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Identification of a homeobox-containing gene with enhanced expression during soybean (Glycine max L.) somatic embryo development

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Abstract

Homeotic genes are key ‘switches’ that control developmental processes. Homeotic genes containing the consensus ‘homeobox’ domain have been identified from a number of organisms including Drosophila melanogaster, Caenorhabditis elegans, Homo sapiens, and Zea mays. Although homeotic genes have been demonstrated to be important in embryo development of some insects, amphibians, and mammals, there are no reports of their involvement in plant embryogenesis. Here, we report the isolation and characterization of a cDNA clone for a homeobox-containing gene expressed in somatic embryos of soybean. The cDNA (Sbh1 for soybean homeobox-containing gene) was isolated using maize Knotted-1 (Kn1) cDNA as a heterologous probe. The Sbh1 cDNA clone is 1515 bp long which is the approximate size of its transcript. Within the homeodomain, the amino acid sequence of a helix-turn-helix structure, and invariant and conserved residues were identified. The deduced SBH1 protein shares a high amino acid identity with KN1 protein (47.0% overall and 87.5% for the homeodomain). Southern hybridization analysis indicated that Sbh1 is a member of a small gene family. The expression of Sbh1 is development-and tissue-specific. The transcript of Sbh1 was present in early-stage somatic embryos, increased prior to cotyledon formation and decreased thereafter. Sbh1 was weakly expressed in soybean stems and hypocotyl but was not detected in other plant tissues and nonembryogenic materials. The enhanced expression during embryogenesis, the homology with maize Kn1 gene, and the regulatory nature of homeodomain proteins suggest that the SBH1 protein plays an important role in plant embryo development.

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References

  1. Aviv H, Leder P: Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc Natl Acad Sci USA 69: 1408–1412 (1972).

    PubMed  Google Scholar 

  2. Bellmann 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).

    PubMed  Google Scholar 

  3. Benton WD, Davis RW: Screening λgt recombinant clones by hybridization to single plaques in situ. Science 196: 180–182 (1977).

    PubMed  Google Scholar 

  4. Bürglin TR, Finney M, Coulson A, Ruvkun G: Caenorhabditis elegans has scores of homeobox-containing genes. Nature 341: 239–243 (1989).

    Article  PubMed  Google Scholar 

  5. Chasan R: In the realm of the homeodomain. Plant Cell 4: 237–240 (1992).

    Article  PubMed  Google Scholar 

  6. Davis LG, Dibner MD, Batty JF: Basic Methods in Molecular Biology. Elsevier Science Publishing, New York (1986).

    Google Scholar 

  7. Feinberg AP, Vogelstein B: A technique for radiolabelling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132: 6–13 (1983).

    PubMed  Google Scholar 

  8. Finer JJ, McMullen MD: Transformation of soybean via particle bombardment of embryogenic suspension culture tissue. In Vitro Cell Devel Biol 27: 175–182 (1991).

    Google Scholar 

  9. Finer JJ, Nagasawa A: Development of an embryogenic suspension culture of soybean [Glycine max (L.) Merrill.]. Plant Cell Tissue Organ Cult 15: 125–136 (1988).

    Google Scholar 

  10. Gehring WJ: The homeobox in perspective. Trends Biotechnol Sci 17: 277–280 (1992).

    Article  Google Scholar 

  11. Gehring WJ, Hiromi Y: Homeotic genes and the Homeobox. Annu Rev Genet 20: 147–173 (1986).

    Article  PubMed  Google Scholar 

  12. Hinnebusch AG: Mechanisms of gene regulation in the general control of amino acid biosynthesis in Saccharomyces cerevisiae. Microbiol Rev 52: 248–273 (1988).

    PubMed  Google Scholar 

  13. Joyner AL, Martin GR: En-1 and En-2, two mouse genes with sequence homology to the Drosophila engrailed gene: expression during embryogenesis. Genes Devel 1: 29–38 (1987).

    PubMed  Google Scholar 

  14. 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).

    PubMed  Google Scholar 

  15. Kempter B, Luppa P, Neumeier D: A short procedure for Southern blotting on neutral and anionic membranes. Trends Genet 7: 109–110 (1991).

    Article  Google Scholar 

  16. Kissinger CR, Liu B, Martin-Blanco E, Kornberg TB, Pabo CO: Crystal structure of an engrailed homeodomai-DNA complex at 2.8 Å resolution: a framework for understanding homeodomain-DNA interactions. Cell 63: 579–590 (1990).

    Article  PubMed  Google Scholar 

  17. Kozak M: An analysis of 5′-noncoding sequences from 699 vertebrate messenger RNAs. Nucl Acids Res 15: 8125–8148 (1987).

    PubMed  Google Scholar 

  18. Kozak M: The scanning model for translation: An update. Cell Biol 108: 229–241 (1989).

    Article  PubMed  Google Scholar 

  19. Lohmer S, Maddaloni M, Motto M, Salamini F, Thompson RD: Translation of the mRNA of the maize transcriptional activator Opaque-2 is inhibited by upstream open reading frames present in the leader sequence. Plant Cell 5: 65–73 (1993).

    Article  PubMed  Google Scholar 

  20. Mattsson J, Söderman E, Svenson M, Borkird C, Engström P: A new homeobox-leucine zipper gene from Arabidopsis thaliana. Plant Mol Biol 18: 1019–1022 (1992).

    PubMed  Google Scholar 

  21. McGinnis W, Levine MS, Hafen E, Kuroiwa A, Gehring WJ: A conserved DNA sequence in homeotic genes of the Drosophila antennapedia and biothorax complexes. Nature 308: 428–433 (1984).

    PubMed  Google Scholar 

  22. Meinke DW: Embryonic mutants of Arabidopsis thaliana Devel Genet 12: 382–392 (1991).

    Google Scholar 

  23. 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).

    PubMed  Google Scholar 

  24. 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).

    PubMed  Google Scholar 

  25. 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).

    PubMed  Google Scholar 

  26. Ptashne M: How eukaryotic transcriptional activators work. Nature 335: 683–689 (1988).

    Article  PubMed  Google Scholar 

  27. Qian YQ, Billeter M, Otting G, Müller M, Gehring WJ, Wüthrich K: The structure of the Antennapedia homeodomain determined by NMR spectroscopy in solution: comparison with prokaryotic repressors. Cell 59: 573–580 (1989).

    PubMed  Google Scholar 

  28. Ruberti I, Sessa G, Lucchetti S, Morelli G: A novel class of plant proteins containing a homeodomain with a closely linked leucine zipper motif. EMBO J 10: 1787–1791 (1991).

    PubMed  Google Scholar 

  29. Saghai-Maroof MA, Soliman KM, Jorgensen RA, Allard RW: Ribosomal DNA spacer-length polymorphisms in barley: Mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci USA 81: 8014–8018 (1984).

    PubMed  Google Scholar 

  30. Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual, 2nd ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).

    Google Scholar 

  31. Schena M, Davis RW: HD-Zip proteins: Members of an Arabidopsis homeodomain protein superfamily. Proc Natl Acad Sci USA 89: 3894–3898 (1992).

    PubMed  Google Scholar 

  32. Scott MP, Tamkun JW, HartzellIII GW: The structure and function of the homeodomain. Biochim Biophys Acta 989: 25–48 (1989).

    PubMed  Google Scholar 

  33. Scott MP, Weiner AJ: Structural relationship among genes that control development: Sequence homology between the Antennapedia, Ultrabithorax, and fushi tarazu loci of Drosophila. Proc Natl Acad Sci USA 81: 4115–4119 (1984).

    PubMed  Google Scholar 

  34. Thomas PS: Hybridization of denatured RNA transferred or dotted to nitrocellulose paper. Meth Enzymol 100: 255–266 (1983).

    PubMed  Google Scholar 

  35. Vieira J, Messing J: Production of single-stranded plasmid DNA. Meth Enzymol 153: 3–11 (1987).

    PubMed  Google Scholar 

  36. Vollbrecht E, Kerstetter R, Lowe B, Veit B, Hake S: Homeobox genes in plant development: mutational and molecular analysis. In Spradling AC (ed), Evolutionary Conservation of Developmental Mechanisms, pp. 111–123. Wiley-Liss, New York (1993).

    Google Scholar 

  37. 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).

    PubMed  Google Scholar 

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Author notes

  1. Michael D. McMullen

    Present address: USDA-ARS, University of Missouri, Room 301 Curtis Hall, 65211, Columbia, MO, USA

Authors and Affiliations

  1. Corn and Soybean Research Unit, USDA-Agricultural Research Service, 44691, Wooster, OH, USA

    Michael D. McMullen

Authors
  1. Hongchang Ma
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  2. Michael D. McMullen
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  3. John J. Finer
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Department of agronomy, The Ohio State University

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Ma, H., McMullen, M.D. & Finer, J.J. Identification of a homeobox-containing gene with enhanced expression during soybean (Glycine max L.) somatic embryo development. Plant Mol Biol 24, 465–473 (1994). https://doi.org/10.1007/BF00024114

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  • DOI: https://doi.org/10.1007/BF00024114

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