Phenolic acid production is more effectively enhanced than tanshinone production by methyl jasmonate in Salvia miltiorrhiza hairy roots

Plant Cell, Tissue and Organ Culture

Volumn 134, Issue 1, 2018, Pages 119-129

  Xing, Bingcong ^a,b   Yang, Dongfeng ^c   Liu, Lin ^d   Han, Ruilian ^a,c   Sun, Yanfang ^c   Liang, Zongsuo ^a,b,c,d  

^a INSTITUTE OF SOIL AND WATER CONSERVATION   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c ZHEJIANG SCI TECH UNIVERSITY   (China)

^d NORTHWEST A F UNIVERSITY   (China)

Author keywords

Hairy roots; MeJA; Phenolic acids; Regulation; Salvia miltiorrhiza Bunge; Tanshinones

Indexed keywords

AMINO ACIDS; BIOCHEMISTRY; BIOSYNTHESIS;

HAIRY ROOTS; MEJA; PHENOLIC ACIDS; REGULATION; SALVIA MILTIORRHIZA BUNGE; TANSHINONES;

GENE EXPRESSION;

ACCUMULATION; AMINO ACIDS; BIOCHEMISTRY; BIOSYNTHESIS; CONTROL SYSTEMS; FOLDING ENDURANCE; PHENOLIC ACIDS; PRODUCTION;

EID: 85043691827     PISSN: 01676857     EISSN: 15735044     Source Type: Journal    
DOI: 10.1007/s11240-018-1405-x     Document Type: Article

References (50)

1. Bassolino L, Giacomelli E, Giovanelli S et al (2015) Tissue culture and aromatic profile in Salvia dolomitica Codd. Plant Cell Tiss Organ Cult 121:83–95. 10.1007/s11240-014-0681-3
2. Campos-Vargas R, Saltveit ME (2002) Involvement of putative chemical wound signals in the induction of phenolic metabolism in wounded lettuce. Physiol Plant 114(1):73–84. 10.1034/j.1399-3054.2002.1140111.x
3. Cheng H, Li X, Li X, Li Y, Wang L, Xue M (2012) Simultaneous quantification of selected compounds from Salvia herbs by HPLC method and their application. Food Chem 130(4):1031–1035. 10.1016/j.foodchem.2011.07.126
4. Cui G, Duan L, Jin B, Qian J, Xue Z, Shen G, Snyder JH, Song J, Chen S, Huang L, Peters RJ, Qi X (2015) Functional divergence of diterpene syntheses in the medicinal plant Salvia miltiorrhiza. Plant Physiol 169(3):1607–1618. 10.1104/pp.15.00695
5. Dai Z, Cui G, Zhou S-F, Zhang X, Huang L (2011) Cloning and characterization of a novel 3-hydroxy-3-methylglutaryl coenzyme A reductase gene from Salvia miltiorrhiza involved in diterpenoid tanshinone accumulation. J Plant Physiol 168(2):148–157. 10.1016/j.jplph.2010.06.008
6. Di P (2012) Exploring the biosynthesis pathway of phenolic acids and functional study of the involved genes. Dissertation, The Second Military Medical University
7. 13C tracer reveals phenolic acids biosynthesis in hairy root cultures of Salvia miltiorrhiza. ACS Chem Biol 8(7):1537–1548. 10.1021/cb3006962
8. Gao W, Hillwig ML, Huang L, Cui G, Wang X, Kong J, Yang B, Peters RJ (2009) A functional genomics approach to tanshinone biosynthesis provides stereochemical insights. Org Lett 11(22):5170–5173. 10.1021/ol902051v
9. Gao W, Sun HX, Xiao H, Cui G, Hillwig M, Jackson A, Wang X, Shen Y, Zhao N, Zhang L et al (2014) Combining metabolomics and transcriptomics to characterize tanshinone biosynthesis in Salvia miltiorrhiza. BMC Genom 15:73. 10.1186/1471-2164-15-73
10. Goossens J, Fernandez-Calvo P, Schweizer F, Goossens A (2016) Jasmonates: signal transduction components and their roles in environmental stress responses. Plant Mol Biol 91(6):673–689. 10.1007/s11103-016-0480-9
11. Gundlach H, Müller MJ, Kutchan TM, Zenk MH (1992) Jasmonic acid is a signal transducer in elicitor-induced plant cell cultures. Proc Natl Acad Sci 89(6):2389–2393. 10.1073/pnas.89.6.2389
12. Han M, Guo W, Liang Z, Yang D, Yan X, Zhu Y, Liu Y (2015) Effects of cerous nitrate on growth and tanshinone production in Salvia miltiorrhiza hairy roots. J Rare Earths 33(11):1228–1235. 10.1016/s1002-0721(14)60549-4
13. Hao X, Shi M, Cui L, Xu C, Zhang Y, Kai G (2015) Effects of methyl jasmonate and salicylic acid on tanshinone production and biosynthetic gene expression in transgenic Salvia miltiorrhiza hairy roots. Biotechnol Appl Biochem 62(1):24–31. 10.1002/bab.1236
14. Hua W, Song J, Li C, Wang Z (2012) Molecular cloning and characterization of the promoter of SmGGPPs and its expression pattern in Salvia miltiorrhiza. Mol Biol Rep 39(5):5775–5783. 10.1007/s11033-011-1388-8
15. Huang B, Duan Y, Yi B, Sun L, Lu B, Yu X, Sun H, Zhang H, Chen W (2008a) Characterization and expression profiling of cinnamate 4-hydroxylase gene from Salvia miltiorrhiza in rosmarinic acid biosynthesis pathway. Russ J Plant Physiol 55(3):390–399. 10.1134/s1021443708030163
16. Huang B, Yi B, Duan Y, Sun L, Yu X, Guo J, Chen W (2008b) Characterization and expression profiling of tyrosine aminotransferase gene from Salvia miltiorrhiza (Dan-shen) in rosmarinic acid biosynthesis pathway. Mol Biol Rep 35(4):601–612. 10.1007/s11033-007-9130-2
17. Jin X, Chen Z, Tan R, Zhao S, Hu Z (2012) Isolation and functional analysis of 4-coumarate: coenzyme A ligase gene promoters from Salvia miltiorrhiza. Biol Plant 56(2):261–268. 10.1007/s10535-012-0085-3
18. 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(3):319–327. 10.1016/j.ymben.2011.02.003
19. Lee EJ, Park SY, Paek KY (2015) Enhancement strategies of bioactive compound production in adventitious root cultures of Eleutherococcus koreanum Nakai subjected to methyl jasmonate and salicylic acid elicitation through airlift bioreactors. Plant Cell Tiss Organ Cult 120:1–10. 10.1007/s11240-014-0567-4
20. Li X, Guo H, Qi Y et al (2016) Salicylic acid-induced cytosolic acidification increases the accumulation of phenolic acids in Salvia miltiorrhiza cells. Plant Cell Tiss Organ Cult 126:333–341. 10.1007/s11240-016-1001-x
21. Liang Z, Yang D, Liang X, Zhang Y, Liu Y, Liu F (2012) Roles of reactive oxygen species in methyl jasmonate and nitric oxide-induced tanshinone production in Salvia miltiorrhiza hairy roots. Plant Cell Rep 31(5):873–883. 10.1007/s00299-011-1208-6
22. Liu A, Li L, Xu M, Lin Y, Guo H, Guo D (2006) Simultaneous quantification of six major phenolic acids in the roots of Salvia miltiorrhiza and four related traditional Chinese medicinal preparations by HPLC–DAD method. J Pharm Biomed Anal 41(1):48–56. 10.1016/j.jpba.2005.10.021
23. Liu H, Wang X, Wang D, Zou Z, Liang Z (2011) Effect of drought stress on growth and accumulation of active constituents in Salvia miltiorrhiza Bunge. Ind Crops Prod 33(1):84–88. 10.1016/j.indcrop.2010.09.006
24. Liu L, Yang D, Liang T, Zhang H, He Z, Liang Z (2016) Phosphate starvation promoted the accumulation of phenolic acids by inducing the key enzyme genes in Salvia miltiorrhiza hairy roots. Plant Cell Rep 35(9):1933–1942. 10.1007/s00299-016-2007-x
25. Ma X, Ma Y, Tang J, He Y, Liu Y, Ma X, Shen Y, Cui G, Lin H, Rong Q, Guo J, Huang L (2015) The biosynthetic pathways of tanshinones and phenolic acids in Salvia miltiorrhiza. Molecules 20(9):16235–16254. 10.3390/molecules200916235
26. Min S, Luo X, Ju G, Li L, Huang S, Tong Z, Wang H, Kai G (2016) Enhanced diterpene tanshinone accumulation and bioactivity of transgenic Salvia miltiorrhiza hairy roots by pathway engineering. J Agric Food Chem 64(12):2523–2530. 10.1021/acs.jafc.5b04697
27. Pilaisangsuree V, Somboon T, Tonglairoum P et al (2018) Enhancement of stilbene compounds and anti-inflammatory activity of methyl jasmonate and cyclodextrin elicited peanut hairy root culture. Plant Cell Tiss Organ Cult 132:165–179. 10.1007/s11240-017-1321-5
28. Shi Z, He J, Yao T, Chang W, Zhao M (2005) Simultaneous determination of cryptotanshinone, tanshinone I and tanshinone IIA in traditional Chinese medicinal preparations containing Radix salvia miltiorrhiza by HPLC. J Pharm Biomed Anal 37(3):481–486. 10.1016/j.jpba.2004.11.015
29. Song J, Wang Z (2009) Molecular cloning, expression and characterization of a phenylalanine ammonia-lyase gene (SmPAL1) from Salvia miltiorrhiza. Mol Biol Rep 36(5):939–952. 10.1007/s11033-008-9266-8
30. Song J, Wang Z (2011) RNAi-mediated suppression of the phenylalanine ammonia-lyase gene in Salvia miltiorrhiza causes abnormal phenotypes and a reduction in rosmarinic acid biosynthesis. J Plant Res 124(1):183–192. 10.1007/s10265-010-0350-5
31. Vaccaro M, Malafronte N, Alfieri M et al (2014) Enhanced biosynthesis of bioactive abietane diterpenes by overexpressing AtDXS or AtDXR genes in Salvia sclarea hairy roots. Plant Cell Tiss Organ Cult 119:65–77. 10.1007/s11240-014-0514-4
32. Wang B, Sun W, Li Q, Li Y, Luo H, Song J, Sun C, Qian J, Zhu Y, Hayward A, Xu H, Chen S (2015a) Genome-wide identification of phenolic acid biosynthetic genes in Salvia miltiorrhiza. Planta 241(3):711–725. 10.1007/s00425-014-2212-1
33. Wang D, Zhang W, Wang T, Li N, Mu H, Zhang J, Duan J (2015b) Unveiling the mode of action of two antibacterial tanshinone derivatives. Int J Mol Sci 16(8):17668–17681. 10.3390/ijms160817668
34. 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):1–9. 10.1111/j.1399-3054.2009.01257.x
35. Xiao Y, Zhang L, Gao S, Saechao S, Di P, Chen J, Chen W (2010) The c4h, tat, hppr and hppd genes prompted engineering of rosmarinic acid biosynthetic pathway in Salvia miltiorrhiza hairy root cultures. PLoS ONE 6(12):e29713. 10.1371/journal.pone.0029713
36. + as a more effective elicitor for production of tanshinones than phenolic acids in Salvia miltiorrhiza hairy roots. Molecules 20(1):309–324. 10.3390/molecules20010309
37. Yan Q, Shi M, Ng J, Wu J (2006) Elicitor-induced rosmarinic acid accumulation and secondary metabolism enzyme activities in Salvia miltiorrhiza hairy roots. Plant Sci 170(4):853–858. 10.1016/j.plantsci.2005.12.004
38. Yan X, Zhang L, Wang J, Liao P, Zhang Y, Zhang R, Kai G (2009) Molecular characterization and expression of 1-deoxy-d-xylulose 5-phosphate reductoisomerase (DXR) gene from Salvia miltiorrhiza. Acta Physiol Plant 31(5):1015–1022. 10.1007/s11738-009-0320-5
39. Yang D, Du X, Liang X, Han R, Liang Z, Liu Y, Liu F, Zhao J (2012a) Different roles of the mevalonate and methylerythritol phosphate pathways in cell growth and tanshinone production of Salvia miltiorrhiza hairy roots. PLoS ONE 7(11):e46797. 10.1371/journal.pone.0046797
40. Yang D, Ma P, Liang X, Wei Z, Liang Z, Liu Y, Liu F (2012b) PEG and ABA trigger methyl jasmonate accumulation to induce the MEP pathway and increase tanshinone production in Salvia miltiorrhiza hairy roots. Physiol Plant 146(2):173–183. 10.1111/j.1399-3054.2012.01603.x
41. Yang D, Huang Z, Xing B, Jin W, Yan X, Guo Z, Liang Z (2016) Regulation of folic acid on phenolic acids production in Salvia miltiorrhiza hairy roots. Plant Cell Tissue Organ Cult 127(1):175–185. 10.1007/s11240-016-1040-3
42. Yi B (2007) Molecular cloning and regulation analysis of important genes involved in tyrosine-branch pathway of rosmarinic acid metabolism from Salvia miltiorrhiza Bunge. Dissertation, The Second Military Medical University
43. Yu H, Liu X, Gao S, Han X, Cheng A, Lou H (2014) Molecular cloning and functional characterization of a phenylalanine ammonia-lyase from liverwort Plagiochasma appendiculatum. Plant Cell Tissue Organ Cult 117(2):265–277. 10.1007/s11240-014-0438-z
44. Zhang L, Yan X, Wang J, Li S, Liao P, Kai G (2011) Molecular cloning and expression analysis of a new putative gene encoding 3-hydroxy-3-methylglutaryl-CoA synthase from Salvia miltiorrhiza. Acta Physiol Plant 33(3):953–961. 10.1007/s11738-010-0627-2
45. Zhang Y, Jiang P, Ye M, Kim SH, Jiang C, Lu J (2012) Tanshinones: sources, pharmacokinetics and anti-cancer activities. Int J Mol Sci 13(10):13621–13666. 10.3390/ijms131013621
46. Zhang S, Yan Y, Wang B, Liang Z, Liu Y, Liu F, Qi Z (2014) Selective responses of enzymes in the two parallel pathways of rosmarinic acid biosynthetic pathway to elicitors in Salvia miltiorrhiza hairy root cultures. J Biosci Bioeng 117(5):645–651. 10.1016/j.jbiosc.2013.10.013
47. Zhao J, Zhou L, Wu J (2010) Effects of biotic and abiotic elicitors on cell growth and tanshinone accumulation in Salvia miltiorrhiza cell cultures. Appl Microbiol Biotechnol 87(1):137–144. 10.1007/s00253-010-2443-4
48. Zhao J, Lou J, Mou Y, Li P, Wu J, Zhou L (2011) Diterpenoid tanshinones and phenolic acids from cultured hairy roots of Salvia miltiorrhiza Bunge and their antimicrobial activities. Molecules 16(3):2259–2267. 10.3390/molecules16032259
49. Zhou Y, Li W, Xu L, Chen L (2011) In Salvia miltiorrhiza, phenolic acids possess protective properties against amyloid beta-induced cytotoxicity, and tanshinones act as acetylcholinesterase inhibitors. Environ Toxicol Pharmacol 31(3):443–452. 10.1016/j.etap.2011.02.006
50. Zhou X, Chan S, Tseng H, Deng Y, Hoi P, Choi P, Or P, Yang J, Lam F, Lee S, Leung G, Kong S, Ho H, Kwan Y, Yeung J (2012) Danshensu is the major marker for the antioxidant and vasorelaxation effects of Danshen (Salvia miltiorrhiza) water-extracts produced by different heat water-extractions. Phytomedicine 19(14):1263–1269. 10.1016/j.phymed.2012.08.011