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A WD40-repeat gene from Malus × domestica is a functional homologue of Arabidopsis thaliana TRANSPARENT TESTA GLABRA1

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Abstract

The WD40 repeat protein TRANSPARENT TESTA GLABRA1 (TTG1) is involved in a multitude of developmental and biochemical reactions in Arabidopsis thaliana such as the production of seed coat colour and mucilage, pigmentation by anthocyanins as well as the formation of trichomes and root hairs. In this study, a putative TTG1 homologue was isolated from apple (Malus × domestica Borkh.) showing 80.2% identity to A. thaliana TTG1 on nucleotide and 90.7% similarity on amino acid level. The MdTTG1 candidate was able to activate the AtBAN promoter in cooperation with the A. thaliana transcription factors TT2 and TT8 in A. thaliana protoplasts. This indicates that the encoded protein can be integrated into the complex that activates BAN in A. thaliana, and that a similar complex might also be present in apple. When transformed into ttg1 mutants of A. thaliana, the apple sequence was able to restore trichome growth, anthocyanin production in young seedlings as well as proanthocyanidin production in seeds. Additionally, roots of complemented mutant plants showed root hair formation resembling wild type. These results show that the studied apple WD40 gene is a functional homologue of AtTTG1 and we refer to this gene as MdTTG1.

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References

  • Bagchi D, Sen CK, Ray SD, Das DK, Bagchi M, Preuss HG, Vinson JA (2003) Molecular mechanisms of cardioprotection by a novel grape seed proanthocyanidin extract. Mutat Res 523–524:87–97

    PubMed  Google Scholar 

  • Ban Y, Honda C, Hatsuyama Y, Igarashi M, Bessho H, Moriguchi T (2007) Isolation and functional analysis of a MYB transcription factor gene that is a key regulator for the development of red coloration in apple skin. Plant Cell Physiol 48:958–970

    Article  CAS  PubMed  Google Scholar 

  • Baudry A, Heim MA, Dubreucq B, Caboche M, Weisshaar B, Lepiniec L (2004) TT2, TT8, and TTG1 synergistically specify the expression of BANYULS and proanthocyanidin biosynthesis in Arabidopsis thaliana. Plant J 39:366–380

    Article  CAS  PubMed  Google Scholar 

  • Borevitz JO, Xia YJ, 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  Google Scholar 

  • Carey CC, Strahle JT, Selinger DA, Chandler VL (2004) Mutations in the pale aleurone color1 Regulatory Gene of the Zea mays anthocyanin pathway have distinct phenotypes relative to the functionally similar TRANSPARENT TESTA GLABRA1 Gene in Arabidopsis thaliana. Plant Cell 16:450–464

    Article  CAS  PubMed  Google Scholar 

  • Casas-Mollano JA, Destefano-Beltran L (2000) Characterization of a cDNA encoding a TTG1-like protein (Accession No. AF220203) from apple fruits. Plant Physiol 122:1458

    Google Scholar 

  • Chagne D, Carlisle CM, Blond C, Volz RK, Whitworth CJ, Oraguzie NC, Crowhurst RN, Allan AC, Espley RV, Hellens RP, Gardiner SE (2007) Mapping a candidate gene (MdMYB10) for red flesh and foliage colour in apple. BMC Genomics 8:212

    Article  PubMed  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Crespy V, Williamson G (2004) A review of the health effects of green tea catechins in in vivo animal models. J Nutr 134:3431S–3440S

    CAS  PubMed  Google Scholar 

  • de Vetten N, Quattrocchio F, Mol J, Koes R (1997) The an11 locus controlling flower pigmentation in petunia encodes a novel WD-repeat protein conserved in yeast, plants, and animals. Genes Dev 11:1422–1434

    Article  PubMed  Google Scholar 

  • Debeaujon I, Leon-Kloosterziel K, Koornneef M (2000) Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. Plant Physiol 122:403–413

    Article  CAS  PubMed  Google Scholar 

  • Dressel A, Hemleben V (2009) Transparent testa glabra 1 (TTG1) and TTG1-like genes in Matthiola incana R. Br. and related Brassicaceae and mutation in the WD-40 motif. Plant Biol 11:204–212

    Article  CAS  PubMed  Google Scholar 

  • Espley RV, Hellens RP, Putterill J, Stevenson DE, Kutty-Amma S, Allan AC (2007) Red colouration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10. Plant J 49:414–427

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Galway ME, Masucci JD, Lloyd AM, Walbot V, Davis RW, Schiefelbein JW (1994) The TTG gene is required to specify epidermal cell fate and cell patterning in the Arabidopsis root. Dev Biol 166:740–754

    Article  CAS  PubMed  Google Scholar 

  • Gasic K, Hernandez A, Korban S (2004) RNA extraction from different apple tissues rich in polyphenols and polysaccharides for cDNA library construction. Plant Mol Biol Rep 22:437–438

    Article  CAS  Google Scholar 

  • Honda C, Kotoda N, Wada M, Kondo S, Kobayashi S, Soejima J, Zhang Z, Tsuda T, Moriguchi T (2002) Anthocyanin biosynthetic genes are coordinately expressed during red coloration in apple skin. Plant Physiol Biochem 40:955–962

    Article  CAS  Google Scholar 

  • Humphries JA, Walker AR, Timmis JN, Orford SJ (2005) Two WD-repeat genes from cotton are functional homologues of the Arabidopsis thaliana TRANSPARENT TESTA GLABRA1 (TTG1) gene. Plant Mol Biol 57:67–81

    Article  CAS  PubMed  Google Scholar 

  • Koncz C, Schell J (1986) The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector. Mol Gen Genet 204:383–396

    Article  CAS  Google Scholar 

  • Koornneef M (1981) The complex syndrome of ttg mutants. Arabidopsis Inf Serv 18:45–51

    Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Lepiniec L, Debeaujon I, Routaboul JM, Baudry A, Pourcel L, Nesi N, Caboche M (2006) Genetics and biochemistry of seed flavonoids. Annu Rev Plant Biol 57:405–430

    Article  CAS  PubMed  Google Scholar 

  • Marles MA, Ray H, Gruber MY (2003) New perspectives on proanthocyanidin biochemistry and molecular regulation. Phytochemistry 64:367–383

    Article  CAS  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  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Plant Physiol 15:473–497

    Article  CAS  Google Scholar 

  • Nakai K, Horton P (1999) PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem Sci 24:34–36

    Article  CAS  PubMed  Google Scholar 

  • Nesi N, Debeaujon I, Jond C, Pelletier G, Caboche M, Lepiniec L (2000) The TT8 gene encodes a basic helix–loop–helix domain protein required for expression of DFR and BAN genes in Arabidopsis siliques. Plant Cell 12:1863–1878

    Article  CAS  PubMed  Google Scholar 

  • Pang Y, Wenger JP, Saathoff K, Peel GJ, Wen J, Huhman D, Allen SN, Tang Y, Cheng X, Tadege M, Ratet P, Mysore KS, Sumner LW, Marks MD, Dixon RA (2009) A WD40 repeat protein from Medicago truncatula is necessary for tissue-specific anthocyanin and proanthocyanidin biosynthesis, but not for trichome development. Plant Physiol 151:1114–1129

    Article  CAS  PubMed  Google Scholar 

  • Renard CM, Dupont N, Guillermin P (2007) Concentrations and characteristics of procyanidins and other phenolics in apples during fruit growth. Phytochemistry 68:1128–1138

    Article  CAS  PubMed  Google Scholar 

  • Rogers SO, Bendich AJ (1985) Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant tissues. Plant Mol Biol 5:69–76

    Article  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York, NY

    Google Scholar 

  • Sompornpailin K, Makita Y, Yamazaki M, Saito K (2002) A WD-repeat-containing putative regulatory protein in anthocyanin biosynthesis in Perilla frutescens. Plant Mol Biol 50:485–495

    Article  CAS  PubMed  Google Scholar 

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

    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  Google Scholar 

  • Stultz CM, White JV, Smith TF (1993) Structural analysis based on state-space modeling. Protein Sci 2:305–314

    Article  CAS  PubMed  Google Scholar 

  • Takos AM, Jaffe FW, Jacob SR, Bogs J, Robinson SP, Walker AR (2006) Light-induced expression of a MYB gene regulates anthocyanin biosynthesis in red apples. Plant Physiol 142:1216–1232

    Article  CAS  PubMed  Google Scholar 

  • Van de Peer Y, De Wachter R (1994) TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Comput Appl Biosci 10:569–570

    PubMed  Google Scholar 

  • Walker AR, Davison PA, Bolognesi-Winfield AC, James CM, Srinivasan N, Blundell TL, Esch JJ, Marks MD, Gray JC (1999) The TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein. Plant Cell 11:1337–1350

    Article  CAS  PubMed  Google Scholar 

  • Winkel-Shirley B (2001) Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126:485–493

    Article  CAS  PubMed  Google Scholar 

  • Xie DY, Sharma SB, Paiva NL, Ferreira D, Dixon RA (2003) Role of anthocyanidin reductase, encoded by BANYULS in plant flavonoid biosynthesis. Science 299:396–399

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Lu Y, Yuan Y, Zhang X, Geng J, Chen Y, Cloutier S, McVetty PB, Li G (2009) Map-based cloning and characterization of a gene controlling hairiness and seed coat color traits in Brassica rapa. Plant Mol Biol 69:553–563

    Article  CAS  PubMed  Google Scholar 

  • Zhao M, Morohashi K, Hatlestad G, Grotewold E, Lloyd A (2008) The TTG1-bHLH-MYB complex controls trichome cell fate and patterning through direct targeting of regulatory loci. Development 135:1991–1999

    Article  CAS  PubMed  Google Scholar 

  • Zimmermann IM, Heim MA, Weisshaar B, Uhrig JF (2004) Comprehensive identification of Arabidopsis thaliana MYB transcription factors interacting with R/B-like BHLH proteins. Plant J 40:22–34

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Marten Koornneef for the gift of ttg1-1 seeds, Marc Jakoby for providing pANGUS as well as Thilo Fischer and Judith Pfeiffer for providing the apple plant material. This work was funded by the EU project FLAVO (FOOD-CT-2004-513960).

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Authors and Affiliations

  1. Department of Biology, Bielefeld University, 33594, Bielefeld, Germany

    Julian Brueggemann, Bernd Weisshaar & Martin Sagasser

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  1. Julian Brueggemann
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  2. Bernd Weisshaar
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  3. Martin Sagasser
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Corresponding author

Correspondence to Martin Sagasser.

Additional information

Communicated by R. Schmidt.

Nucleotide sequences reported in this paper were submitted to GenBank under accession numbers GU173813 and GU173814.

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Brueggemann, J., Weisshaar, B. & Sagasser, M. A WD40-repeat gene from Malus × domestica is a functional homologue of Arabidopsis thaliana TRANSPARENT TESTA GLABRA1 . Plant Cell Rep 29, 285–294 (2010). https://doi.org/10.1007/s00299-010-0821-0

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