Home LiteratureArticle Details
PMID: 14555692 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Proanthocyanidin-accumulating cells in Arabidopsis testa: regulation of differentiation and role in seed development.

The Plant cell ·Vol. 15 ·No. 11 ·2003-11-00 ·Pages 2514-31

Debeaujon I, Nesi N, Perez P, Devic M, Grandjean O, Caboche M, Lepiniec L

Abstract

Anthocyanidin reductase encoded by the BANYULS (BAN) gene is the core enzyme in proanthocyanidin (PA) biosynthesis. Here, we analyzed the developmental mechanisms that regulate the spatiotemporal expression of BAN in the developing Arabidopsis seed coat. PA-accumulating cells were localized histochemically in the inner integument (seed body and micropyle) and pigment strand (chalaza). BAN promoter activity was detected specifically in these cells. Gain-of-function experiments showed that an 86-bp promoter fragment functioned as an enhancer specific for PA-accumulating cells. Mutations in regulatory genes of PA biosynthesis abolished BAN promoter activity (transparent testa2 [tt2], tt8, and transparent testa glabra1 [ttg1]), modified its spatial pattern (tt1 and tt16), or had no influence (ttg2), thus revealing complex regulatory interactions at several developmental levels. Genetic ablation of PA-accumulating cells targeted by the BAN promoter fused to BARNASE led to the formation of normal plants that produced viable yellow seeds. Importantly, these seeds had no obvious defects in endosperm and embryo development.

MeSH Terms
Arabidopsis/genetics,growth & development,metabolism Arabidopsis Proteins/genetics,metabolism Base Sequence Cell Differentiation/genetics,physiology DNA-Binding Proteins/genetics,metabolism Gene Expression Regulation, Developmental Gene Expression Regulation, Plant MADS Domain Proteins/genetics,metabolism Molecular Sequence Data Mutation NADH, NADPH Oxidoreductases/genetics,metabolism Proanthocyanidins/biosynthesis,metabolism Promoter Regions, Genetic/genetics Seeds/genetics,growth & development,metabolism Sequence Homology, Nucleic Acid Tannins/biosynthesis
Chemicals
Arabidopsis Proteins DNA-Binding Proteins MADS Domain Proteins Proanthocyanidins TT16 protein, Arabidopsis TT2 protein, Arabidopsis Tannins BANYULS protein, Arabidopsis NADH, NADPH Oxidoreductases
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Debeaujon Isabelle
Laboratoire de Biologie des Semences, Unité Mixte de Recherche, 204 Institut National de la Recherche Agronomique, Paris-Grignon, 78026 Versailles, France.
Nesi Nathalie
Perez Pascual
Devic Martine
Grandjean Olivier
Caboche Michel
Lepiniec Loïc
References (44)
44 references, click to expand
  1. An allelic series for the chalcone synthase locus in Arabidopsis.
    Gene. 2000 Sep 19;255(2):127-38 PMID: 11024274
  2. Development of tannin vacuoles in chalaza and seed coat of barley in relation to early chalazal necrosis in the seg1 mutant.
    Planta. 1984 Nov;161(6):540-9 PMID: 24253924
  3. Plant cell identity. The role of position and lineage.
    Plant Physiol. 2001 Jan;125(1):112-4 PMID: 11154310
  4. A. thaliana TRANSPARENT TESTA 1 is involved in seed coat development and defines the WIP subfamily of plant zinc finger proteins.
    Genes Dev. 2002 Jan 1;16(1):138-49 PMID: 11782451
  5. C1- and R-dependent expression of the maize Bz1 gene requires sequences with homology to mammalian myb and myc binding sites.
    Plant Cell. 1991 Mar;3(3):317-25 PMID: 1840914
  6. Positional cues specify and maintain aleurone cell fate in maize endosperm development.
    Development. 2000 Sep;127(18):4039-48 PMID: 10952901
  7. The TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein.
    Plant Cell. 1999 Jul;11(7):1337-50 PMID: 10402433
  8. Plant biology. Seeing red.
    Science. 2003 Jan 17;299(5605):352-3 PMID: 12532002
  9. Mutations in FIE, a WD polycomb group gene, allow endosperm development without fertilization.
    Plant Cell. 1999 Mar;11(3):407-16 PMID: 10072400
  10. Phenylpropanoid biosynthesis and its regulation.
    Curr Opin Plant Biol. 1998 Jun;1(3):251-7 PMID: 10066590
  11. Endosperm: the crossroad of seed development.
    Curr Opin Plant Biol. 2003 Feb;6(1):42-50 PMID: 12495750
  12. Multifunctionality and diversity within the plant MYB-gene family.
    Plant Mol Biol. 1999 Nov;41(5):577-85 PMID: 10645718
  13. Control of cell division in the root epidermis of Arabidopsis thaliana.
    Dev Biol. 1998 Feb 15;194(2):235-45 PMID: 9501025
  14. Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis.
    Plant Physiol. 2000 Feb;122(2):403-14 PMID: 10677433
  15. Mutation rate and novel tt mutants of Arabidopsis thaliana induced by carbon ions.
    Genetics. 2003 Apr;163(4):1449-55 PMID: 12702688
  16. The Arabidopsis thaliana MERISTEM LAYER 1 promoter specifies epidermal expression in meristems and young primordia.
    Plant J. 1999 Oct;20(2):259-63 PMID: 10571886
  17. The TRANSPARENT TESTA16 locus encodes the ARABIDOPSIS BSISTER MADS domain protein and is required for proper development and pigmentation of the seed coat.
    Plant Cell. 2002 Oct;14(10):2463-79 PMID: 12368498
  18. The TT8 gene encodes a basic helix-loop-helix domain protein required for expression of DFR and BAN genes in Arabidopsis siliques.
    Plant Cell. 2000 Oct;12(10):1863-78 PMID: 11041882
  19. The BANYULS gene encodes a DFR-like protein and is a marker of early seed coat development.
    Plant J. 1999 Aug;19(4):387-98 PMID: 10504561
  20. Cap-independent enhancement of translation by a plant potyvirus 5' nontranslated region.
    J Virol. 1990 Apr;64(4):1590-7 PMID: 2319646
  21. BANYULS, a novel negative regulator of flavonoid biosynthesis in the Arabidopsis seed coat.
    Plant J. 1997 Feb;11(2):289-99 PMID: 9076994
  22. The Arabidopsis TT2 gene encodes an R2R3 MYB domain protein that acts as a key determinant for proanthocyanidin accumulation in developing seed.
    Plant Cell. 2001 Sep;13(9):2099-114 PMID: 11549766
  23. Dual DNA binding specificity of a petal epidermis-specific MYB transcription factor (MYB.Ph3) from Petunia hybrida.
    EMBO J. 1995 Apr 18;14(8):1773-84 PMID: 7737128
  24. Repression domains of class II ERF transcriptional repressors share an essential motif for active repression.
    Plant Cell. 2001 Aug;13(8):1959-68 PMID: 11487705
  25. Functional analysis of the transcriptional activator encoded by the maize B gene: evidence for a direct functional interaction between two classes of regulatory proteins.
    Genes Dev. 1992 May;6(5):864-75 PMID: 1577278
  26. ANTHOCYANINLESS2, a homeobox gene affecting anthocyanin distribution and root development in Arabidopsis.
    Plant Cell. 1999 Jul;11(7):1217-26 PMID: 10402424
  27. Genes controlling fertilization-independent seed development in Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 1999 Jan 5;96(1):296-301 PMID: 9874812
  28. ANTHOCYANIN1 of petunia controls pigment synthesis, vacuolar pH, and seed coat development by genetically distinct mechanisms.
    Plant Cell. 2002 Sep;14(9):2121-35 PMID: 12215510
  29. Dynamic analyses of the expression of the HISTONE::YFP fusion protein in arabidopsis show that syncytial endosperm is divided in mitotic domains.
    Plant Cell. 2001 Mar;13(3):495-509 PMID: 11251092
  30. Identification and biochemical characterization of mutants in the proanthocyanidin pathway in Arabidopsis.
    Plant Physiol. 2002 Oct;130(2):561-76 PMID: 12376625
  31. Role of anthocyanidin reductase, encoded by BANYULS in plant flavonoid biosynthesis.
    Science. 2003 Jan 17;299(5605):396-9 PMID: 12532018
  32. TRANSPARENT TESTA GLABRA2, a trichome and seed coat development gene of Arabidopsis, encodes a WRKY transcription factor.
    Plant Cell. 2002 Jun;14(6):1359-75 PMID: 12084832
  33. Structure and regulation of the maize Bronze2 promoter.
    Plant Mol Biol. 1996 Nov;32(4):599-609 PMID: 8980512
  34. Activation of the maize anthocyanin gene a2 is mediated by an element conserved in many anthocyanin promoters.
    Plant Physiol. 1998 Jun;117(2):437-45 PMID: 9625696
  35. New light on Myc and Myb. Part II. Myb.
    Genes Dev. 1990 Dec;4(12B):2235-41 PMID: 2279697
  36. Zinc-finger proteins: the classical zinc finger emerges in contemporary plant science.
    Plant Mol Biol. 1999 Apr;39(6):1073-8 PMID: 10380795
  37. Transposon insertions in the promoter of the Zea mays a1 gene differentially affect transcription by the Myb factors P and C1.
    Genetics. 2002 Jun;161(2):793-801 PMID: 12072474
  38. Gibberellin requirement for Arabidopsis seed germination is determined both by testa characteristics and embryonic abscisic acid.
    Plant Physiol. 2000 Feb;122(2):415-24 PMID: 10677434
  39. Identification of a meristem L1 layer-specific gene in Arabidopsis that is expressed during embryonic pattern formation and defines a new class of homeobox genes.
    Plant Cell. 1996 Dec;8(12):2155-68 PMID: 8989876
  40. Binary vectors which allow the exchange of plant selectable markers and reporter genes.
    Nucleic Acids Res. 1990 Jan 11;18(1):203 PMID: 2408008
  41. Downregulation of ovule-specific MADS box genes from petunia results in maternally controlled defects in seed development.
    Plant Cell. 1997 May;9(5):703-15 PMID: 9165748
  42. The myb-homologous P gene controls phlobaphene pigmentation in maize floral organs by directly activating a flavonoid biosynthetic gene subset.
    Cell. 1994 Feb 11;76(3):543-53 PMID: 8313474
  43. Elements of the maize A1 promoter required for transactivation by the anthocyanin B/C1 or phlobaphene P regulatory genes.
    Plant Cell. 1994 Nov;6(11):1655-63 PMID: 7827497
  44. The TRANSPARENT TESTA12 gene of Arabidopsis encodes a multidrug secondary transporter-like protein required for flavonoid sequestration in vacuoles of the seed coat endothelium.
    Plant Cell. 2001 Apr;13(4):853-71 PMID: 11283341
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
Published
2003-11-00
Epub
2003-00-10
Pages
2514-31
Language
English
Region
England
NLM ID
9208688
PMCID
PMC280558
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]