Nothing Special   »   [go: up one dir, main page]
Skip to main content
Springer Nature Link
Log in

Differential combinatorial interactions of cis-acting elements recognized by R2R3-MYB, BZIP, and BHLH factors control light-responsive and tissue-specific activation of phenylpropanoid biosynthesis genes

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Chalcone synthase (CHS), chalcone flavanone isomerase (CFI), flavanone 3-hydroxylase (F3H) and flavonol synthase (FLS) catalyze successive steps in the biosynthetic pathway leading to the production of flavonols. We show that in Arabidopsis thaliana all four corresponding genes are coordinately expressed in response to light, and are spatially coexpressed in siliques, flowers and leaves. Light regulatory units (LRUs) sufficient for light responsiveness were identified in all four promoters. Each unit consists of two necessary elements, namely a MYB-recognition element (MRE) and an ACGT-containing element (ACE). C1 and Sn, a R2R3-MYB and a BHLH factor, respectively, known to control tissue specific anthocyanin biosynthesis in Z. mays, were together able to activate the AtCHS promoter. This activation of the CHS promoter required an intact MRE and a newly identified sequence designated R response element (RRE AtCHS) containing the BHLH factor consensus binding site CANNTG. The RRE was dispensable for light responsiveness, and the ACE was not necessary for activation by C1/Sn. These data suggest that a BHLH and a R2R3-MYB factor cooperate in directing tissue-specific production of flavonoids, while an ACE-binding factor, potentially a BZIP, and a R2R3-MYB factor work together in conferring light responsiveness.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

ACE:

ACGT-containing element

ACS:

ACE-like sequence

BHLH:

basic helix-loop-helix

BZIP:

basic region/leucine zipper

CFI:

chalcone flavanone isomerase

CHS:

chalcone synthase

chx:

cycloheximide

EMSA:

electrophoretic mobility shift assay

F3H:

flavanone 3-hydroxylase

FLS:

flavonol synthase

LRU:

light regulatory unit

MRE:

MYB-recognition element

MRS:

MRE-like sequence

RRE:

R response element

References

  • G.A. Armstrong B. Weisshaar K. Hahlbrock (1992) ArticleTitleHomodimeric and heterodimeric leucine zipper proteins and nuclear factors from parsley recognize diverse promoter elements with ACGT cores Plant Cell 4 525–537

    Google Scholar 

  • A. Batschauer P.M. Gilmartin F. Nagy E. Schäfer (1994) The molecular biology of photoregulated genes R.E. Kendrick G.H.M. Kronenberg (Eds) Photomorphogenesis in Plants. EditionNumber2 Kluwer Academic Publishers Dordrecht The Netherlands 559–599

    Google Scholar 

  • T.K. Blackwell H. Weintraub (1990) ArticleTitleDifferences and similarities in DNA-binding preferences of MyoD and E2A protein complexes revealed by binding site selection Science 250 1104–1110 Occurrence Handle1:CAS:528:DyaK3MXls1yqsg%3D%3D Occurrence Handle2174572

    CAS  PubMed  Google Scholar 

  • A. Block J.L. Dangl K. Hahlbrock P. Schulze-Lefert (1990) ArticleTitleFunctional borders, genetic fine structure, and distance requirements of cis elements mediating light responsiveness of the parsley chalcone synthase promoter Proc. Natl. Acad. Sci. USA 87 5387–5391

    Google Scholar 

  • J.P. Bodeau V. Walbot (1996) ArticleTitleStructure and regulation of the maize Bronze2 promoter Plant Mol. Biol. 32 599–609

    Google Scholar 

  • U. Brinkmann R.E. Martes P. Buckel (1989) ArticleTitleHigh-level expression of recombinant genes in Escherichia coli is dependent on the availability of the dnaY gene product Gene 85 109–114 Occurrence Handle10.1016/0378-1119(89)90470-8 Occurrence Handle2515992

    Article  PubMed  Google Scholar 

  • C.S. Buer G.K. Muday (2004) ArticleTitleThetransparent testa4 mutation prevents flavonoid synthesis and alters auxin transport and the response of Arabidopsis roots to gravity and light Plant Cell 16 1191–1205

    Google Scholar 

  • J. Chappell K. Hahlbrock (1984) ArticleTitleTranscription of plant defense genes in response to UV light or fungal elicitor Nature 311 76–78

    Google Scholar 

  • J.M. Christie G.I. Jenkins (1996) ArticleTitleDistinct UV-B and UV-A/blue light signal transduction pathways induce chalcone synthase gene expression in Arabidopsis cells Plant Cell 8 1555–1567

    Google Scholar 

  • J.L. Dangl K.-D. Hauffe S. Lipphardt K. Hahlbrock D. Scheel (1987) ArticleTitleParsley protoplasts retain differential responsiveness to UV light and fungal elicitor EMBO J 6 2551–2556 Occurrence Handle1:CAS:528:DyaL2sXlslWmtr8%3D

    CAS  Google Scholar 

  • C. Douglas H. Hoffmann W. Schulz K. Hahlbrock (1987) ArticleTitleStructure and elicitor or U.V.-light-stimulated expression of two 4-coumarate:CoA ligase genes in parsley EMBO J 6 1189–1195

    Google Scholar 

  • W. Dröge-Laser A. Kaiser W.P. Lindsay B.A. Halkier G.J. Loake P. Doerner R.A. Dixon C. Lamb (1997) ArticleTitleRapid stimulation of a soybean protein-serine kinase that phosphorylates a novel bZIP DNA-binding protein, G/HBF-1, during the induction of early transcription-dependent defenses EMBO J 16 726–738

    Google Scholar 

  • O. Faktor J.M. Kooter G.J. Loake R.A. Dixon C.J. Lamb (1997) ArticleTitleDifferential utilization of regulatory cis-elements for stress-induced and tissue-specific activity of a French bean chalcone synthase promoter Plant Sci. 124 175–182

    Google Scholar 

  • O. Faktor G. Loake R.A. Dixon C.J. Lamb (1997) ArticleTitleThe G-box and H-box in a 39 bp region of a French bean chalcone synthase promoter constitute a tissue-specific regulatory element Plant J 11 1105–1113

    Google Scholar 

  • R.L. Feinbaum F.M. Ausubel (1988) ArticleTitleTranscriptional regulation of the Arabidopsis thaliana chalcone synthase gene Mol. Cell. Biol. 8 1985–1992

    Google Scholar 

  • R.L. Feinbaum G. Storz F.M. Ausubel (1991) ArticleTitleHigh intesity and blue light regulated expression of chimeric chalcone synthase genes in transgenic Arabidopsis thaliana plants Molecular General Genetics 226 449–456

    Google Scholar 

  • M. Feldbrügge M. Sprenger M. Dinkelbach K. Yazaki K. Harter B. Weisshaar (1994) ArticleTitleFunctional analysis of a light-responsive plant bZIP transcriptional regulator Plant Cell 6 1607–1621

    Google Scholar 

  • M. Feldbrügge M. Sprenger K. Hahlbrock B. Weisshaar (1997) ArticleTitlePcMYB1, a novel plant protein containing a DNA-binding domain with one MYB repeat, interacts in vivo with a light-regulatory promoter unit Plant J 11 1079–1093 Occurrence Handle10.1046/j.1365-313X.1997.11051079.x Occurrence Handle1:STN:280:ByiA3snjtVU%3D Occurrence Handle9193077

    Article  CAS  PubMed  Google Scholar 

  • G. Forkmann S. Martens (2001) ArticleTitleMetabolic engineering and applications of flavonoids Curr. Opin. Biotech. 12 155–160

    Google Scholar 

  • R. Foster T. Izawa N.-H. Chua (1994) ArticleTitlePlant bZIP proteins gather at ACGT elements FASEB J 8 192–200 Occurrence Handle1:CAS:528:DyaK2cXitlOisLw%3D Occurrence Handle8119490

    CAS  PubMed  Google Scholar 

  • M.A. Frohman M.K. Dush G.R. Martin (1988) ArticleTitleRapid production of full-length cDNAs from rare transcripts: Amplification using a single gene-specific oligonucleotide primer Proc. Natl. Acad. Sci. USA 85 8998–9002

    Google Scholar 

  • P.J. Green S.A. Kay N.-H. Chua (1987) ArticleTitleSequence-specific interactions of a pea nuclear factor with light-responsive elements upstream of the rbcS-3A gene EMBO J 6 2543–2549

    Google Scholar 

  • E. Grotewold B.J. Drummond B. Bowen T. Peterson (1994) ArticleTitleThe myb-homologous P gene controls phlobaphene pigmentation in maize floral organs by directly activating a flavonoid biosynthetic gene subset Cell 76 543–553

    Google Scholar 

  • K. Hahlbrock H. Ragg (1975) ArticleTitleLight-induced changes of enzyme activities in parsley cell suspension cultures Effects of inhibitors of RNA and protein synthesis. Arch. Biochem. Biophys 166 41–46

    Google Scholar 

  • U. Hartmann W.J. Valentine J.M. Christie J. Hays G.I. Jenkins B. Weisshaar (1998) ArticleTitleIdentification of UV/blue light-response elements in the Arabidopsis thaliana chalcone synthase promoter using a homologous protoplast transient expression system Plant Mol. Biol. 36 741–754

    Google Scholar 

  • M.A. Heim M. Jakoby M. Werber C. Martin B. Weisshaar P.C. Bailey (2003) ArticleTitleThe basic helix-loop-helix transcription factor family in plants: a genome-wide study of protein structure and functional diversity Mol. Biol. Evol 20 735–747

    Google Scholar 

  • T.A. Holton E.C. Cornish (1995) ArticleTitleGenetics and Biochemistry of Anthocyanin Biosynthesis Plant Cell 7 1071–1083 Occurrence Handle10.1105/tpc.7.7.1071 Occurrence Handle1:CAS:528:DyaK2MXnt1Sgt7g%3D Occurrence Handle12242398

    Article  CAS  PubMed  Google Scholar 

  • T. Izawa R. Foster N.H. Chua (1993) ArticleTitlePlant bZIP protein DNA binding specificity J. Mol. Biol. 230 1131–1144

    Google Scholar 

  • D. Jackson K. Roberts C. Martin (1992) ArticleTitleTemporal and spatial control of expression of anthocyanin biosynthetic genes in developing flowers of Antirrhinum majus Plant J 2 425–434

    Google Scholar 

  • H. Jin E. Cominelli P. Bailey A. Parr F. Mehrtens J. Jones C. Tonelli B. Weisshaar C. Martin (2000) ArticleTitleTranscriptional repression by AtMYB4 controls production of UV-protecting sunscreens in Arabidopsis EMBO J 19 6150–6161 Occurrence Handle10.1093/emboj/19.22.6150

    Article  Google Scholar 

  • T. Kaiser K. Emmler T. Kretsch B. Weisshaar E. Schäfer A. Batschauer (1995) ArticleTitlePromoter elements of the mustard CHS1 gene sufficient for light regulation in transgenic plants Plant Mol. Biol. 28 219–229

    Google Scholar 

  • P. Kawalleck I.E. Somssich M. Feldbrügge K. Hahlbrock B. Weisshaar (1993) ArticleTitlePolyubiquitin gene expression and structural properties of the ubi4–2 gene in Petroselinum crispum Plant Mol. Biol. 21 673–684

    Google Scholar 

  • M.A. Koch B. Weisshaar J. Kroymann B. Haubold T. Mitchell-Olds (2001) ArticleTitleComparative genomics and regulatory evolution: conservation and function of the Chs and Apetala3 promoters Mol. Biol. Evol 18 1882–1891

    Google Scholar 

  • M. Koornneef W. Luiten P. Vlaming Particlede A.W. Schram (1982) ArticleTitleA gene controling flavonoid 3′-hydroxylation in Arabidopsis Arab. Inf. Serv 19 113–115

    Google Scholar 

  • W.L. Kubasek B.W. Shirley A. McKillop H.M. Goodman W. Briggs F.M. Ausubel (1992) ArticleTitleRegulation of flavonoid biosynthetic genes in germinating Arabidopsis seedlings Plant Cell 4 1229–1236 Occurrence Handle10.1105/tpc.4.10.1229 Occurrence Handle1:CAS:528:DyaK3sXls1aqsw%3D%3D Occurrence Handle12297632

    Article  CAS  PubMed  Google Scholar 

  • J. Li T.-M. Ou-Lee R. Raba R.G. Amundson R.L. Last (1993) ArticleTitleArabidopsis flavonoid mutants are hypersensitive to UV-B irradiation Plant Cell 5 171–179 Occurrence Handle10.1105/tpc.5.2.171 Occurrence Handle1:CAS:528:DyaK3sXit12hsbk%3D Occurrence Handle12271060

    Article  CAS  PubMed  Google Scholar 

  • C. Martin A. Prescott S. Mackay J. Bartlett E. Vrijlandt (1991) ArticleTitleControl of anthocyanin biosynthesis in flowers of Antirrhinum majus Plant J 1 37–49

    Google Scholar 

  • A.E. Menkens U. Schindler A.R. Cashmore (1995) ArticleTitleThe G-box: a ubiquitous regulatory DNA element in plants bound by the GBF family of bZIP proteins Trends Biochem. Sci. 20 506–510

    Google Scholar 

  • J. Mol E. Grotewold R. Koes (1998) ArticleTitleHow genes paint flowers and seeds Trends Plant Sci 3 212–217 Occurrence Handle10.1016/S1360-1385(98)01242-4

    Article  Google Scholar 

  • J. Mol G.I. Jenkins E. Schäfer D. Weiss (1996) ArticleTitleSignal perception, transduction, and gene expression involved in anthocyanin biosynthesis Critical Rev. Plant Sci 15 525–557

    Google Scholar 

  • E. Moyano J.F. Martinez-Garcia C. Martin (1996) ArticleTitleApparent redundancy in myb gene function provides gearing for the control of flavonoid biosynthesis in Antirrhinum flowers Plant Cell 8 1519–1532

    Google Scholar 

  • A. Murphy W.A. Peer L. Taiz (2000) ArticleTitleRegulation of auxin transport by aminopeptidases and endogenous flavonoids Planta 211 315–324

    Google Scholar 

  • N. Nesi I. Debeaujon C. Jond G. Pelletier M. Caboche L. Lepiniec (2000) ArticleTitleThe TT8gene encodes a basic helix-loop-helix domain protein required for expression of DFR and BAN genes in Arabidopsis siliques Plant Cell 12 1863–1878

    Google Scholar 

  • N. Nesi C. Jond I. Debeaujon M. Caboche L. Lepiniec (2001) ArticleTitleThe Arabidopsis TT2 gene encodes an R2R3 MYB domain protein that acts as a key determinant for proanthocyanidin accumulation in developing seed Plant Cell 13 2099–2114

    Google Scholar 

  • W.A. Peer A. Bandyopadhyay J.J. Blakeslee S.N. Makam R.J. Chen P.H. Masson A.S. Murphy (2004) ArticleTitleVariation in expression and protein localization of the PIN family of auxin efflux facilitator proteins in flavonoid mutants with altered auxin transport in Arabidopsis thaliana Plant Cell 16 1898–1911 Occurrence Handle10.1105/tpc.021501 Occurrence Handle1:CAS:528:DC%2BD2cXmtFSqtLc%3D Occurrence Handle15208397

    Article  CAS  PubMed  Google Scholar 

  • W.A. Peer D.E. Brown B.W. Tague G.K. Muday L. Taiz A.S. Murphy (2001) ArticleTitleFlavonoid Accumulation Patterns of Transparent TestaMutants of Arabidopsis Plant Physiol 126 536–548

    Google Scholar 

  • M.K. Pelletier J.R. Murrell B.W. Shirley (1997) ArticleTitleCharacterization of flavonol synthase and leucoanthocyanidin dioxygenase genes in Arabidopsis Plant Physiol 113 1437–1445

    Google Scholar 

  • M.K. Pelletier B.W. Shirley (1996) ArticleTitleAnalysis of flavanone 3-hydroxylase in Arabidopsis seedlings. Coordinate regulation with chalcone synthase and chalcone isomerase Plant Physiol 111 339–345

    Google Scholar 

  • A. Procissi S. Dolfini A. Ronchi C. Tonelli (1997) ArticleTitleLight-dependent spatial and temporal expression of pigment regulatory genes in developing maize seeds Plant Cell 9 1547–1557

    Google Scholar 

  • P. Rabinowicz E. Braun A. Wolfe B. Bowen E. Grotewold (1999) ArticleTitleMaize R2R3 Myb genes: Sequence analysis reveals amplification in the higher plants Genetics 153 427–444 Occurrence Handle1:CAS:528:DyaK1MXmsVWqur0%3D Occurrence Handle10471724

    CAS  PubMed  Google Scholar 

  • I. Romero A. Fuertes M.J. Benito J.M. Malpical A. Leyva J. Paz-Ares (1998) ArticleTitleMore than 80 R2R3-MYB regulatory genes in the genome of Arabidopsis thaliana Plant J 14 273–284 Occurrence Handle10.1046/j.1365-313X.1998.00113.x Occurrence Handle1:CAS:528:DyaK1cXjslOmu70%3D Occurrence Handle9628022

    Article  CAS  PubMed  Google Scholar 

  • M.B. Sainz E. Grotewold V.L. Chandler (1997) ArticleTitleEvidence for direct activation of an anthocyanin promoter by the maize C1 protein and comparison of DNA binding by related Myb domain proteins Plant Cell 9 611–625

    Google Scholar 

  • J. Sambrook E.F. Fritsch T. Maniatis (1989) Molecular Cloning: A Laboratory Manual Cold Spring Harbor Laboratory Press New York, NY

    Google Scholar 

  • G. Sarkar S.S. Sommer (1990) ArticleTitleThe “megaprimer” method of site-directed mutagenesis BioTechniques 8 404–407

    Google Scholar 

  • U. Schindler H. Beckmann A.R. Cashmore (1992) ArticleTitleTGA1 and G-box binding factors: Two distinct classes of Arabidopsis leucine zipper proteins compete for the G-box-like element TGACGTGG Plant Cell 4 1309–1319 Occurrence Handle10.1105/tpc.4.10.1309 Occurrence Handle1:CAS:528:DyaK3sXitVKmtbg%3D Occurrence Handle1446171

    Article  CAS  PubMed  Google Scholar 

  • C. Schoenbohm S. Martens C. Eder G. Forkmann B. Weisshaar (2000) ArticleTitleIdentification of the Arabidopsis thaliana flavonoid 3′-hydroxylase gene and functional expression of the encoded P450 enzyme Biol. Chem 381 749–753

    Google Scholar 

  • P. Schulze-Lefert J.L. Dangl M. Becker-André K. Hahlbrock W. Schulz (1989) ArticleTitleInducible in vivoDNA footprints define sequences necessary for UV light activation of the parsley chalcone synthase gene EMBO J 8 651–656

    Google Scholar 

  • B.W. Shirley (1996) ArticleTitleFlavonoid biosynthesis: ‘new’ functions for an ‘old’ pathway Trends Plant Sci 1 377–382 Occurrence Handle10.1016/1360-1385(96)10040-6

    Article  Google Scholar 

  • B.W. Shirley S. Hanley H.M. Goodman (1992) ArticleTitleEffects of ionizing radiation on a plant genome: analysis of two Arabidopsis transparent testa mutations Plant Cell 4 333–347 Occurrence Handle10.1105/tpc.4.3.333 Occurrence Handle1:CAS:528:DyaK38XitlSrsrs%3D Occurrence Handle1354004

    Article  CAS  PubMed  Google Scholar 

  • B.W. Shirley W.L. Kubasek G. Storz E. Bruggemann M. Koornneef F.M. Ausubel H.M. Goodman (1995) ArticleTitleAnalysis of Arabidopsis mutants deficient in flavonoid biosynthesis Plant J 8 659–671

    Google Scholar 

  • M. Sprenger-Haussels B. Weisshaar (2000) ArticleTitleTransactivation properties of parsley proline rich bZIP transcription factors Plant J 22 1–8

    Google Scholar 

  • R. Stracke M. Werber B. Weisshaar (2001) ArticleTitleThe R2R3-MYB gene family in Arabidopsis thaliana Curr. Opin. Plant Biol 4 447–456

    Google Scholar 

  • G.F. Trezzini A. Horrichs I.E. Somssich (1993) ArticleTitleIsolation of putative defense-related genes from Arabidopsis thaliana and expression in fungal elicitor-treated cells Plant Mol. Biol 21 385–389

    Google Scholar 

  • B. Weisshaar G.A. Armstrong A. Block O. daCostae Silva K. Hahlbrock (1991) ArticleTitleLight-inducible and constitutively expressed DNA-binding proteins recognizing a plant promoter element with functional relevance in light responsiveness EMBO J 10 1777–1786 Occurrence Handle1:CAS:528:DyaK38XhtVSgtLY%3D Occurrence Handle2050115

    CAS  PubMed  Google Scholar 

  • B. Weisshaar G.I. Jenkins (1998) ArticleTitlePhenylpropanoid biosynthesis and its regulation Curr. Opin. Plant Biol 1 251–257

    Google Scholar 

  • M.E. Williams R. Foster Chua N.-H. (1992) ArticleTitleSequences flanking the hexameric G-box core CACGTG affect the specificity of protein binding Plant Cell 4 485–496

    Google Scholar 

  • B. Winkel-Shirley (2001) ArticleTitleFlavonoid biosynthesis A colorful model for Genetics, Biochemistry, Cell Biology, and Biotechnology. Plant Physiol. 126 485–493

    Google Scholar 

  • E. Wisman U. Hartmann M. Sagasser E. Baumann K. Palme K. Hahlbrock H. Saedler B. Weisshaar (1998) ArticleTitleKnock-out mutants from an En-1 mutagenized Arabidopsis thaliana population generate new phenylpropanoid biosynthesis phenotypes Proc. Natl. Acad. Sci. USA 95 12432–12437

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Plant Breeding and Yield Physiology, Max-Planck-Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, D-50829, Köln, Germany

    Ulrike Hartmann, Martin Sagasser, Frank Mehrtens, Ralf Stracke & Bernd Weisshaar

  2. Genome Research, Department of Biology, Bielefeld University, D-33594, Bielefeld, Germany

    Martin Sagasser, Frank Mehrtens, Ralf Stracke & Bernd Weisshaar

Authors
  1. Ulrike Hartmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Martin Sagasser
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Frank Mehrtens
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ralf Stracke
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bernd Weisshaar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bernd Weisshaar.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hartmann, U., Sagasser, M., Mehrtens, F. et al. Differential combinatorial interactions of cis-acting elements recognized by R2R3-MYB, BZIP, and BHLH factors control light-responsive and tissue-specific activation of phenylpropanoid biosynthesis genes. Plant Mol Biol 57, 155–171 (2005). https://doi.org/10.1007/s11103-004-6910-0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-004-6910-0

Keywords

Search

Navigation