Identification of a cinnamoyl-CoA reductase from Cinnamomum cassia involved in trans-cinnamaldehyde biosynthesis.
Cinnamomum cassia
trans-Cinnamaldehyde
Biosynthetic pathway
Cinnamoyl-CoA reductase
Transcriptome
Journal
Planta
ISSN: 1432-2048
Titre abrégé: Planta
Pays: Germany
ID NLM: 1250576
Informations de publication
Date de publication:
30 Apr 2024
30 Apr 2024
Historique:
received:
30
11
2023
accepted:
16
04
2024
medline:
30
4
2024
pubmed:
30
4
2024
entrez:
30
4
2024
Statut:
epublish
Résumé
The identification of a functional cinnamoyl-CoA reductase enzyme from Cinnamomum cassia involved in trans-cinnamaldehyde biosynthesis offers the potential for enhancing trans-cinnamaldehyde production through genetic engineering. A significant accumulation of trans-cinnamaldehyde has been found in the bark tissues of C. cassia, used in traditional Chinese medicine. trans-Cinnamaldehyde exhibits various pharmacological properties such as anti-inflammatory, analgesic, and protection of the stomach and the digestive tract. However, further elucidation and characterization of the biosynthetic pathway for trans-cinnamaldehyde is required. In this study, we conducted an integrated analysis of trans-cinnamaldehyde accumulation profiles and transcriptomic data from five different C. cassia tissues to identify the genes involved in its biosynthesis. The transcriptome data we obtained included nearly all genes associated with the trans-cinnamaldehyde pathway, with the majority demonstrating high abundance in branch barks and trunk barks. We successfully cloned four C. cassia cinnamoyl-CoA reductases (CcCCRs), a key gene in trans-cinnamaldehyde biosynthesis. We found that the recombinant CcCCR1 protein was the only one that more efficiently converted cinnamoyl-CoA into trans-cinnamaldehyde. CcCCR1 exhibited approximately 14.7-fold higher catalytic efficiency (k
Identifiants
pubmed: 38687380
doi: 10.1007/s00425-024-04419-w
pii: 10.1007/s00425-024-04419-w
doi:
Substances chimiques
Acrolein
7864XYD3JJ
cinnamaldehyde
SR60A3XG0F
Aldehyde Oxidoreductases
EC 1.2.-
cinnamoyl CoA reductase
EC 1.2.1.44
Plant Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
138Subventions
Organisme : Guangdong Basic and Applied Basic Research Foundation
ID : 2020B1515420007
Organisme : The Open Competition Program of Ten Major Directions of Agricultural Science and Technology Innovation for the 14th Five-Year Plan of Guangdong Province, China
ID : 2022SDZG07
Organisme : Nature Science Foundation of China
ID : 32370383
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Baltas M, Lapeyre C, Bedos-Belval F et al (2005) Kinetic and inhibition studies of cinnamoyl-CoA reductase 1 from Arabidopsis thaliana. Plant Physiol Biochem 43(8):746–753
pubmed: 16122934
doi: 10.1016/j.plaphy.2005.06.003
Bang HB, Lee YH, Kim SC et al (2016) Metabolic engineering of Escherichia coli for the production of cinnamaldehyde. Microb Cell Fact 15:16
pubmed: 26785776
pmcid: 4719340
doi: 10.1186/s12934-016-0415-9
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30(15):2114–2120
pubmed: 24695404
pmcid: 4103590
doi: 10.1093/bioinformatics/btu170
Chao N, Li N, Qi Q et al (2017) Characterization of the cinnamoyl-CoA reductase (CCR) gene family in Populus tomentosa reveals the enzymatic active sites and evolution of CCR. Planta 245(1):61–75
pubmed: 27580618
doi: 10.1007/s00425-016-2591-6
Chen XB, Zhang YN, Wan HX et al (2016) Stereoselective organocatalytic oxidation of alcohols to enals: a homologation method to prepare polyenes. Chem Commun 52(17):3532–3535
doi: 10.1039/C5CC10093C
Chen CJ, Chen H, Zhang Y et al (2020) TBtools: An integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13(8):1194–1202
pubmed: 32585190
doi: 10.1016/j.molp.2020.06.009
China Pharmacopeia Commission (2020) Pharmacopoeia of the People’s Republic of China, vol 1. Chinese Medical Science and Technology Press, Beijing, p 142
Conesa A, Götz S, García-Gómez JM et al (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21(18):3674–3676
pubmed: 16081474
doi: 10.1093/bioinformatics/bti610
Davidson NM, Oshlack A (2014) Corset: enabling differential gene expression analysis for de novo assembled transcriptomes. Genome Biol 15:410
pubmed: 25063469
pmcid: 4165373
Doyle AA, Stephens JC (2019) A review of cinnamaldehyde and its derivatives as antibacterial agents. Fitoterapia 139:104405
pubmed: 31707126
doi: 10.1016/j.fitote.2019.104405
Doyle AA, Krämer T, Kavanagh K et al (2019) Cinnamaldehydes: synthesis, antibacterial evaluation, and the effect of molecular structure on antibacterial activity. Res Chem 1:100013
Escamilla-Treviño LL, Shen H, Uppalapati SR et al (2010) Switchgrass (Panicum virgatum) possesses a divergent family of cinnamoyl CoA reductases with distinct biochemical properties. New Phytol 185(1):143–155
pubmed: 19761442
doi: 10.1111/j.1469-8137.2009.03018.x
Gao H, Xu D, Zhang H et al (2020) Transcriptomics and metabolomics analyses reveal the differential accumulation of phenylpropanoids between Cinnamomum cassia Presl and Cinnamomum cassia Presl var. macrophyllum Chu. Ind Crop Prod 148:112282
doi: 10.1016/j.indcrop.2020.112282
Goujon T, Ferret V, Mila I et al (2003) Down-regulation of the AtCCR1 gene in Arabidopsis thaliana: effects on phenotype, lignins and cell wall degradability. Planta 217:218–228
pubmed: 12783329
doi: 10.1007/s00425-003-0987-6
Grabherr MG, Haas BJ, Yassour M et al (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29(7):644–652
pubmed: 21572440
pmcid: 3571712
doi: 10.1038/nbt.1883
Gross GG, Kreiten W (1975) Reduction of coenzyme a thioesters of cinnamic acids with an enzyme preparation from lignifying tissue of Forsythia. FEBS Lett 54(2):259–262
pubmed: 236926
doi: 10.1016/0014-5793(75)80087-1
Guo L, Yao H, Chen W et al (2022) Natural products of medicinal plants: biosynthesis and bioengineering in post-genomic era. Hortic Res 9:uhac223
pubmed: 36479585
pmcid: 9720450
doi: 10.1093/hr/uhac223
Hayashi Y, Sakamoto D, Okamura D (2016) One-pot synthesis of (S)-baclofen via aldol condensation of acetaldehyde with diphenylprolinol silyl ether mediated asymmetric michael reaction as a key step. Org lett 18(1):4–7
pubmed: 26636719
doi: 10.1021/acs.orglett.5b02839
Huang M, Sanchez-Moreiras AM, Abel C et al (2012) The major volatile organic compound emitted from Arabidopsis thaliana flowers, the sesquiterpene (E)-β-caryophyllene, is a defense against a bacterial pathogen. New Phytol 193(4):997–1008
pubmed: 22187939
doi: 10.1111/j.1469-8137.2011.04001.x
Jumper J, Evans R, Pritzel A et al (2021) Highly accurate protein structure prediction with AlphaFold. Nature 596(7873):583–589
pubmed: 34265844
pmcid: 8371605
doi: 10.1038/s41586-021-03819-2
Kim TW (2022) Cinnamaldehyde induces autophagy-mediated cell death through ER stress and epigenetic modification in gastric cancer cells. Acta Pharmacol Sin 43(3):712–723
pubmed: 33980998
doi: 10.1038/s41401-021-00672-x
Kim ME, Na JY, Lee JS (2018) Anti-inflammatory effects of trans-cinnamaldehyde on lipopolysaccharide-stimulated macrophage activation via MAPKs pathway regulation. Immunopharmacol Immunotoxicol 40(3):219–224
pubmed: 29355056
doi: 10.1080/08923973.2018.1424902
Kumar S, Singh S, Singh RKP (2010) Electrochemical synthesis of α, β-unsaturated aldehydes at Pt cathode in the dimethylformamide solvent. J Indian Chem Soc 87(9):1145–1148
Lacombe E, Hawkins S, van Doorsselaere J et al (1997) Cinnamoyl CoA reductase, the first committed enzyme of the lignin branch biosynthetic pathway: cloning, expression and phylogenetic relationships. Plant J 11(3):429–441
pubmed: 9107033
doi: 10.1046/j.1365-313X.1997.11030429.x
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9(4):357–359
pubmed: 22388286
pmcid: 3322381
doi: 10.1038/nmeth.1923
Lauvergeat V, Lacomme C, Lacombe E et al (2001) Two cinnamoyl-CoA reductase (CCR) genes from Arabidopsis thaliana are differentially expressed during development and in response to infection with pathogenic bacteria. Phytochemistry 57(7):1187–1195
pubmed: 11430991
doi: 10.1016/S0031-9422(01)00053-X
Leple JC, Dauwe R, Morreel K et al (2007) Downregulation of cinnamoyl-coenzyme A reductase in poplar: multiple-level phenotyping reveals effects on cell wall polymer metabolism and structure. Plant Cell 19(11):3669–3691
pubmed: 18024569
pmcid: 2174873
doi: 10.1105/tpc.107.054148
Li YQ, Kong DX, Huang RS et al (2013a) Variations in essential oil yields and compositions of Cinnamomum cassia leaves at different developmental stages. Ind Crop Prod 47:92–101
doi: 10.1016/j.indcrop.2013.02.031
Li YQ, Kong DX, Wu H (2013b) Analysis and evaluation of essential oil components of cinnamon barks using GC–MS and FTIR spectroscopy. Ind Crop Prod 41:269–278
doi: 10.1016/j.indcrop.2012.04.056
Li G, Yang Q, Zhang Y et al (2014) Cloning and analysis of the gene encoding Cinnamoyl-CoA reductase from Caragana korshinkii Kom. China Biotechnol 34(1):50–56
Liu J, Zhu J, Jiang HL et al (2010) Pd-catalyzed cascade Heck–Saegusa: direct synthesis of enals from aryl iodides and allyl alcohol. Chem Commun 46(3):415–417
doi: 10.1039/B922351G
Liu L, Stein A, Wittkop B et al (2012) A knockout mutation in the lignin biosynthesis gene CCR1 explains a major QTL for acid detergent lignin content in Brassica napus seeds. Theor Appl Genet 124(8):1573–1586
pubmed: 22350089
doi: 10.1007/s00122-012-1811-0
Mateen S, Rehman MT, Shahzad S et al (2019) Anti-oxidant and anti-inflammatory effects of cinnamaldehyde and eugenol on mononuclear cells of rheumatoid arthritis patients. Eur J Pharmacol 852:14–24
pubmed: 30796902
doi: 10.1016/j.ejphar.2019.02.031
Mirdita M, Schütze K, Moriwaki Y et al (2022). ColabFold: making protein folding accessible to all. Nat Methods 19:679–682
pubmed: 35637307
pmcid: 9184281
doi: 10.1038/s41592-022-01488-1
Pan H, Zhou R, Louie GV et al (2014) Structural studies of cinnamoyl-CoA reductase and cinnamyl-alcohol dehydrogenase, key enzymes of monolignol biosynthesis. Plant Cell 26(9):3709–3727
pubmed: 25217505
pmcid: 4213152
doi: 10.1105/tpc.114.127399
Pichon M, Courbou I, Beckert M et al (1998) Cloning and characterization of two maize cDNAs encoding cinnamoyl-CoA reductase (CCR) and differential expression of the corresponding genes. Plant Mol Biol 38(4):671–676
pubmed: 9747812
doi: 10.1023/A:1006060101866
Pomar F, Merino F, Barceló AR (2002) O-4-Linked coniferyl and sinapyl aldehydes in lignifying cell walls are the main targets of the Wiesner (phloroglucinol-HCl) reaction. Protoplasma 220(1–2):17–28
pubmed: 12417933
doi: 10.1007/s00709-002-0030-y
Robert X, Gouet P (2014) Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res 42(W1):W320–W324
pubmed: 24753421
pmcid: 4086106
doi: 10.1093/nar/gku316
Rohloff J, Bones AM (2005) Volatile profiling of Arabidopsis thaliana - Putative olfactory compounds in plant communication. Phytochemistry 66(16):1941–1955
pubmed: 16081115
doi: 10.1016/j.phytochem.2005.06.021
Sattler SA, Walker AM, Vermerris W et al (2017) Structural and biochemical characterization of cinnamoyl-CoA reductases. Plant Physiol 173(2):1031–1044
pubmed: 27956488
doi: 10.1104/pp.16.01671
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22(22):4673–4680
pubmed: 7984417
pmcid: 308517
doi: 10.1093/nar/22.22.4673
Vanholme R, Meester B, De Ralph J et al (2019) Lignin biosynthesis and its integration into metabolism. Curr Opin Biotechnol 56:230–239
pubmed: 30913460
doi: 10.1016/j.copbio.2019.02.018
Wengenmayer H, Ebel J, Grisebach H (1976) Enzymic synthesis of lignin precursors. Purification and properties of a cinnamoyl-CoA: NADPH reductase from cell suspension cultures of soybean (Glycine max). Eur J Biochem 65(2):529–536
pubmed: 7454
doi: 10.1111/j.1432-1033.1976.tb10370.x
Xue J, Luo D, Xu D et al (2015) CCR1, an enzyme required for lignin biosynthesis in Arabidopsis, mediates cell proliferation exit for leaf development. Plant J 83(3):375–387
pubmed: 26058952
doi: 10.1111/tpj.12902
Zhang SL, Xie HX, Song AG et al (2011) Efficient preparation of trans-α, β-unsaturated aldehydes from saturated aldehydes by oxidative enamine catalysis. Sci China Chem 54:1932–1936
doi: 10.1007/s11426-011-4432-6
Zhou R, Jackson L, Shadle G et al (2010) Distinct cinnamoyl CoA reductases involved in parallel routes to lignin in Medicago truncatula. PNAS 107(41):17803–17808
pubmed: 20876124
pmcid: 2955080
doi: 10.1073/pnas.1012900107
Liu B, Wei G, Hu Z, et al. (2019) Benzaldehyde synthases are encoded by cinnamoyl-CoA reductase genes in cucumber (Cucumis sativus L.). bioRxiv https://doi.org/10.1101/2019.12.26.889071