Skip to main content

Advertisement

SpringerLink
Log in

AtMYB11 regulates caffeoylquinic acid and flavonol synthesis in tomato and tobacco

  • Original Paper
  • Published:
Plant Cell, Tissue and Organ Culture (PCTOC) Aims and scope Submit manuscript

Abstract

Interest in so-called functional foods, i.e., foods that promote health and disease prevention, is increasing. Consumption of plant polyphenols has been implicated in the prevention of age-related diseases, cardiovascular disease and cancer. AtMYB12 and AtMYB111, which were originally identified as flavonol-specific transcriptional activator in Arabidopsis thaliana, induces the accumulation of high levels of polyphenols in tobacco and tomato plants. In this study, we determined that the transcription factor AtMYB11 as its close homologs, AtMYB12 and AtMYB111, regulate flavonoid and caffeoylquinic acid biosynthesis in tomato and tobacco plants. Constitutive expression of AtMYB11 enhanced the expression of genes in the phenylpropanoid biosynthesis pathway, resulting in the accumulation of flavonoids and chlorogenic acid in tobacco and tomato plants. Increases in dicaffeoylquinic acid and tricaffeoylquinic acid content were only detected in AtMYB11-expressing tomato fruits. These results suggest the potential of transgenic tomatoes with improved antioxidant properties as functional foods.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

PAL:

Phenylalanine ammonium lyase

C4H:

Cinnamate 4-hydroxylase

CHI:

Chalcone isomerase

CHS:

Chalcone synthase

4CL:

4-Hydroxy-cinnamoyl CoA ligase

F3H:

Flavanone-3-hydroxylase

F3′H:

Flavonoid-3′-hydroxylase

FLS:

Flavonol synthase

GT:

Flavonol-3-glucosyltransferase

HPLC:

High-performance liquid chromatography

HCT:

Hydroxycinnamoyl transferase

HQT:

Hydroxycinnamoyl CoA quinate transferase

C3H:

p-Coumaroyl ester 3-hydroxylase

CGA:

Chlorogenic acid

diCQA:

Dicaffeoylquinic acid

tiCQA:

Tricaffeoylquinic acid

CQA:

Caffeoyl quinic acid

References

  • Ackland ML, van de Waarsengurg S, Jones R (2005) Synergistic antiproliferative action of the flavonols quercetin and kaempferol in cultured human cancer cell lines. In Vivo 19:69–76

    CAS  PubMed  Google Scholar 

  • Andersson KB, Berge T, Matre V, Gabrielsen OS (1999) Sequence selectivity of c-Myb in vivo resolution of a DNA target specificity paradox. J Biol Chem 274:21986–21994

    Article  CAS  PubMed  Google Scholar 

  • Arima H, Ashida H, Gi Danno (2002) Rutin-enhanced antibacterial activities of flavonoids against Bacillus cereus and Salmonella enteritidis. Biosci Biotechnol Biochem 66:1009–1014

    Article  CAS  PubMed  Google Scholar 

  • Borevitz JO, Xia Y, Blount J, Dixon RA, Lamb C (2000) Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12:2383–2393

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Brouillard R, George F, Fougerousse A (1997) Polyphenols produced during red wine ageing. Biofactors 6:403–410

    Article  CAS  PubMed  Google Scholar 

  • Chen F, Srinivasa Reddy MS, Temple S, Jackson L, Shadle G, Dixon RA (2006) Multi-site genetic modulation of monolignol biosynthesis suggests new routes for formation of syringyl lignin and wall-bound ferulic acid in alfalfa (Medicago sativa L.). Plant J 48:113–124

    Article  CAS  PubMed  Google Scholar 

  • Choi J, Park JK, Lee KT, Park KK, Kim WB, Lee JH, Jung HJ, Park HJ (2005) In vivo antihepatotoxic effects of Ligularia fischeri var. spiciformis and the identification of the active component, 3, 4-dicaffeoylquinic acid. J Med Food 8:348–352

    Article  CAS  PubMed  Google Scholar 

  • Christina E, Maddox Lisa M, Laur Li Tian (2009) Antibacterial Activity of Phenolic Compounds Against the Phytopathogen Xylella fastidiosa. Curr Microbiol 60:53–58

    Google Scholar 

  • Deikman J, Kline R, Fischer RL (1992) Organization of ripening and ethylene regulatory regions in a fruit-specific promoter from tomato (Lycopersicon esculentum). Plant Physiol 100:2013–2017

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Du H, Zhang L, Liu L, Tang XF, Yang WJ, Wu YM, Huang YB, Tang YX (2009) Biochemical and molecular characterization of plant MYB transcription factor family. Biochemistry (Moscow) 74:1–11

    Article  CAS  Google Scholar 

  • Elkind Y, Edwards R, Mavandad M, Hedrick SA, Ribak O, Dixon RA, Lamb CJ (1990) Abnormal plant development and down-regulation of phenylpropanoid biosynthesis in transgenic tobacco containing a heterologous phenylalanine ammonialyase gene. Proc Natl Acad Sci USA 87:9057–9061

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Escamilla-Trevino LL, Shen H, Hernandez T, Yin Y, Xu Y, Dixon RA (2014) Early lignin pathway enzymes and routes in switch grass (Panicum virgatum L.). Plant Mol Biol 84:565–576

    Article  CAS  PubMed  Google Scholar 

  • Fillatti JJ, Kiser J, Rose R, Comai L (1987) Efficient transfer of a glyphosate tolerance gene into tomato using a binary Agrobacterium tumefaciens vector. Nat Biotechnol 5:726–730

    Article  CAS  Google Scholar 

  • Franke R, Humphreys JM, Hemm MR, Denault JW, Ruegger MO, Cusumano JC, Chapple C (2002) The Arabidopsis REF8 gene encodes the 3-hydroxylase of phenylpropanoid metabolism. Plant J 30:33–45

    Article  CAS  PubMed  Google Scholar 

  • Guerineau F, Mullineaux P (1993) Plant transformation and expression vectors. In: Croy RR (ed) Plant Molecular Biology LABFAX. Bios Scientific Publishers, Oxford, pp 121–147

    Chapter  Google Scholar 

  • Hannum SM (2004) Potential impact of strawberries on human health: a review of the science. Crit Rev Food Sci Nutr 44:1–17

    Article  CAS  PubMed  Google Scholar 

  • Hertog MG, Feskens EJ, Kromhout D, Hollman P, Katan M (1993) Dietary antioxidant flavonoids and risk of coronary heart disease: the zutphen elderly study. Lancet 342:1007–1011

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann L, Maury S, Martz F, Geoffroy P, Legrand M (2003) Purification, cloning, and properties of an acyltransferase controlling shikimate and quinate ester intermediates in phenylpropanoid metabolism. J Biol Chem 278:95–103

    Article  CAS  PubMed  Google Scholar 

  • Hou DX, Fujii M, Terahara N, Yoshimoto M (2004) Molecular mechanisms behind the chemopreventive effects of anthocyanidins. J Biomed Biotechnol 2004:321–325

    Article  PubMed Central  PubMed  Google Scholar 

  • Howles PA, Sewalt VJ, Paiva NL, Elkind Y, Bate NJ, Lamb C, Dixon RA (1996) Overexpression of l-phenylalanine ammonia-lyase in transgenic tobacco plants reveals control points for flux into phenylpropanoid biosynthesis. Plant Physiol 112:1617–1624

    CAS  PubMed Central  PubMed  Google Scholar 

  • Islam S (2006) Sweetpotato (Ipomoea batatas L.) leaf: its potential effect on human health and nutrition. J Food Sci 71:R13–R121

    Article  CAS  Google Scholar 

  • Jia L, Clegg MT, Jiang T (2004) Evolutionary dynamics of the DNA-binding domains in putative R2R3-MYB genes identified from rice subspecies indica and japonica genomes. Plant Physiol 134:575–585

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Johnson G, Schaal LA (1952) Relation of chlorogenic acid to scab resistance in potatoes. Science 115:627–629

    Article  CAS  PubMed  Google Scholar 

  • Joseph JA, Shukitt-Hale B, Denisova NA, Bielinski D, Martin A, McEwen JJ, Bickford PC (1999) Reversals of age-related declines in neuronal signal transduction, cognitive, and motor behavioral deficits with blueberry, spinach, or strawberry dietary supplementation. J Neurosci 19:8114–8121

    CAS  PubMed  Google Scholar 

  • La Casa C, Villegas I, Alarcon de La Lastra C, Motilva V, Martın Calero M (2000) Evidence for protective and antioxidant properties of rutin, a natural flavone, against ethanol induced gastric lesions. J Ethnopharmacol 71:45–53

    Article  PubMed  Google Scholar 

  • Li N, Kong L, Zhou W, Zhang X, Wei S, Ding X, Chu Z (2013) Overexpression of Os2H16 enhances resistance to phytopathogens and tolerance to drought stress in rice. Plant Cell Tissue Organ Cult 115:429–441

    Article  CAS  Google Scholar 

  • Lipsick JS (1996) One billion years of Myb. Oncogene 13:223–235

    CAS  PubMed  Google Scholar 

  • Lister CE, Lancaster JE, Walker JR (1996) Phenylalanine ammonia-lyase (PAL) activity and its relationship to anthocyanin and flavonoid levels in New Zealand-grown apple cultivars. J Am Soc Hortic Sci 121:281–285

    CAS  Google Scholar 

  • Luo J, Nishiyama Y, Fuell C, Taguchi G, Elliott K, Hill L, Tanaka Y, Kitayama M, Yanazaki 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

    Article  CAS  PubMed  Google Scholar 

  • Luo J, Butelli E, Hill L, Parr A, Niggeweg R, Bailey P, Weisshaar B, Martin C (2008) AtMYB12 regulates caffeoyl quinic acid and flavonol synthesis in tomato: expression in fruit results in very high levels of both types of polyphenol. Plant J 56:316–326

    Article  CAS  PubMed  Google Scholar 

  • Martin C, Butelli E, Petroni K, Tonelli C (2011) How can research on plants contribute to promoting human health. Plant Cell 23:1685–1699

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mehrtens F, Kranz H, Bednarek P, Weisshaar B (2005) The Arabidopsis transcription factor MYB12 is a flavonol-specific regulator of phenylpropanoid biosynthesis. Plant Physiol 138:1083–1096

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Misra P, Pandey A, Tiwari M, Chandrashekar K, Sidhu OP, Asif MH, Chakarabarty D, Singh PK, Trivedi PK, Nath P, Tuli R (2010) Modulation of transcriptome and metabolome of tobacco by Arabidopsis transcription factor, AtMYB12, leads to insect resistance. Plant Physiol 152:2258–2268

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Moco S, Bino RJ, Vorst O, Verhoeven HA, de Groot J, van Beek TA, Vervoort J, de Vos CH (2006) A liquid chromatography-mass spectrometry-based metabolome database for tomato. Plant Physiol 141:1205–1218

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Moores R, McDermott DL, Wood T (1948) Determination of chlorogenic acid in coffee. Anal Chem 20:620–624

    Article  CAS  Google Scholar 

  • Nakajima Y, Shimazawa M, Mishima S, Hara H (2007) Water extract of propolis and its main constituents, caffeoylquinic acid derivatives, exert neuroprotective effects via antioxidant actions. Life Sci 80:370–377

    Article  CAS  PubMed  Google Scholar 

  • Niggeweg R, Michael AJ, Martin C (2004) Engineering plants with increased levels of the antioxidant chlorogenic acid. Nat Biotechnol 22:746–754

    Article  CAS  PubMed  Google Scholar 

  • Pandey A, Misra P, Chandrashekar K, Trivedi PK (2012) Development of AtMYB12-expressing transgenic tobacco callus culture for production of rutin with biopesticidal potential. Plant Cell Report 31:1867–1876

    Article  CAS  Google Scholar 

  • Pandey A, Misra P, Bhambhani S, Bhatia C, Trivedi PK (2014a) Expression of Arabidopsis MYB transcription factor, AtMYB111, in tobacco requires light to modulate flavonol content. Sci Rep 4:5018

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pandey A, Misra P, Khan MP, Swarnkar G, Tewari MC, Bhambhani S, Trivedi R, Chattopadhyay N, Trivedi PK (2014b) Co-expression of Arabidopsis transcription factor, AtMYB12, and soybean isoflavone synthase, GmIFS1, genes in tobacco leads to enhanced biosynthesis of isoflavones and flavonols resulting in osteoprotective activity. Plant Biotechnol J 12:69–80

    Article  CAS  PubMed  Google Scholar 

  • Park JS, Rho HS, Kim DH, Chang IS (2006) Enzymatic preparation of kaempferol from green tea seed and its antioxidant activity. J Agric Food Chem 54:2951–2956

    Article  CAS  PubMed  Google Scholar 

  • Pellegrini N, Re R, Yang M, Rice-Evans P (1999) Screening of dietary carotenoids and carotenoid-rich fruit extracts for anti-oxidant activities applying the 2,2′-azinobis (3-ethylenebenzo-thiazoline-6-sulfonic) acid radical cation decolorization assay. Methods Enzymol 299:379–389

    Article  CAS  Google Scholar 

  • Sawa T, Nakao M, Akaike T, Ono K, Maeda H (1999) Alkylperoxyl radical-scavenging activity of various flavonoids and other phenolic compounds: implications for the anti-tumor-promoter effect of vegetables. J Agric Food Chem 47:397–402

    Article  CAS  PubMed  Google Scholar 

  • Schoch G, Goepfert S, Morant M, Hehn A, Meyer D, UIImann 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

    Article  CAS  PubMed  Google Scholar 

  • Soobrattee MA, Bahorun T, Aruoma OI (2006) Chemopreventive actions of polyphenolic compounds in cancer. Biofactors 27:19–35

    Article  CAS  PubMed  Google Scholar 

  • Stracke R, Ishihara H, Huep G, Barsch A, Mehrtens F, Niehaus K, Weisshaar B (2007) Differential regulation of closely related R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis thaliana seedling. Plant J 50:660–677

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stracke R, Jahns O, Keck M, Tohge T, Niehaus K, Fernie AR, Weisshaar B (2010) Analysis of production of flavonol glycosides-dependent flavonol glycoside accumulation in Arabidopsis thaliana plants reveals MYB11-, MYB12-and MYB111-independent flavonol glycoside accumulation. New Phytol 188:985–1000

    Article  CAS  PubMed  Google Scholar 

  • Taguri T, Tanaka T, Kouno I (2006) Antibacterial spectrum of plant polyphenols and extracts depending upon hydroxyphenyl structure. Biol Pharm Bull 29:2226–2235

    Article  CAS  PubMed  Google Scholar 

  • Tamura H, Akioka T, Ueno K, Chujyo T, Ki Okazaki, King PJ, Robinson WE Jr (2006) Anti-human immunodeficiency virus activity of 3, 4, 5-tricaffeoylquinic acid in cultured cells of lettuce leaves. Mol Nutr Food Res 50:396–400

    Article  CAS  PubMed  Google Scholar 

  • Treutter D (2005) Significance of flavonoids in plant resistance and enhancement of their biosynthesis. Plant Biol 7:581–591

    Article  CAS  PubMed  Google Scholar 

  • Villegas RJ, Kojima M (1986) Purification and characterization of hydroxycinnamoyl d-glucose: quinate hydroxycinnamoyl trans -ferase in the root of sweet potato, Ipomoea batatas Lam. J Biol Chem 261:8729–8733

    CAS  PubMed  Google Scholar 

  • Williamson G, Day A, Plumb G, Couteau D (2000) Human metabolic pathways of dietary flavonoids and cinnamates. Biochem Soc Trans 28:16–21

    CAS  PubMed  Google Scholar 

  • Zuo J, Niu QW, Simon GM, Chua NH (2001) Chemical-regulated, site-specific DNA excision in transgenic plants. Nat Biotechnol 19:157–161

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by Ph.D. Programs Foundation of Ministry of Education of China (Grant No. 20123702110014), Foundation for the Author of National Excellent Doctoral Dissertation of PR China (Grant No. 201132), Promotive research fund for excellent young and middle-aged scientists of Shandong Province (BS2012SW014), the National High Technology Research and Development Program of China (2010AA10Z103) and the Taishan Scholar of Shandong Province.

Conflict of interest

The authors declare no competing financial interest.

Author information

Authors and Affiliations

  1. State Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory of Agricultural Microbiology, Shandong Agricultural University, Tai’an, 271018, Shandong, People’s Republic of China

    Yang Li, Ming Chen, Shaoli Wang, Xinhua Ding & Zhaohui Chu

  2. Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI, 48824, USA

    Jing Ning

Authors
  1. Yang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ming Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shaoli Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jing Ning
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xinhua Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zhaohui Chu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Xinhua Ding or Zhaohui Chu.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, Y., Chen, M., Wang, S. et al. AtMYB11 regulates caffeoylquinic acid and flavonol synthesis in tomato and tobacco. Plant Cell Tiss Organ Cult 122, 309–319 (2015). https://doi.org/10.1007/s11240-015-0767-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-015-0767-6

Keywords

Search

Navigation