Skip to main content
SpringerLink
Log in

Seed-specific transcription factors ABI3 and FUS3: molecular interaction with DNA

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

In Arabidopsis thaliana (L.) Heynh. the seed-specific transcription factors ABI3 and FUS3 have key regulatory functions during the development of mature seeds. The highly conserved RY motif [DNA motif CATGCA(TG)], present in many seed-specific promoters, is an essential target of both regulators. Here we show that, in vitro, the full-length ABI3 protein, as well as FUS3 protein, is able to bind to RY-DNA and that the B3 domains of both transcription factors are necessary and sufficient for the specific interaction with the RY element. Flanking sequences of the RY motif modulate the binding, but the presence of an RY sequence alone allows the specific interaction of ABI3 and FUS3 with the target in vitro. Transcriptional activity of ABI3 and FUS3, measured by transient promoter activation, requires the B3 DNA-binding domain and an activation domain. In addition to the known N-terminal-located activation domain, a second transcription activation domain was found in the B1 region of ABI3.

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. 1a–d
Fig. 2a,b
Fig. 3a–c
Fig. 4
Fig. 5a,b
Fig. 6a,b

Similar content being viewed by others

Abbreviations

ABI3 :

Abscisic acid insensitive 3

FUS3 :

FUSCA 3

GUS :

β-Glucuronidase

LEC1(2) :

Leafy cotyledon 1 (2)

RY :

DNA motif CATGCA(TG)

References

  • Bäumlein H, Wobus U, Pustell J, Kafatos FC (1986) The legumin gene family: structure of a B-type gene of Vicia faba and a possible legumin gene specific regulatory element. Nucleic Acids Res 14:2707–2720

    PubMed  Google Scholar 

  • Bäumlein H, Boerjan W, Nagy I, Bassüner R, van Montagu M, Inze D, Wobus U (1991a) A novel seed protein gene from Vicia faba is developmentally regulated in transgenic tobacco and Arabidopsis plants. Mol Gen Genet 22:459–467

    Google Scholar 

  • Bäumlein H, Boerjan W, Nagy I, Panitz R, Inze D, Wobus U (1991b) Upstream sequences regulating legumin gene expression in heterologous transgenic plants. Mol Gen Genet 225:121–128

    PubMed  Google Scholar 

  • Bäumlein H, Nagy I, Villarroel R, Inze D, Wobus U (1992) Cis-analysis of a seed protein gene promoter: the conservative RY repeat CATGCATG within the legumin box is essential for tissue-specific expression of a legumin gene. Plant J 2:233–239

    PubMed  Google Scholar 

  • Bäumlein H, Misera S, Luerssen H, Kölle K, Horstmann C, Wobus U, Müller AJ (1994) The FUS3 gene of Arabidopsis thaliana is a regulator of gene expression during late embryogenesis. Plant J 6:379–387

    Article  Google Scholar 

  • Benotmane AM, Hoylaerts MF, Collen D, Belayew A (1997) Nonisotopic quantitative analysis of protein–DNA interactions at equilibrium. Anal Biochem 250:181–185

    Article  CAS  PubMed  Google Scholar 

  • Bobb AJ, Chern MS, Bustos MM (1997) Conserved RY repeats mediate transactivation of seed specific promoters by the developmental regulator PvALF. Nucleic Acids Res 25:641–647

    Article  CAS  PubMed  Google Scholar 

  • Dickinson CD, Evans RP, Nielsen NC (1988) RY repeats are conserved in the 5′-flanking regions of legume seed-protein genes. Nucleic Acids Res 16:371

    CAS  PubMed  Google Scholar 

  • Ellerström M, Stalberg K, Ezcurra I, Rask L (1996) Functional dissection of a napin gene promoter: identification of promoter elements required for embryo and endosperm-specific transcription. Plant Mol Biol 32:1019–1027

    PubMed  Google Scholar 

  • Ezcurra I, Wycliffe P, Nehlin L, Ellerström M, Rask L (2000) Transactivation of the Brassica napus napin promoter by ABI3 requires interaction of the conserved B2 and B3 domains of ABI3 with different cis-elements: B2 mediates activation through an ABRE, whereas B3 interacts with an RY/G-box. Plant J 24:57–66

    Article  CAS  PubMed  Google Scholar 

  • Fisher RJ, Fivash M, Casas-Finet J, Erickson JW, Kondoh A, Bladen SV, Fisher C, Watson DK, Papas T (1994) Real-time DNA binding measurements of the ETS1 recombinant oncoproteins reveal significant kinetic differences between the p42 and p51 isoforms. Protein Sci 3:257–266

    CAS  PubMed  Google Scholar 

  • Giraudat J, Hauge BM, Valon C, Smalle J, Parcy F, Goodman HM (1992) Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell 4:1251–1261

    PubMed  Google Scholar 

  • Goldberg RB, Depaiva G, Yadegari R (1994) Plant embryogenesis—zygote to seed. Science 266:605–614

    CAS  Google Scholar 

  • Hobo T, Kowyama Y, Hattori T (1999) A bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid-induced transcription. Proc Natl Acad Sci USA 96:15348–15353

    Article  CAS  PubMed  Google Scholar 

  • Holdsworth MJ, Kurup S, McKibbin R (1999) Molecular and genetic mechanisms regulating the transition from embryo development to germination. Trends Plant Sci 4:275–280

    Article  Google Scholar 

  • Koornneef M, Reuling G, Karssen CM (1984) The isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana. Plant Physiol 90:463–469

    Google Scholar 

  • Kurup S, Jones HD, Holdsworth MJ (2000) Interaction of the developmental regulator ABI3 with proteins identified from developing Arabidopsis seeds. Plant J 21:143–146

    Article  CAS  PubMed  Google Scholar 

  • Lazarova G, Zeng Y, Kermode AR (2002) Cloning and expression of an ABSCISIC ACID-INSENSITIVE 3 (ABI3) gene homologue of yellow-cedar (Chamaecyparis nootkatensis). J Exp Bot 53:1219–1221

    Article  CAS  PubMed  Google Scholar 

  • Lotan T, Harada JJ (1998) Arabidopsis LEAFY COTYLEDON 1 is sufficient to induce embryo development in vegetative cells. Cell 93:1195–1205

    CAS  PubMed  Google Scholar 

  • Luerssen H, Kirik V, Herrmann P, Misera S (1998) FUSCA3 encodes a protein with a conserved VP1/ABI3-like B3 domain which is of functional importance for the regulation of seed maturation in Arabidopsis thaliana. Plant J 15:755–764

    Article  CAS  PubMed  Google Scholar 

  • Mayer U, Torres Ruiz RA, Misera S, Jürgens G (1991) Mutations affecting body organization in the Arabidopsis embryo. Nature 353:402–407

    Article  Google Scholar 

  • McCarty DR (1995) Genetic control and integration of maturation and germination pathways in seed development. Annu Rev Plant Physiol Plant Mol Biol 46:71–93

    CAS  Google Scholar 

  • McCarty DR, Hattori T, Carson CB, Vasil V, Lazar M, Vasil IK (1991) The Viviparous-1 developmental gene of maize encodes a novel transcriptional activator. Cell 66:895–905

    PubMed  Google Scholar 

  • McKay IA, Kirby L, Volyanik EV, Kumar V, Wong PW, Bustin SA (1998) An enzyme-linked immunosorbent assay for the detection of agents which interfere with the DNA binding activities of transcription factors—exemplified by NF-IL6. Anal Biochem 265:28–34

    Article  CAS  PubMed  Google Scholar 

  • Meinke DW, Franzmann LH, Nickle TC, Yeung EC (1994) Leafy cotyledon mutants of Arabidopsis. Plant Cell 6:1049–1064

    Article  CAS  PubMed  Google Scholar 

  • Müller AJ (1963) Embryonentest zum Nachweis rezessiver Lethalfaktoren bei Arabidopsis thaliana. Biol Zentralbl 83:133–163

    Google Scholar 

  • Nakamura S, Lynch TJ, Finkelstein RR (2001) Physical interaction between ABA response loci of Arabidopsis. Plant J 26: 627-635

    Article  CAS  PubMed  Google Scholar 

  • Parcy F, Valon C, Raynal M, Gaubiercomella P, Delseny M, Giraudat J (1994) Regulation of gene-expression programs during Arabidopsis seed development—roles of the ABI3 locus and of endogenous abscisic-acid. Plant Cell 6:1567–1582

    Article  CAS  PubMed  Google Scholar 

  • Parcy F, Valon Ch, Kohara A, Misera S, Giraudat J (1997) The ABSCISIC ACID-INSENSITIVE3, FUSCA3, and LEAFY COTYLEDON1 loci act in concert to control multiple aspects of Arabidopsis seed development. Plant Cell 9:1265–1277

    Article  CAS  PubMed  Google Scholar 

  • Raz V, Bergervoet JH, Koornneef M (2001) Sequential steps for developmental arrest in Arabidopsis seeds. Development 128:243–252

    CAS  PubMed  Google Scholar 

  • Reidt W (2002) Analysis of transcription factors during late-embryogenesis: the role of FUS3, LEC1, ABI3 and AtET. Thesis, University of Halle, Germany

  • Reidt W, Wohlfarth T, Ellerström M, Czihal A, Tewes A, Ezcurra I, Rask L, Bäumlein H (2000) Gene regulation during late embryogenesis: the RY motif of maturation-specific gene promoters is a direct target of the FUS3 gene product. Plant J 21:1–8

    Article  PubMed  Google Scholar 

  • Reidt W, Ellerström M, Kölle K, Tewes A, Tiedemann J, Altschmied L, Bäumlein H (2001) FUS3-dependent gene regulation during late embryogenesis. J Plant Physiol 158:411–418

    CAS  Google Scholar 

  • Stalberg K, Ellerström M, Ezcurra I, Ablov S, Rask L (1996) Disruption of an overlapping E-box/ABRE motif abolished high transcription of the napA storage-protein promoter in transgenic Brassica napus seeds. Planta 199:515–519

    CAS  PubMed  Google Scholar 

  • Stone SL, Kwong LW, Yee KM, Pelletier J, Lepiniec L, Fischer RL, Goldberg RB, Harada JJ (2001) LEAFY COTYLEDON2 encodes a B3 domain transcription factor that induces embryo development. Proc Natl Acad Sci USA 98:11806–11811

    Article  CAS  PubMed  Google Scholar 

  • Suzuki M, Kao CY, McCarty DR (1997) The conserved B3 domain of VIVIPAROUS1 has a cooperative DNA binding activity. Plant Cell 9:799–807

    Article  CAS  PubMed  Google Scholar 

  • West MAJ, Yee KM, Danao J, Zimmermann JL, Fischer RL, Goldberg RB, Harada JJ (1994) LEAFY COTYLEDON 1 is an essential regulator of late embryogenesis and cotyledon identity. Plant Cell 6:1731–1745

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to Barbara Kettig for her excellent help with FPLC, to Sabine Skiebe for skillful handling of the transactivation experiments and to Heike Ernst for graphical support.

Author information

Authors and Affiliations

  1. Institut für Pflanzengenetik und Kulturpflanzenforschung Gatersleben, Corrensstr.3, 6466, Gatersleben, Germany

    Gudrun Mönke, Lothar Altschmied, Annegret Tewes, Wim Reidt, Hans-Peter Mock, Helmut Bäumlein & Udo Conrad

Authors
  1. Gudrun Mönke
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lothar Altschmied
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Annegret Tewes
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wim Reidt
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hans-Peter Mock
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Helmut Bäumlein
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Udo Conrad
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Udo Conrad.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mönke, G., Altschmied, L., Tewes, A. et al. Seed-specific transcription factors ABI3 and FUS3: molecular interaction with DNA. Planta 219, 158–166 (2004). https://doi.org/10.1007/s00425-004-1206-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-004-1206-9

Keywords

Search

Navigation