Overexpression of SmANS enhances anthocyanin accumulation and alters phenolic acids content in salvia miltiorrhiza and salvia miltiorrhiza bge f. Alba plantlets

International Journal of Molecular Sciences

Volumn 20, Issue 9, 2019, Pages

  Li, Hongyan ^a   Liu, Jingling ^a   Pei, Tianlin ^a   Bai, Zhenqing ^a   Han, Ruilian ^b   Liang, Zongsuo ^a,b  

^a NORTHWEST A F UNIVERSITY   (China)

^b ZHEJIANG SCI TECH UNIVERSITY   (China)

Author keywords

Anthocyanin; Flavonoids; Phenolic acids; Salvia miltiorrhiza; Salvia miltiorrhiza Bge f. alba; SmANS

Indexed keywords

ANTHOCYANIDIN SYNTHASE; ANTHOCYANIN; CATECHIN; EPICATECHIN; FLAVONOID; PHYTOHORMONE; PLANT PROTEIN; POLYPHENOL; ROSMARINIC ACID; SALVIANOLIC ACID B; UNCLASSIFIED DRUG; HYDROXYBENZOIC ACID DERIVATIVE; OXYGENASE; PHENOLIC ACID;

ARTICLE; BIOINFORMATICS; BIOSYNTHESIS; CELL MEMBRANE; CONTROLLED STUDY; DOWN REGULATION; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; FLOWER COLOR; GENE EXPRESSION; GENE OVEREXPRESSION; GOLGI COMPLEX; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; NONHUMAN; PETAL; PISTIL; PLANT GROWTH; PLANT LEAF; PLANT ROOT; PLANT STEM; PLANTLET; PLASTID; PROTEIN LOCALIZATION; REAL TIME POLYMERASE CHAIN REACTION; SALVIA; SALVIA MILTIORRHIZA; SALVIA MILTIORRHIZA BGE F. ALBA; STAMEN; UPREGULATION; GENETICS; METABOLISM;

ANTHOCYANINS; HYDROXYBENZOATES; OXYGENASES; PLANT PROTEINS; SALVIA MILTIORRHIZA;

EID: 85065783948     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms20092225     Document Type: Article

References (59)

1. Ma, Y.; Yuan, L.; Wu, B.; Li, X.E.; Chen, S.; Lu, S. Genome-wide identification and characterization of novel genes involved in terpenoid biosynthesis in Salvia miltiorrhiza. J. Exp. Bot. 2012, 63, 2809–2823. [CrossRef]
2. Hao, G.P.; Jiang, X.Y.; Feng, L.; Tao, R.; Li, Y.L.; Huang, L.Q. Cloning, molecular characterization and functional analysis of a putative R2R3-MYB transcription factor of the phenolic acid biosynthetic pathway in S. miltiorrhiza Bge f. alba. Plant Cell Tissue Organ Cult. 2016, 124, 151–168. [CrossRef]
3. Zhang, S.; Ma, P.; Yang, D.; Li, W.; Liang, Z.; Liu, Y.; Liu, F. Cloning and characterization of a putative R2R3 MYB transcriptional repressor of the rosmarinic acid biosynthetic pathway from Salvia miltiorrhiza. PLoS ONE 2013, 8, e73259. [CrossRef]
4. Ravipati, A.S.; Zhang, L.; Koyyalamudi, S.R.; Jeong, S.C.; Reddy, N.; Bartlett, J.; Smith, P.T.; Shanmugam, K.; Munch, G.; Wu, M.J.; et al. Antioxidant and anti-inflammatory activities of selected Chinese medicinal plants and their relation with antioxidant content. BMC Complement. Altern. Med. 2012, 12, 173. [CrossRef] [PubMed]
5. Tanaka, Y.; Sasaki, N.; Ohmiya, A. Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. Plant J. 2008, 54, 733–749. [CrossRef]
6. Veitch, N.C.; Grayer, R.E.J. Flavonoids and their glycosides, including anthocyanins. Nat. Prod. Rep. 2008, 25, 555–611. [CrossRef] [PubMed]
7. Winkel-Shirley, B. Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol. 2001, 126, 485–493. [CrossRef] [PubMed]
8. Nakabayashi, R.; Saito, K. Integrated metabolomics for abiotic stress responses in plants. Curr. Opin. Plant Biol. 2015, 24, 10–16. [CrossRef]
9. Medina-Puche, L.; Cumplido-Laso, G.; Amil-Ruiz, F.; Hoffmann, T.; Ring, L.; Rodriguez-Franco, A.; Luis Caballero, J.; Schwab, W.; Munoz-Blanco, J.; Blanco-Portales, R. MYB10 plays a major role in the regulation of flavonoid/phenylpropanoid metabolism during ripening of Fragaria ananassa fruits. J. Exp. Bot. 2014, 65, 401–417. [CrossRef] [PubMed]
10. Qi, T.; Song, S.; Ren, Q.; Wu, D.; Huang, H.; Chen, Y.; Fan, M.; Peng, W.; Ren, C.; Xie, D. The Jasmonate-ZIM-Domain Proteins Interact with the WD-Repeat/bHLH/MYB Complexes to Regulate Jasmonate-Mediated Anthocyanin Accumulation and Trichome Initiation in Arabidopsis thaliana. Plant Cell 2011, 23, 1795–1814. [CrossRef] [PubMed]
11. Yousuf, B.; Gul, K.; Wani, A.A.; Singh, P. Health benefits of anthocyanins and their encapsulation for potential use in food systems: A review. Crit. Rev. Food Sci. 2016, 56, 2223–2230. [CrossRef]
12. Zhang, Y.; Yan, Y.P.; Wu, Y.C.; Hua, W.P.; Chen, C.; Ge, Q.; Wang, Z.Z. Pathway engineering for phenolic acid accumulations in Salvia miltiorrhiza by combinational genetic manipulation. Metab. Eng. 2014, 21, 71–80. [CrossRef] [PubMed]
13. Zhang, S.; Li, H.; Liang, X.; Yan, Y.; Xia, P.; Jia, Y.; Liang, Z. Enhanced production of phenolic acids in Salvia miltiorrhiza hairy root cultures by combing the RNAi-mediated silencing of chalcone synthase gene with salicylic acid treatment. Biochem. Eng. J. 2015, 103, 185–192. [CrossRef]
14. Wang, N.; Xu, H.; Jiang, S.; Zhang, Z.; Lu, N.; Qiu, H.; Qu, C.; Wang, Y.; Wu, S.; Chen, X. MYB12 and MYB22 play essential roles in proanthocyanidin and flavonol synthesis in red-fleshed apple (Malus sieversii f. niedzwetzkyana). Plant J. 2017, 90, 276–292. [CrossRef] [PubMed]
15. Li, P.; Chen, B.; Zhang, G.; Chen, L.; Dong, Q.; Wen, J.; Mysore, K.S.; Zhao, J. Regulation of anthocyanin and proanthocyanidin biosynthesis by Medicago truncatula bHLH transcription factor MtTT8. New Phytol. 2016, 210, 905–921. [CrossRef]
16. Wang, N.; Qu, C.; Jiang, S.; Chen, Z.; Xu, H.; Fang, H.; Su, M.; Zhang, J.; Wang, Y.; Liu, W.; et al. The proanthocyanidin-specific transcription factor MdMYBPA1 initiates anthocyanin synthesis under low-temperature conditions in red-fleshed apples. Plant J. 2018, 96, 39–55. [CrossRef]
17. Xu, W.; Grain, D.; Bobet, S.; Le Gourrierec, J.; Thevenin, J.; Kelemen, Z.; Lepiniec, L.; Dubos, C. Complexity and robustness of the flavonoid transcriptional regulatory network revealed by comprehensive analyses of MYB-bHLH-WDR complexes and their targets in Arabidopsis seed. New Phytol. 2014, 202, 132–144. [CrossRef]
18. Xu, W.; Dubos, C.; Lepiniec, L. Transcriptional control of flavonoid biosynthesis by MYB-bHLH-WDR complexes. Trends Plant Sci. 2015, 20, 176–185. [CrossRef] [PubMed]
19. Li, S.; Wu, Y.; Kuang, J.; Wang, H.; Du, T.; Huang, Y.; Zhang, Y.; Cao, X.; Wang, Z. SmMYB111 is a key factor to phenolic acid biosynthesis and interacts with both SmTTG1 and SmbHLH51 in Salvia miltiorrhiza. J. Agric. Food Chem. 2018, 66, 8069–8078. [CrossRef] [PubMed]
20. Ding, K.; Pei, T.; Bai, Z.; Jia, Y.; Ma, P.; Liang, Z. SmMYB36, a Novel R2R3-MYB transcription factor, enhances tanshinone accumulation and decreases phenolic acid content in Salvia miltiorrhiza hairy roots. Sci. Rep. 2017, 7, 5104. [CrossRef]
21. Li, C.; Lu, S. Genome-wide characterization and comparative analysis of R2R3-MYB transcription factors shows the complexity of MYB-associated regulatory networks in Salvia miltiorrhiza. BMC Genom. 2014, 15. [CrossRef]
22. Ben-Simhon, Z.; Judeinstein, S.; Trainin, T.; Harel-Beja, R.; Bar-Ya’akov, I.; Borochov-Neori, H.; Holland, D. A "White" anthocyanin-less pomegranate (Punica granatum L.) caused by an insertion in the coding region of the leucoanthocyanidin dioxygenase (LDOX; ANS) gene. PLoS One 2015, 10, 1–21. [CrossRef] [PubMed]
23. Li, Y.; Fang, J.; Qi, X.; Lin, M.; Zhong, Y.; Sun, L. A key structural gene, AaLDOX, is involved in anthocyanin biosynthesis in all red-fleshed kiwifruit (Actinidia arguta) based on transcriptome analysis. Gene 2018, 648, 31–41. [CrossRef] [PubMed]
24. Rafique, M.Z.; Carvalho, E.; Stracke, R.; Palmieri, L.; Herrera, L.; Feller, A.; Malnoy, M.; Martens, S. Nonsense mutation inside anthocyanidin synthase gene controls pigmentation in yellow raspberry (Rubus idaeus L.). Front. Plant Sci. 2016, 7, 1892. [CrossRef]
25. Yu, Z.; Liao, Y.; da Silva, J.A.T.; Yang, Z.; Duan, J. Differential accumulation of anthocyanins in dendrobium officinale stems with red and green peels. Int. J. Mol. Sci. 2018, 19, 2857. [CrossRef] [PubMed]
26. Liu, Y.; Shi, Z.; Maximova, S.; Payne, M.J.; Guiltinan, M.J. Proanthocyanidin synthesis in Theobroma cacao: genes encoding anthocyanidin synthase, anthocyanidin reductase, and leucoanthocyanidin reductase. BMC Plant Biol. 2013, 13, 1–19. [CrossRef] [PubMed]
27. Jun, J.H.; Xiao, X.; Rao, X.; Dixon, R.A. Proanthocyanidin subunit composition determined by functionally diverged dioxygenases. Nat. Plants 2018, 4, 1034–1043. [CrossRef] [PubMed]
28. Szankowski, I.; Flachowsky, H.; Li, H.; Halbwirth, H.; Treutter, D.; Regos, I.; Hanke, M.-V.; Stich, K.; Fischer, T.C. Shift in polyphenol profile and sublethal phenotype caused by silencing of anthocyanidin synthase in apple (Malus sp.). Planta 2009, 229, 681–692. [CrossRef]
29. Giampieri, F.; Gasparrini, M.; Forbes-Hernandez, T.Y.; Mazzoni, L.; Capocasa, F.; Sabbadini, S.; Alvarez-Suarez, J.M.; Afrin, S.; Rosati, C.; Pandolfini, T.; et al. Overexpression of the anthocyanidin synthase gene in strawberry enhances antioxidant capacity and cytotoxic effects on human hepatic cancer cells. J. Agric. Food Chem. 2018, 66, 581–592. [CrossRef]
30. Shao, Y.X.; Wei, J.B.; Wu, F.L.; Zhang, H.H.; Yang, D.F.; Liang, Z.S.; Jin, W.B. DsTRD: Danshen transcriptional resource database. PLoS ONE 2016, 11, 1–8. [CrossRef]
31. Pei, T.; Ma, P.; Ding, K.; Liu, S.; Jia, Y.; Ru, M.; Dong, J.; Liang, Z. SmJAZ8 acts as a core repressor regulating JA-induced biosynthesis of salvianolic acids and tanshinones in Salvia miltiorrhiza hairy roots. J. Exp. Bot. 2018, 69, 1663–1678. [CrossRef] [PubMed]
32. Deng, Y.; Li, C.; Li, H.; Lu, S. Identification and characterization of flavonoid biosynthetic enzyme genes in Salvia miltiorrhiza (Lamiaceae). Molecules 2018, 23, 1467. [CrossRef]
33. Nakatsuka, T.; Nishihara, M.; Mishiba, K.; Yamamura, S. Two different mutations are involved in the formation of white-flowered gentian plants. Plant Sci. 2005, 169, 949–958. [CrossRef]
34. Jiang, S.-H.; Sun, Q.-G.; Chen, M.; Wang, N.; Xu, H.-F.; Fang, H.-C.; Wang, Y.-C.; Zhang, Z.-Y.; Chen, X.-S. Methylome and transcriptome analyses of apple fruit somatic mutations reveal the difference of red phenotype. BMC Genom. 2019, 20, 1–13. [CrossRef] [PubMed]
35. Yang, N.; Zhao, K.; Li, X.; Zhao, R.; Aslam, M.Z.; Yu, L.; Chen, L. Comprehensive analysis of wintersweet flower reveals key structural genes involved in flavonoid biosynthetic pathway. Gene 2018, 676, 279–289. [CrossRef]
36. Reddy, A.M.; Reddy, V.S.; Scheffler, B.E.; Wienand, U.; Reddy, A.R. Novel transgenic rice overexpressing anthocyanidin synthase accumulates a mixture of flavonoids leading to an increased antioxidant potential. Metab. Eng. 2007, 9, 95–111. [CrossRef] [PubMed]
37. Chen, M.; Xu, M.; Xiao, Y.; Cui, D.; Qin, Y.; Wu, J.; Wang, W.; Wang, G. Fine mapping identifies smfas encoding an anthocyanidin synthase as a putative candidate gene for flower purple color in Solanum melongena L. Int. J. Mol. Sci. 2018, 19, 789. [CrossRef] [PubMed]
38. Xu, Z.-S.; Huang, Y.; Wang, F.; Song, X.; Wang, G.-L.; Xiong, A.-S. Transcript profiling of structural genes involved in cyanidin-based anthocyanin biosynthesis between purple and non-purple carrot (Daucus carota L.) cultivars reveals distinct patterns. BMC Plant Biol. 2014, 14, 262. [CrossRef]
39. Luo, J.R.; Shi, Q.Q.; Niu, L.X.; Zhang, Y.L. Transcriptomic analysis of leaf in tree peony reveals differentially expressed pigments genes. Molecules 2017, 22, 324. [CrossRef]
40. Suzuki, K.; Suzuki, T.; Nakatsuka, T.; Dohra, H.; Yamagishi, M.; Matsuyama, K.; Matsuura, H. RNA-seq-based evaluation of bicolor tepal pigmentation in Asiatic hybrid lilies (Lilium spp.). BMC Genom. 2016, 17, 611. [CrossRef]
41. Sun, Y.; Li, H.; Huang, J.-R. Arabidopsis TT19 functions as a carrier to transport anthocyanin from the cytosol to tonoplasts. Mol. Plant 2012, 5, 387–400. [CrossRef]
42. Wang, H.L.; Wang, W.; Zhang, P.; Pan, Q.H.; Zhan, J.C.; Huang, W.D. Gene transcript accumulation, tissue and subcellular localization of anthocyanidin synthase (ANS) in developing grape berries. Plant Sci. 2010, 179, 103–113. [CrossRef]
43. Hrazdina, G.; Wagner, G.J. Metabolic pathways as enzyme complexes: evidence for the synthesis of phenylpropanoids and flavonoids on membrane associated enzyme complexes. Arch. Biochem. Biophys. 1985, 237, 88–100. [CrossRef]
44. Fujino, N.; Tenma, N.; Waki, T.; Ito, K.; Komatsuzaki, Y.; Sugiyama, K.; Yamazaki, T.; Yoshida, S.; Hatayama, M.; Yamashita, S.; et al. Physical interactions among flavonoid enzymes in snapdragon and torenia reveal the diversity in the flavonoid metabolon organization of different plant species. Plant J. 2018, 94, 372–392. [CrossRef]
45. Chen, C.; Wei, K.; Wang, L.; Ruan, L.; Li, H.; Zhou, X.; Lin, Z.; Shan, R.; Cheng, H. Expression of key structural genes of the phenylpropanoid pathway associated with catechin epimerization in tea cultivars. Front. Plant Sci. 2017, 8, 702. [CrossRef]
46. Li, J.; Zhao, A.; Yu, M.; Li, Y.; Liu, X.; Chen, X. Function analysis of anthocyanidin synthase from Morus alba L. by expression in bacteria and tobacco. Electron. J. Biotechn. 2018, 36, 9–14. [CrossRef]
47. Zhang, J.; Han, Z.Y.; Tian, J.; Zhang, X.; Song, T.-T.; Yao, Y.C. The expression level of anthocyanidin synthase determines the anthocyanin content of crabapple (Malus sp.) petals. Acta Physiol. Plant. 2015, 37, 109. [CrossRef]
48. Mouradov, A.; Spangenberg, G. Flavonoids: A metabolic network mediating plants adaptation to their real estate. Front. Plant Sci. 2014, 5, 620. [CrossRef] [PubMed]
49. Strygina, K.V.; Boerner, A.; Khlestkina, E.K. Identification and characterization of regulatory network components for anthocyanin synthesis in barley aleurone. BMC Plant Biol. 2017, 17, 110–155. [CrossRef]
50. Jun, J.H.; Liu, C.; Xiao, X.; Dixon, R.A. The Transcriptional repressor MYB2 regulates both spatial and temporal patterns of proanthocyandin and anthocyanin pigmentation in Medicago truncatula. Plant Cell 2015, 27, 2860–2879. [CrossRef]
51. Lim, S.H.; Kim, D.H.; Kim, J.K.; Lee, J.Y.; Ha, S.H. A radish basic helix-loop-helix transcription factor, RsTT8 acts a positive regulator for anthocyanin biosynthesis. Front. Plant Sci. 2017, 8. [CrossRef]
52. Yan, Y.; Wang, Z. Genetic transformation of the medicinal plant Salvia miltiorrhiza by Agrobacterium tumefaciens-mediated method. Plant Cell Tissue Organ Cult. 2007, 88, 175–184. [CrossRef]
53. Staheli, J.R.; Boyce, R.; Kovarik, D.; Rose, T.M. CODEHOP PCR and CODEHOP pcr primer design. Meth. Mol. Biol. 2011, 687, 57–73. [CrossRef]
54. Yang, Y.F.; Hou, S.; Cui, G.H.; Chen, S.L.; Wei, J.H.; Huang, L.Q. Characterization of reference genes for quantitative real-time pcr analysis in various tissues of Salvia miltiorrhiza. Mol. Biol. Rep. 2010, 37, 507–513. [CrossRef] [PubMed]
55. Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative pcr and the 2(T)(-delta delta c) method. Methods 2001, 25, 402–408. [CrossRef] [PubMed]
56. Nelson, B.K.; Cai, X.; Nebenfuehr, A. A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 2007, 51, 1126–1136. [CrossRef]
57. Ru, M.; Wang, K.; Bai, Z.; Peng, L.; He, S.; Pei, T.; Jia, Y.; Li, H.; Liang, Z. Molecular cloning and characterisation of two enzymes involved in the rosmarinic acid biosynthesis pathway of Prunella vulgaris L. Plant Cell Tissue Organ Cult. 2017, 128, 381–390. [CrossRef]
58. Mano, H.; Ogasawara, F.; Sato, K.; Higo, H.; Minobe, Y. Isolation of a regulatory gene of anthocyanin biosynthesis in tuberous roots of purple-fleshed sweet potato. Plant Physiol. 2007, 143, 1252–1268. [CrossRef]
59. Xing, B.; Liang, L.; Liu, L.; Hou, Z.; Yang, D.; Yan, K.; Zhang, X.; Liang, Z. Overexpression of SmbHLH148 induced biosynthesis of tanshinones as well as phenolic acids in Salvia miltiorrhiza hairy roots. Plant Cell Rep. 2018, 37, 1681–1692. [CrossRef]