SmMYB2 promotes salvianolic acid biosynthesis in the medicinal herb Salvia miltiorrhiza.
CYP98A14
Salvia miltiorrhiza
SmMYB2
anthocyanin
rosmarinic acid
salvianolic acid B
Journal
Journal of integrative plant biology
ISSN: 1744-7909
Titre abrégé: J Integr Plant Biol
Pays: China (Republic : 1949- )
ID NLM: 101250502
Informations de publication
Date de publication:
Nov 2020
Nov 2020
Historique:
received:
01
03
2020
accepted:
27
04
2020
pubmed:
29
4
2020
medline:
22
6
2021
entrez:
29
4
2020
Statut:
ppublish
Résumé
MYB transcription factors play vital roles in plant growth and metabolism. The phytohormone methyl jasmonate (MeJA) promotes phenolic acid accumulation in the medicinal herb Salvia miltiorrhiza, but the regulatory mechanism is poorly understood. Here, we identified the MeJA-responsive R2R3-MYB transcription factor gene SmMYB2 from a transcriptome library produced from MeJA-treated S. miltiorrhiza hairy roots. SmMYB2 expression was tightly correlated with the expression of key salvianolic acid biosynthetic genes including CYP98A14. SmMYB2 was highly expressed in the periderm of S. miltiorrhiza and SmMYB2 localized to the nucleus. Overexpressing SmMYB2 in S. miltiorrhiza hairy roots significantly increased the levels of salvianolic acids (including rosmarinic acid and salvianolic acid B) by upregulating salvianolic acid biosynthetic genes such as CYP98A14. SmMYB2 binds to the MYB-binding motifs in the promoter of CYP98A14, as confirmed by a dual-luciferase assay and electrophoretic mobility shift assays. Anthocyanin contents were significantly higher in SmMYB2-overexpressing hairy root lines than the control, primarily due to the increased expression of CHI, DFR, and ANS. These findings reveal the novel regulatory role of SmMYB2 in MeJA-mediated phenolic acid biosynthesis, providing a useful target gene for metabolic engineering and shedding light on the salvianolic acid regulatory network.
Substances chimiques
Alkenes
0
Plant Proteins
0
Polyphenols
0
salvianolic acid
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1688-1702Subventions
Organisme : National Natural Science Fund of China
ID : 81522049
Organisme : National Natural Science Fund of China
ID : 31571735
Organisme : National Natural Science Fund of China
ID : 31270007
Organisme : National Natural Science Fund of China
ID : 30900110
Organisme : "Dawn" Program of Shanghai Education Commission
ID : 16SG38
Organisme : Shanghai Science and Technology Committee Project
ID : 17JC1404300
Organisme : Shanghai Science and Technology Committee Project
ID : 15430502700
Organisme : Zhejiang Provincial Wanren Program for Leading Talents of Science and Technology Innovation
ID : 2018R52050
Organisme : Zhejiang Provincial Program for the Cultivation of High-level Innovative Health talents
ID : 2018-62-3
Organisme : New Century Talent Project
ID : NECT-13-0902
Organisme : Key University (Traditional Chinese Pharmacology), Zhejiang Chinese Medical University
ID : ZYAOX2018019
Informations de copyright
© 2020 Institute of Botany, Chinese Academy of Sciences.
Références
Ampomah-Dwamena C, Thrimawithana AH, Dejnoprat S, Lewis D, Espley RV, Allan AC (2019) A kiwifruit (Actinidia deliciosa) R2R3-MYB transcription factor modulates chlorophyll and carotenoid accumulation. New Phytol 221: 309-325
An X, Tian Y, Chen K, Liu X, Liu D, Xie X, Cheng C, Cong P, Hao Y (2015) MdMYB9 and MdMYB11 are involved in the regulation of the JA-induced biosynthesis of anthocyanin and proanthocyanidin in apples. Plant Cell Physiol 56: 650-662
Anwar M, Yu W, Yao H, Zhou P, Allan AC, Zeng L (2019) NtMYB3, an R2R3-MYB from Narcissus, regulates flavonoid biosynthesis. Int J Mol Sci 20: pii: E5456
Bai Y, Li C, Zhang J, Li S, Luo X, Yao H, Chen H, Zhao H, Park SU, Wu Q (2014) Characterization of two tartary buckwheat R2R3-MYB transcription factors and their regulation of proanthocyanidin biosynthesis. Physiol Plant 152: 431-440
Borevitz JO, Xia Y, Blount J, Dixon RA, Lamb C (2000) Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12: 2383-2394
Cao W, Wang Y, Shi M, Hao X, Zhao W, Wang Y, Ren J, Kai G (2018) Transcription factor SmWRKY1 positively promotes the biosynthesis of tanshinones in Salvia miltiorrhiza. Front Plant Sci 9: 554
Chen L, Hu B, Qin Y, Hu G, Zhao J (2019) Advance of the negative regulation of anthocyanin biosynthesis by MYB transcription factors. Plant Physiol Biochem 136: 178-187
Chen M, Yan T, Shen Q, Lu X, Pan Q, Huang Y, Tang Y, Fu X, Liu M, Jiang W, Lv Z, Shi P, Ma Y, Hao X, Zhang L, Li L, Tang K (2017) GLANDULAR TRICHOME-SPECIFIC WRKY 1 promotes artemisinin biosynthesis in Artemisia annua. New Phytol 214: 304-316
Cheng T (2006) Danshen: A popular Chinese cardiac herbal drug. J Am Coll Cardiol 47: 1499-1500
Czemmel S, Heppel SC, Bogs J (2012) R2R3 MYB transcription factors: Key regulators of the flavonoid biosynthetic pathway in grapevine. Protoplasma 249(Suppl 2): S109-S118
Deng C, Hao X, Shi M, Fu R, Wang Y, Zhang Y, Zhou W, Feng Y, Nokwanda PM, Kai G (2019) Tanshinone production could be increased by the expression of SmWRKY2 in Salvia miltiorrhiza hairy roots. Plant Sci 284: 1-8
Deng Y, Li C, Li H, Lu S (2018) Identification and characterization of flavonoid biosynthetic enzyme genes in Salvia miltiorrhiza (Lamiaceae). Molecules 23: pii: E1467
Di P, Zhang L, Chen J, Tan H, Xiao Y, Dong X, Zhou X, Chen W (2013) ¹³C tracer reveals phenolic acids biosynthesis in hairy root cultures of Salvia miltiorrhiza. ACS Chem Biol 8: 1537-1548
Ding K, Pei T, Bai Z, Jia Y, Ma P, Liang Z (2017) SmMYB36, a novel R2R3-MYB transcription factor, enhances tanshinone accumulation and decreases phenolic acid content in Salvia miltiorrhiza hairy roots. Sci Rep 7: 5104
Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15: 573-581
Fu L, Han B, Zhou Y, Ren J, Cao WZ, Patel G, Kai GY, Zhang J (2020) The anticancer properties of tanshinones and the pharmacological effects of their active ingredients. Front Pharmacol 11: 193
Hao X, Pu Z, Cao G, You D, Zhou Y, Deng C, Shi M, Nile SH, Wang Y, Zhou W, Kai G (2020) Tanshinone and salvianolic acid biosynthesis are regulated by SmMYB98 in Salvia miltiorrhiza hairy roots. J Adv Res 23: 1-12
Höll J, Vannozzi A, Czemmel S, D'Onofrio C, Walker AR, Rausch T, Lucchin M, Boss PK, Dry IB, Bogs J (2013) The R2R3-MYB transcription factors MYB14 and MYB15 regulate stilbene biosynthesis in Vitis vinifera. Plant Cell 25: 4135-4149
Huang Q, Sun M, Yuan T, Wang Y, Shi M, Lu S, Tang B, Pan J, Wang Y, Kai G (2019) The AP2/ERF transcription factor SmERF1L1 regulates the biosynthesis of tanshinones and phenolic acids in Salvia miltiorrhiza. Food Chem 274: 368-375
Kai G, Xu H, Zhou C, Liao P, Xiao J, Luo X, You L, Zhang L (2011) Metabolic engineering tanshinone biosynthetic pathway in Salvia miltiorrhiza hairy root cultures. Metab Eng 13: 319-327
Landmark K (1997) Acetylsalicylic acid in the treatment of cardiovascular and cerebrovascular diseases. Tidsskr Nor Laegeforen 117: 4432-4436
Li C, Lu S (2014) Genome-wide characterization and comparative analysis of R2R3-MYB transcription factors shows the complexity of MYB-associated regulatory networks in Salvia miltiorrhiza. BMC Genomics 15: 277
Li H, Liu J, Pei T, Bai Z, Han R, Liang Z (2019) Overexpression of SmANS enhances anthocyanin accumulation and alters phenolic acids content in Salvia miltiorrhiza and Salvia miltiorrhiza Bge f. alba plantlets. Int J Mol Sci 20: pii: E2225
Li M, Chen J, Peng Y, Wu Q, Xiao P (2008) Investigation of Danshen and related medicinal plants in China. J Ethnopharmacol 120: 419-426
Li S, Wu Y, Kuang J, Wang H, Du T, Huang Y, Zhang Y, Cao X, Wang Z (2018) SmMYB111 is a key factor to phenolic acid biosynthesis and interacts with both SmTTG1 and SmbHLH51 in Salvia miltiorrhiza. J Agric Food Chem 66: 8069-8078
Liang Z, Ma Y, Xu T, Cui B, Liu Y, Guo Z, Yang D (2013) Effects of abscisic acid, gibberellin, ethylene and their interactions on production of phenolic acids in Salvia miltiorrhiza bunge hairy roots. PLoS One 8: e72806
Liu B, Du Y, Cong L, Jia X, Ge Y (2016) Danshen (Salvia miltiorrhiza) compounds improve the biochemical indices of the patients with coronary heart disease. Evid Based Complement Alternat Med 2016: 9781715
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408
Ni J, Zhao Y, Tao R, Yin L, Gao L, Strid Å, Qian M, Li J, Li Y, Shen J, Teng Y, Bai S (2019) Ethylene mediates the branching of the jasmonate-induced flavonoid biosynthesis pathway by suppressing anthocyanin biosynthesis in red Chinese pear fruits. Plant Biotechnol J 18: 1223-1240
Ren J, Fu L, Nile SH, Zhang J, Kai G (2019) Salvia miltiorrhiza in treating cardiovascular diseases: A review on its pharmacological and clinical applications. Front Pharmacol 10: 753
Rosinski JA, Atchley WR (1998) Molecular evolution of the Myb family of transcription factors: Evidence for polyphyletic origin. J Mol Evol 46: 74-83
Shi M, Huang F, Deng C, Wang Y, Kai G (2019) Bioactivities, biosynthesis and biotechnological production of phenolic acids in Salvia miltiorrhiza. Crit Rev Food Sci Nutr 59: 953-964
Sun M, Shi M, Wang Y, Huang Q, Yuan T, Wang Q, Wang C, Zhou W, Kai G (2019) The AP2/ERF transcription factor SmERF115 positively regulates the biosynthesis of phenolic acids in Salvia miltiorrhiza. J Exp Bot 70: 243-254
Wang L, Lu W, Ran L, Dou L, Yao S, Hu J, Fan D, Li C, Luo K (2019a) R2R3-MYB transcription factor MYB6 promotes anthocyanin and proanthocyanidin biosynthesis but inhibits secondary cell wall formation in Populus tomentosa. Plant J 99: 733-751
Wang L, Tang W, Hu Y, Zhang Y, Sun J, Guo X, Lu H, Yang Y, Fang C, Niu X, Yue J, Fei Z, Liu Y (2019b) A MYB/bHLH complex regulates tissue-specific anthocyanin biosynthesis in the inner pericarp of red-centered kiwifruit Actinidia chinensis cv. Hongyang. Plant J 99: 359-378
Xiao Y, Gao S, Di P, Chen J, Chen W, Zhang L (2009) Methyl jasmonate dramatically enhances the accumulation of phenolic acids in Salvia miltiorrhiza hairy root cultures. Physiol Plant 137: 1-9
Xiao Y, Zhang L, Gao S, Saechao SS, Di P, Chen J, Chen W (2011) The c4h, tat, hppr and hppd genes prompted engineering of rosmarinic acid biosynthetic pathway in Salvia miltiorrhiza hairy root cultures. PLoS One 6: e29713
Xu H, Song J, Luo H, Zhang Y, Li Q, Zhu Y, Xu J, Li Y, Song C, Wang B, Sun W, Shen G, Zhang X, Qian J, Ji A, Xu Z, Luo X, He L, Li C, Sun C, Yan H, Cui G, Li X, Li X, Wei J, Liu J, Wang Y, Hayward A, Nelson D, Ning Z, Peters RJ, Qi X, Chen S (2016) Analysis of the genome sequence of the medicinal plant Salvia miltiorrhiza. Mol Plant 9: 949-952
Yang N, Zhou W, Su J, Wang X, Li L, Wang L, Cao X, Wang Z (2017) Overexpression of SmMYC2 increases the production of phenolic acids in Salvia miltiorrhiza. Front Plant Sci 8: 1804
Zhang J, Zhou L, Zheng X, Zhang J, Yang L, Tan R, Zhao S (2017) Overexpression of SmMYB9b enhances tanshinone concentration in Salvia miltiorrhiza hairy roots. Plant Cell Rep 36: 1297-1309
Zhang S, Ma P, Yang D, Li W, Liang Z, Liu Y, Liu F (2013) Cloning and characterization of a putative R2R3 MYB transcriptional repressor of the rosmarinic acid biosynthetic pathway from Salvia miltiorrhiza. PLoS One 8: e73259
Zhang Y, Li X, Wang Z (2010) Antioxidant activities of leaf extract of Salvia miltiorrhiza Bunge and related phenolic constituents. Food Chem Toxicol 48: 2656-2662
Zhang Y, Wang Z (2009) Phenolic composition and antioxidant activities of two Phlomis species: A correlation study. C R Biol 332: 816-826
Zhang Y, Yan Y, Wu Y, Hua W, Chen C, Ge Q, Wang Z (2014) Pathway engineering for phenolic acid accumulations in Salvia miltiorrhiza by combinational genetic manipulation. Metab Eng 21: 71-80
Zhou W, Huang Q, Wu X, Zhou Z, Ding M, Shi M, Huang F, Li S, Kai G (2017) Comprehensive transcriptome profiling of Salvia miltiorrhiza for discovery of genes associated with the biosynthesis of tanshinones and phenolic acids. Sci Rep 7: 10554
Zhou Z, Tan H, Li Q, Chen J, Gao S, Wang Y, Chen W, Zhang L (2018) CRISPR/Cas9-mediated efficient targeted mutagenesis of RAS in Salvia miltiorrhiza. Phytochemistry 148: 63-70