Molecular cloning and characterisation of two enzymes involved in the rosmarinic acid biosynthesis pathway of Prunella vulgaris L

Plant Cell, Tissue and Organ Culture

Volumn 128, Issue 2, 2017, Pages 381-390

  Ru, Mei ^a   Wang, Kunru ^b   Bai, Zhenqing ^b   Peng, Liang ^c   He, Shaoxuan ^d   Pei, Tianlin ^b   Jia, Yanyan ^b   Li, Hongyan ^b   Liang, Zongsuo ^a,b  

^a INSTITUTE OF SOIL AND WATER CONSERVATION   (China)

^b NORTHWEST A F UNIVERSITY   (China)

^c SHAANXI UNIVERSITY OF CHINESE MEDICINE   (China)

^d Chongqing Environmental Protection Agency   (China)

Author keywords

Cytochrome P450 monooxygenase; Expression pattern; Prunella vulgaris; Rosmarinic acid; Rosmarinic acid synthase; Subcellular localisation

Indexed keywords

BIOCHEMISTRY; BIOLOGICAL MEMBRANES; BIOSYNTHESIS; CELL MEMBRANES; ENCODING (SYMBOLS); ENZYMES; POLYMERASE CHAIN REACTION;

EXPRESSION PATTERNS; MONOOXYGENASES; ROSMARINIC ACID; SUB-CELLULAR LOCALISATION; SYNTHASES; VULGARIS;

CLONING;

EID: 84994158742     PISSN: 01676857     EISSN: 15735044     Source Type: Journal    
DOI: 10.1007/s11240-016-1117-z     Document Type: Article

References (46)

1. Bassard J-E, Richert L, Geerinck J, Renault H, Duval F, Ullmann P, Schmitt M, Meyer E, Mutterer J, Boerjan W (2012) Protein–protein and protein–membrane associations in the lignin pathway. Plant Cell 24:4465–4482
2. Berger A, Meinhard J, Petersen M (2006) Rosmarinic acid synthase is a new member of the superfamily of BAHD acyltransferases. Planta 224:1503–1510
3. Bontpart T, Cheynier V, Ageorges A, Terrier N (2015) BAHD or SCPL acyltransferase? What a dilemma for acylation in the world of plant phenolic compounds. New Phytol 208:695–707
4. Boudet AM (2007) Evolution and current status of research in phenolic compounds. Phytochemistry 68:2722–2735
5. Costa RS, Carneiro TCB, Cerqueira-Lima AT, Queiroz NV, Alcantara-Neves NM, Pontes-de-Carvalho LC, Velozo ED, Oliveira EJ, Figueiredo CA (2012) Ocimum gratissimum Linn. and rosmarinic acid, attenuate eosinophilic airway inflammation in an experimental model of respiratory allergy to Blomia tropicalis. Int Immunopharmacol 13:126–134
6. D’Auria JC (2006) Acyltransferases in plants: a good time to be BAHD. Curr Opin Plant Biol 9:331–340
7. Di P, Zhang L, Chen JF, Tan HX, Xiao Y, Dong X, Zhou X, Chen WS (2013) C-13 tracer reveals phenolic acids biosynthesis in hairy root cultures of Salvia miltiorrhiza. ACS Chem Biol 8:1537–1548
8. Dubois M, Bailly F, Mbemba G, Mouscadet JF, Debyser Z, Witvrouw M, Cotelle P (2008) Reaction of rosmarinic acid with nitrite ions in acidic conditions: discovery of nitro- and dinitrorosmarinic acids as new anti-HIV-1 agents. J Med Chem 51:2575–2579
9. Eberle D, Ullmann P, Werck-Reichhart D, Petersen M (2009) cDNA cloning and functional characterisation of CYP98A14 and NADPH: cytochrome P450 reductase from Coleus blumei involved in rosmarinic acid biosynthesis. Plant Mol Biol 69:239–253
10. Ellis BE, Towers GH (1970) Biogenesis of rosmarinic acid in Mentha. Biochem J 118:291–297
11. Fazal H, Abbasi BH, Ahmad N, Ali M, Ali S (2016) Sucrose induced osmotic stress and photoperiod regimes enhanced the biomass and production of antioxidant secondary metabolites in shake-flask suspension cultures of Prunella vulgaris L. Plant Cell Tissue Organ Cult 124:573–581
12. Feng LA, Jia XB, Zhu MM, Chen Y, Shi F (2010) Antioxidant activities of total phenols of Prunella vulgaris L. in vitro and in tumor-bearing mice. Molecules 15:9145–9156
13. Gang DR, Beuerle T, Ullmann P, Werck-Reichhart D, Pichersky E (2002) Differential production of meta hydroxylated phenylpropanoids in sweet basil peltate glandular trichomes and leaves is controlled by the activities of specific acyltransferases and hydroxylases. Plant Physiol 130:1536–1544
14. Huang BB, Yi B, Duan YB, Sun LN, Yu XJ, Guo J, Chen WS (2008) Characterization and expression profiling of tyrosine aminotransferase gene from Salvia miltiorrhiza (Dan-shen) in rosmarinic acid biosynthesis pathway. Mol Biol Rep 35:601–612
15. Hucherig S, Petersen M (2013) RNAi suppression and overexpression studies of hydroxyphenylpyruvate reductase (HPPR) and rosmarinic acid synthase (RAS) genes related to rosmarinic acid biosynthesis in hairy root cultures of Coleus blumei. Plant Cell Tissue Organ Cult 113:375–385
16. Jiang JJ, Bi HP, Zhuang YB, Liu SW, Liu T, Ma YH (2016) Engineered synthesis of rosmarinic acid in Escherichia coli resulting production of a new intermediate, caffeoyl-phenyllactate. Biotechnol Lett 38:81–88
17. Jirovsky D, Kosina P, Myslinova M, Styskala J, Ulrichova J, Simanek V (2007) HPLC analysis of rosmarinic acid in feed enriched with aerial parts of Prunella vulgaris and its metabolites in pig plasma using dual-channel coulometric detection. J Agric Food Chem 55:7631–7637
18. Kim KH, Janiak V, Petersen M (2004) Purification, cloning and functional expression of hydroxyphenylpyruvate reductase involved in rosmarinic acid biosynthesis in cell cultures of Coleus blumei. Plant Mol Biol 54:311–323
19. Kim YB, Shin YJ, Tuan PA, Li X, Park Y, Park NI, Park SU (2014) Molecular cloning and characterization of genes involved in rosmarinic acid biosynthesis from Prunella vulgaris. Biol Pharm Bull 37:1221–1227
20. Kim GD, Park YS, Jin YH, Park CS (2015) Production and applications of rosmarinic acid and structurally related compounds. Appl Microbiol Biotechnol 99:2083–2092
21. Landmann C, Hücherig S, Fink B, Hoffmann T, Dittlein D, Coiner HA, Schwab W (2011) Substrate promiscuity of a rosmarinic acid synthase from lavender (Lavandula angustifolia L.) Planta 234:305–320
22. Lee H, Lin JY (1988) Antimutagenic activity of extracts from anticancer drugs in Chinese medicine. Mutat Res 204:229–234
23. Luo J, Nishiyama Y, Fuell C, Taguchi G, Elliott K, Hill L, Tanaka Y, Kitayama M, Yamazaki M, Bailey P, Parr A, Michael AJ, Saito K, Martin C (2007) Convergent evolution in the BAHD family of acyl transferases: identification and characterization of anthocyanin acyl transferases from Arabidopsis thaliana. Plant J 50:678–695
24. Matsuno M, Nagatsu A, Ogihara Y, Ellis BE, Mizukami H (2002) CYP98A6 from Lithospermum erythrorhizon encodes 4-coumaroyl-4′-hydroxyphenyllactic acid 3-hydroxylase involved in rosmarinic acid biosynthesis. FEBS Lett 514:219–224
25. National Pharmacopoeia Committee (2015) Chinese pharmacopoeia. Chemical Industry Press, Beijing
26. Nelson B, Cai X, Nebenfuhr A (2007) A multicolored set of in vivo organelle markers for co-ocalization studies in Arabidopsis and other plants. Plant J 51:1126–1136
27. Petersen M (2013) Rosmarinic acid: new aspects. Phytochem Rev 12:207–227
28. Petersen M, Hausler E, Meinhard J, Karwatzki B, Gertlowski C (1994) The biosynthesis of rosmarinic acid in suspension-cultures of Coleus blumei. Plant Cell Tissue Organ Cult 38:171–179
29. Petersen M, Abdullah Y, Benner J, Eberle D, Gehlen K, Hucherig S, Janiak V, Kim KH, Sander M, Weitzel C, Wolters S (2009) Evolution of rosmarinic acid biosynthesis. Phytochemistry 70:1663–1679
30. Razzaque A, Ellis BE (1977) Rosmarinic acid production in Coleus cell cultures. Planta 137:287–291
31. Ru M, An Y, Wang K, Peng L, Li B, Bai Z, Wang B, Liang Z (2016) Prunella vulgaris L. hairy roots: culture, growth, and elicitation by ethephon and salicylic acid. Eng Life Sci 16:494–502
32. Sander M, Petersen M (2011) Distinct substrate specificities and unusual substrate flexibilities of two hydroxycinnamoyltransferases, rosmarinic acid synthase and hydroxycinnamoyl-CoA: shikimate hydroxycinnamoyl-transferase, from Coleus blumei Benth. Planta 233:1157–1171
33. Schoch G, Goepfert S, Morant M, Hehn A, Meyer D, Ullmann P, Werck-Reichhart D (2001) CYP98A3 from Arabidopsis thaliana is a 3′-hydroxylase of phenolic esters, a missing link in the phenylpropanoid pathway. J Biol Chem 276:36566–36574
34. Schuler MA (1996) Plant cytochrome P450 monooxygenases. Crit Rev Plant Sci 15:235–284
35. Song J, Wang ZZ (2009) Molecular cloning, expression and characterization of a phenylalanine ammonia-lyase gene (SmPAL1) from Salvia miltiorrhiza. Mol Biol Rep 36:939–952
36. Srivastava S, Conlan XA, Adholeya A, Cahill DM (2016) Elite hairy roots of Ocimum basilicum as a new source of rosmarinic acid and antioxidants. Plant Cell Tissue Organ Cult 126:19–32
37. Unno H, Ichimaida F, Suzuki H, Takahashi S, Tanaka Y, Saito A, Nishino T, Kusunoki M, Nakayama T (2007) Structural and mutational studies of anthocyanin malonyltransferases establish the features of BAHD enzyme catalysis. J Biol Chem 282:15812–15822
38. Villa-Ruano N, Pacheco-Hernandez Y, Lozoya-Gloria E, Castro-Juarez CJ, Mosso-Gonzalez C, Ramirez-Garcia SA (2015) Cytochrome P450 from plants: platforms for valuable phytopharmaceuticals. Trop J Pharm Res 14:731–742
39. Weitzel C, Petersen M (2010) Enzymes of phenylpropanoid metabolism in the important medicinal plant Melissa officinalis L. Planta 232:731–742
40. Weitzel C, Petersen M (2011) Cloning and characterisation of rosmarinic acid synthase from Melissa officinalis L. Phytochemistry 72:572–578
41. Yamamura Y, Ogihara Y, Mizukami H (2001) Cinnamic acid 4-hydroxylase from Lithospermum erythrorhizon: cDNA cloning and gene expression. Plant Cell Rep 20:655–662
42. Yoo S, Cho Y, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2:1565
43. Yu X-H, Chen M-H, Liu C-J (2008) Nucleocytoplasmic-localized acyltransferases catalyze the malonylation of 7-O-glycosidic (iso)flavones in Medicago truncatula. Plant J 55:382–396
44. Yu X-H, Gou J-Y, Liu C-J (2009) BAHD superfamily of acyl-CoA dependent acyltransferases in Populus and Arabidopsis: bioinformatics and gene expression. Plant Mol Biol 70:421–442
45. Zhang X, Ao ZJ, Bello A, Ran XZ, Liu SP, Wigle J, Kobinger G, Yao XJ (2016) Characterization of the inhibitory effect of an extract of Prunella vulgaris on Ebola virus glycoprotein (GP)-mediated virus entry and infection. Antiviral Res 127:20–31
46. Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23:283–333