Advertisement

Plant Molecular Biology

, Volume 28, Issue 4, pp 723–737 | Cite as

The homeobox gene ATK1 of Arabidopsis thaliana is expressed in the shoot apex of the seedling and in flowers and inflorescence stems of mature plants

  • Jan Dockx
  • Nicolette Quaedvlieg
  • Gerbienne Keultjes
  • Patricia Kock
  • Peter Weisbeek
  • Sjef Smeekens
Research Article

Abstract

The homeodomain is a DNA-binding domain present in a large family of eukaryotic regulatory proteins. Homeodomain proteins have been shown to play key roles in controlling developmental programs in various organisms. Here we report the isolation and characterisation of a homeobox gene from Arabidopsis thaliana designated ATK1. The gene was isolated using as a probe the homeobox domain of the KN1 gene from maize. The homeodomain of ATK1 is highly homologous to the homeodomain of the KN1 gene of maize (81%) but shows only poor homology outside the homeodomain. Therefore ATK1 is probably not the Arabidopsis homologue of the KN1 gene from maize. It contains the four invariant amino acid residues present in the recognition helix 3 of all other homeodomain proteins. Outside the homeodomain a region rich in aspartate and glutamate residues is found suggesting that ATK1 is a transcriptional activator. The gene contains four introns which is similar in the KN1 gene of maize and the Osh1 gene of rice. Primer extension reveals the presence of two transcription initiation sites. The leader sequence of the genuine transcript is 342 nucleotides long and contains two upstream open reading frames. ATK1 is strongly expressed in the shoot apex of seedlings, while in mature plants the gene is primarily expressed in flowers and inflorescence stems. Such an expression pattern is reminiscent of that of the KN1 gene of maize and therefore ATK1 could similarly be involved in determining cell fate.

Key words

Arabidopsis thaliana homeobox shoot apex transcription factor uORF 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Bellman R, Werr W: Zmhoxla, the product of a novel maize homeobox gene, interacts with the Shrunken 26 bp feedback control element. EMBO J 11: 3367–3374 (1992).Google Scholar
  2. 2.
    Brown JWS: A catalogue of splice and putative branch point sequences from plant introns. Nucl Acids Res 14: 9549–9555 (1986).Google Scholar
  3. 3.
    Brusslan JA, Tobin EM: Light-independent developmental regulation of cab gene expression in Arabidopsis thaliana seedlings. Procl Natl Acad Sci USA 89: 7791–7795 (1992).Google Scholar
  4. 4.
    Church GM, Gilbert W: Genomic sequencing. Proc Natl Acad Sci USA 81: 1991–1995 (1984).Google Scholar
  5. 5.
    Damiani RD, Wessler SR: An upstream open reading frame represses expression of Lc, a member of the R/B family of maize transcriptional activators. Proc Natl Acad Sci USA 90: 8244–8248 (1993).Google Scholar
  6. 6.
    Dellaporta SL, Wood J, Hicks JB: A plant DNA minipreparation: version II. Plant Mol Biol Rep 1–4: 19–21 (1983).Google Scholar
  7. 7.
    Feinberg AP, Vogelstein B: A technique for radiolabelling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132: 6–13 (1983).Google Scholar
  8. 8.
    Gehring WJ, Muller M, Affolter M, Percival-Smith A, Billeter M, Qian YQ, Otting G, Wutrich K: The structure of the homeodomain and its functional application. Trends Genet 6: 323–329 (1990).Google Scholar
  9. 9.
    Gelvin SB, Schilperoort RA: Kluwer Academic Publisher (ed), Plant Molecular Biology Manual, A3/7 p. Kluwer Academic Publisher, Dordrecht (1988).Google Scholar
  10. 10.
    Gerber H-P, Seipel K, Georgiev O, Höfferer M, Hug M, Rusconi S, Schaffner W: Transcriptional activation modulated by homopolymeric glutamine and proline stretches. Science 263: 808–811 (1994).Google Scholar
  11. 11.
    Hayashi S, Scott MP: What determines the specificity of action of Drosophila homeodomains proteins? Cell 63: 883–894 (1990).Google Scholar
  12. 12.
    Hinnebusch HG: Involvement of an initiation factor and protein phosphorylation in translational control of GCN4 mRNA. Trends Biochem Sci 15: 148–152 (1990).Google Scholar
  13. 13.
    Jackson D, Veit B, Hake S: Expression of maize KNOTTED1 related homeobox genes in the shoot apical meristems predicts patterns of morphogenesis in the vegetative shoot. Development 120: 405–413 (1994).Google Scholar
  14. 14.
    Jefferson RA, Kavanagh TA, Bevan MW: GUS-fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901–3907 (1987).Google Scholar
  15. 15.
    Kaufman TC, Seeger MA, Olsen G: Molecular and genetic organization of the antennapedia gene complex of Drosphila melanogaster. Adv Genet 27: 309–362 (1990).Google Scholar
  16. 16.
    Kelly M, Burke J, Smith M, Klar A, Beach D: Four mating-type genes control sexual differentiation in the fission yeast. EMBO J 7: 1537–1547 (1988).Google Scholar
  17. 17.
    Kerstetter R, Vollbrecht E, Lowe B, Veit B, Yamaguchi J, Hake S: Sequence analysis and expression pattern divide the maize knotted1-like homeobox genes in two classes. Plant Cell 6: 1877–1887 (1994).Google Scholar
  18. 18.
    Korfhage U, Trezzini GF, Meier I, Hahlbrock K, Somssich IM: Plant homeodomain protein involved in transcriptional regulation of a pathogen defense-related gene. Plant Cell 6: 695–708 (1994).Google Scholar
  19. 19.
    Laughon A: DNA binding specificity of homeodomains. Biochemistry 30: 11357–11367 (1991).Google Scholar
  20. 20.
    Liang X, Dron M, Schmid J, Dixon RA, Lamb CJ: Developmental and environmental regulation of a phenylalanine ammonia-lyase-beta-glucurodinase gene fusion in transgenic tobacco plants. Proc Natl Acad Sci USA 86: 9284–9288 (1989).Google Scholar
  21. 21.
    Lincoln C, Long J, Yamaguchi J, Serikawa K, Hake S: A knotted1-like homeobox gene in Arabidopsis is expressed in the vegetative meristem and dramatically alters leaf morphology when overexpressed in transgenic plants. Plant Cell 6: 1859–1876 (1994).Google Scholar
  22. 22.
    Lohmer S, Maddaloni M, DiFonzo N, Hartings H, Salamini F, Thompson RD: The maize regulatory locus Opaque-2 encodes a DNA-binding protein which activates the transcription of the b-32 gene. EMBO 10 J 3: 617–624 (1991).Google Scholar
  23. 23.
    Ma H, McMullen MD, Finer JJ: Identification of a homeobox-containing gene with enhanced expression during soybean (Glycine max L.) somatic embryo development. Plant Mol Biol 24: 465–473 (1994).Google Scholar
  24. 24.
    Matsuoka M, Ichikawa H, Saito A, Tada Y, Fujimura T, Kano-Marakami Y: Expression of a rice homeobox gene causes altered morphology of transgenic plants. Plant Cell 5: 1039–1048 (1993).Google Scholar
  25. 25.
    Mattsson J, Svenson E: A new homeobox-leucine zipper gene from Arabidopsis thaliana. Plant Mol Biol 18: 1019–1022 (1992).Google Scholar
  26. 26.
    McGinnis W, Levine MS, Hafen E, Kuroiwa A, Gehring WJ: A conserved DNA sequence in homeotic genes of the Drosophila Antennapedia and bithorax complexes. Nature 308: 428–433 (1984).Google Scholar
  27. 27.
    Miller AM, Mackay VL, Nasmyth KA: Identification and comparison of two sequence elements that confer cell-type specific transcription in yeast. Nature 314: 598–603 (1985).Google Scholar
  28. 28.
    Mitchell PJ, Tjian R: Transcriptional regulation in mammalian cells by sequence-specific DNA binding proteins. Science 245: 371–378 (1989).Google Scholar
  29. 29.
    Monica K, Galili N, Nourse J, Saltman D, Cleary ML: PBX2 and PBX3, new homeobox genes with extensive homology to the human proto-oncogene PBX1. Mol Cell Biol 11: 6149–6157 (1991).Google Scholar
  30. 30.
    Nasmyth KA, Tatchell K, Hall BD, Astell C, Smith M: A position effect in the control of transcription at yeast mating type loci. Nature 289: 244–250 (1981).Google Scholar
  31. 31.
    Nourse J, Mellentin JD, Galili N, Wilkinson J, Stanbridge E, Smith SD, Cleary ML: Chromosomal translocation t(1;19) results in synthesis of a homeobox fusion mRNA that codes for a potential chimeric transcription factor. Cell 60: 535–545 (1990).Google Scholar
  32. 32.
    Pruitt RE, Meyerowitz EM: Characterisation of the genome of Arabidopsis thaliana. J Mol Biol 187: 169–183 (1986).Google Scholar
  33. 33.
    Ptashne M: How eukaryotic transcriptional activators work. Nature 335: 683–689 (1988).Google Scholar
  34. 34.
    Rerie WG, Feldmann KA, Marks MD: The GLABRA2 gene encodes a homeodomain protein required for normal trichome development in Arabidopsis. Genes and Dev 8: 1388–1399 (1994).Google Scholar
  35. 35.
    Riddihough G: Homing in on the homeobox. Nature 357: 643–644 (1992).Google Scholar
  36. 36.
    Rogers S, Wells R, Rechstainer M: Amino acid sequences common to rapidly degraded proteins: The PEST hupothesis. Science 234: 364–368 (1986).Google Scholar
  37. 37.
    Ruberti I, Sessa G, Luchetti S, Morelli G: A novel class of plant proteins containing a homeodomain with a closely linked leucine zipper motif. EMBO J 7: 1787–1791 (1991).Google Scholar
  38. 38.
    Schena M, Davis RW: HD-Zip proteins: members of an Arabidopsis homeodomain protein superfamily. Proc Natl Acad Sci USA 89: 3894–3898 (1992).Google Scholar
  39. 39.
    Schena M, Lloyd AM, Davis RM: The HAT4 gene of Arabidopsis encodes a developmental regulator. Genes Dev 7: 367–379 (1993).Google Scholar
  40. 40.
    Scott MP, Weiner AJ: Structural relationships among genes that control development: sequence homology between Antennapedia, Ultrabithorax and fushi tarazu loci of Drosophila. Proc Natl Acad Sci USA 81: 4115–4119 (1984).Google Scholar
  41. 41.
    Smith LG, Greene B, Veit B, Hake S: A dominant mutation in the maize homeobox gene, Knotted-1, causes its ectopic expression in leaf cells with altered fates. Development 116: 21–30 (1992).Google Scholar
  42. 42.
    Steeves TA, Sussex IM: Patterns in plant development. 2nd ed. Cambridge: Cambridge University Press, 1 p (1989).Google Scholar
  43. 43.
    Valvekens D, VanMontague M, Lijsebettens MV: Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants by using kanamycin selection. Proc Natl Acad Sci USA 85: 5536–5540 (1988).Google Scholar
  44. 44.
    Vollbrecht E, Veit B, Sinha N, Hake S: The developmental gene Knotted-1 is a member of a maize homeobox gene family. Nature 350: 241–243 (1991).Google Scholar
  45. 45.
    Werner M, Feller A, Messenguy F, Pierard A: The leader peptide of yeast gene CPA1 is essential for the translational repression of its expression. Cell 49: 805–813 (1987).Google Scholar

Copyright information

© Kluwer Academic Publishers 1995

Authors and Affiliations

  • Jan Dockx
    • 1
  • Nicolette Quaedvlieg
    • 1
  • Gerbienne Keultjes
    • 1
  • Patricia Kock
    • 1
  • Peter Weisbeek
    • 1
  • Sjef Smeekens
    • 1
  1. 1.Department of Molecular Cell BiologyUniversity of UtrechtUtrechtThe Netherlands

Personalised recommendations