: A genomic, transcriptomic, and metabolic database for Coriander. Horticulture Research, 7, 55.
Song X M, Wang J P, Li N, Yu J G, Meng F B, Wei C D, Liu C, Chen W, Nie F L, Zhang Z K, Gong K, Li X Y, Hu J J, Yang Q H, Li Y X, Li C J, Feng S Y, Guo H, Yuan J Q, Pei Q Y, et al. 2019. Deciphering the high-quality genome sequence of Coriander that causes controversial feelings. Plant Biotechnology Journal, 18, 1444–1456.
Stickle D, Bohrer A, Berger R, Morrissey J, Klahr S, Turk J. 1996. Quantitation of the putative neurotransmitter agmatine as the hexafluoroacetylacetonate derivative by stable Isotope dilution gas chromatography and negative-ion chemical ionization mass spectrometry. Analytical Biochemistry, 238, 129–136.
Tanida I, Shirasago Y, Suzuki R, Abe R, Wakita T, Hanada K, Fukasawa M. 2015. Inhibitory effects of caffeic acid, a coffee-related organic acid, on the propagation of hepatitis C virus. Japanese Journal of Infectious Diseases, 68, 268–275.
Trapnell C, Williams B A, Pertea G, Mortazavi A, Kwan G, van Baren M J, Salzberg S L, Wold B J, Pachter L. 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology, 28, 511–515.
Tulsani N J, Hamid R, Jacob F, Umretiya N G, Nandha A K, Tomar R S, Golakiya B A. 2020. Transcriptome landscaping for gene mining and SSR marker development in Coriander (Coriandrum sativum L.). Genomics, 112, 1545–1553.
Wang M, Toda K, Block A, Maeda H A. 2019. TAT1 and TAT2 tyrosine aminotransferases have both distinct and shared functions in tyrosine metabolism and degradation in Arabidopsis thaliana. The Journal of Biological Chemistry, 294, 3563–3576.
Wi?niewska A, Olszanecki R, Totoń-?urańska J, Ku? K, Stachowicz A, Suski M, G?bska A, Gajda M, Jawień J, Korbut R. 2017. Anti-atherosclerotic action of agmatine in ApoE-knockout mice. International Journal of Molecular Sciences, 18, 1706.
Yella S S T, Kumar R N, Ayyanna C, Varghese A M, Amaravathi P, Vangoori Y. 2019. The combined effect of Trigonella foenum seeds and Coriandrum sativum leaf extracts in alloxan-induced diabetes mellitus wistar albino rats. Bioinformation, 15, 716–722.
Young M D, Wakefield M J, Smyth G K, Oshlack A. 2010. Gene ontology analysis for RNA-seq: Accounting for selection bias. Genome Biology, 11, R14.
Zhang N, Chen Y, Zhao Y, Fan D, Li L, Yan B, Tao G, Zhao J, Zhang H, Wang M. 2020. Caffeic acid assists microwave heating to inhibit the formation of mutagenic and carcinogenic PhIP. Food Chemistry, 317, 126447.
Zhang Y B, Tang W, Wang L H, Hu Y W, Liu X W, Liu Y S. 2019. Kiwifruit (Actinidia chinensis) R1R2R3-MYB transcription factor AcMYB3R enhances drought and salinity tolerance in Arabidopsis thaliana. Journal of Integrative Agriculture, 18, 417–427.
Zhao T T, Wang Z Y, Bao Y F, Zhang X C, Yang H H, Zhang D Y, Jiang J B, Zhang H, Li J F, Chen Q S, Xu X Y. 2019. Downregulation of the SL-ZH13 transcription factor gene expression decreases drought tolerance of tomato. Journal of Integrative Agriculture, 18, 1579–1586.