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A new class of plant homeobox genes is expressed in specific regions of determinate symbiotic root nodules

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Abstract

A cDNA containing a homeobox sequence was isolated from a soybean nodule-specific expression library. This homeobox cDNA, Ndx (nodulin homeobox), represents a small gene family with at least two members in soybean (Glycine max) and three in Lotus japonicus. One complete 3304 bp Ndx cDNA from L. japonicus encodes a protein, NDX, of 958 amino acids. An unusual type of homeodomain that differs in two of the most conserved amino acid positions in the consensus sequence is located close to the C-terminal and appears to be the only DNA-binding domain. Weak Ndx gene expression in the root increases very shortly after infection with Rhizobium and remains throughout nodule development. In situ hybridizations show cell-specific expression patterns that suggest developmentally separate regions in maturing determinate nodules. Thus in the maturing nodule Ndx and leghemoglobin genes are expressed in a mutually exclusive fashion. The Ndx transcript is also detectable in the young nodule primordium. Ndx expression is not confined to the root nodule since Ndx is also expressed in shoot and root meristems, indicating that the Ndx gene products might also be involved in developmental processes in other plant tissues.

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References

  1. Aoyama T, Dong CH, Wu Y, Carabelli M, Sessa G, Ruberti I, Morelli G, Chua NH: Ectopic expression of the Arabidopsis transcriptional activator Athb-1 alters leaf cell fate in tobacco. Plant Cell 7: 1773–1785 (1195).

    Google Scholar 

  2. Ausubel JP, Brent R, Kingson RE, Moore DD, Seidman JG, Smith JA, Struhl K: Current Protocols in Molecular Biology. Wiley, New York (1994).

    Google Scholar 

  3. Bauer P, Poirier S, Ratet P, Kondorosi A: MsEnod12A expression is linked to meristematic activity during development of indeterminate and determinate nodules and roots. Mol Plant-Microbe Interact 10: 39–49 (1997).

    Google Scholar 

  4. Becraft PW, Freeling M: Genetic analysis of Rough sheath1 developmental mutants of maize. Genetics 136: 295–311 (1994).

    Google Scholar 

  5. Bellmann R, Werr W: Zmhox1a, 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 

  6. Benson M, Pirrotta V: The product of the Drosophila zeste gene binds to specific DNA sequences in white and Ubx. EMBO J 6: 1387–1392 (1987).

    Google Scholar 

  7. Benson M, Pirrotta V: The Drosophila zeste protein binds cooperatively to sites in many gene regulatory regions: implications for transvection and gene regulation. EMBO J 7: 3907-3915 (1988).

    Google Scholar 

  8. Carabelli M, Morelli G, Whitelam G, Ruberti I: Twilight-zone and canopy shade induction of the Athb-2 homeobox gene in green plants. Proc Natl Acad Sci USA 93: 3530-3535 (1996).

    Google Scholar 

  9. Carabelli M, Sessa G, Baima S, Morelli G, Ruberti I: The Arabidopsis Athb-2 and -4 genes are strongly induced by far-red-rich light. Plant J: 4: 469–479 (1993).

    Google Scholar 

  10. Chen JD, Chan CS, Pirrotta V: Conserved DNA binding and self-association domains of the Drosophila zeste protein. Mol Cell Biol 12: 598–608 (1992).

    Google Scholar 

  11. Chen JD, Pirrotta V: Multimerization of the Drosophila zeste protein is required for efficient DNA binding. EMBO J 12: 2075–2083 (1993).

    Google Scholar 

  12. Christiansen H, Hansen AC, Vijn I, Pallisgaard N, Larsen K, Yang WC, Bisseling T, Marcker KA, Jensen EO: A novel type of DNA-binding protein interacts with a conserved sequence in an early nodulin ENOD12 promoter. PlantMol Biol 2: 809–821 (1996).

    Google Scholar 

  13. Duboule D: Guidebook to the Homeobox Genes. Sambrook and Tooze Publication. Oxford University Press, Oxford, UK (1994).

    Google Scholar 

  14. Gehring WJ: Homeoboxes in the study of development. Science 236: 1245–1252 (1987).

    Google Scholar 

  15. Gehring WJ, Qian YQ, Billetter M, Furukubo-Tokunaga K, Schier AF, Resendez-Perez D, Affolter M, Gottfried O, Wütrich K: Homeodomain-DNA recognition. Cell 78: 211–223 (1994).

    Google Scholar 

  16. Handberg K, Stougaard J: Lotus japonicus, an autogamous, diploid legume species for classical and molecular genetics. Plant Cell 3: 487–496 (1992).

    Google Scholar 

  17. Heidstra R, Nilsen G, Martinez-Abarca F, van Kammen A, Bisseling T: Nod factor-induced expression of leghemoglobin to study the mechanism of NH4NO3 inhibition on root hair deformation. Mol Plant-Microbe Interact 10: 215–220 (1997).

    Google Scholar 

  18. Hyldig-Nielsen JJ, Jensen EØ, Paludan K, Wiborg O, Garett R, Jørgensen P, Marcker KA: The primary structure of two leghemoglobin genes from soybean. Nucl Acids Res 10: 689–701 (1982).

    Google Scholar 

  19. Jackson D, Veit B, Hake S: Expression of maize KNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development 120: 405–413 (1994).

    Google Scholar 

  20. Jensen EØ, Pallisgaard N, Christiansen H, Vijn I, Bisseling T, Gronbaek M, Jørgensen J-E, Larsen K, Hansen AC, Mielczarek M, Sniezko I, Marcker KA: Identification of transacting factors regulating nodulin gene expression. In: Legocki A, Bothe B, Pühler A <nt>(eds)</nt> Biological Fixation of Nitrogen for Ecology and Sustainable Agriculture. Springer-Verlag, Berlin/Heidelberg (1997).

    Google Scholar 

  21. Jones RS, Gelbart WM: Genetic analysis of the enhancer of zeste locus and its role in gene regulation in Drosophila melanogaster. Genetics 126: 185–199 (1990).

    Google Scholar 

  22. Jørgensen JE, Stougaard J, Marcker KA: A two-component nodule-specific enhancer in the soybean N23 gene promoter. Plant Cell 3: 819–827 (1991).

    Google Scholar 

  23. Kappen C, Schughart K, Ruddle FH: Early evolutionary origin of major homeodomain sequence classes. Genomics 18: 54-70 (1993).

    Google Scholar 

  24. Kerstetter R, Vollbrecht E, Lowe B, Veit B, Yamaguchi J, Hake S: Sequence analysis and expression patterns divide the maize knotted1-like homeobox genes into two classes. Plant Cell 6: 1877–1887 (1994).

    Google Scholar 

  25. Klinge B, Werr W: Transcription of the Zea mays homeobox (ZmHox) genes is activated early in embryogenesis and restricted to meristems of the maize plant. Devel Genet 16: 349–357 (1995).

    Google Scholar 

  26. Laney JD, Biggin MD: Zeste-mediated activation by an enhancer is independent of cooperative DNA binding in vivo. Proc Natl Acad Sci USA 94: 3602–3604 (1997).

    Google Scholar 

  27. 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 

  28. Long JA, Moan EI, Medford JI, Barton MK: A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379: 66–69 (1996).

    Google Scholar 

  29. Lu P, Porat R, Nadeau JA, O'Neill SD: 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 8: 2155–2168 (1996).

    Google Scholar 

  30. Lucas WJ, Bouche-Pillon S, Jackson DP, Nguyen L, Baker L, Ding B, Hake S: Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata [see comments]. Science 270: 1980–1983 (1995).

    Google Scholar 

  31. Mansukhani A, Crickmore A, Sherwood PW, Goldberg ML: DNA-binding properties of the Drosophila melanogaster zeste gene product. Mol Cell Biol 8: 615–623 (1988).

    Google Scholar 

  32. Marcker A Lund M Jensen EØ, Marcker KA: Transcription of the soybean leghemoglobin genes during nodule development. EMBO J 3: 1691–1695 (1984).

    Google Scholar 

  33. Masucci JD,' Rerie WG, Foreman DR, Zhang M, Galway ME, Marks MD, Schiefelbein JW: The homeobox gene GLABRA2 is required for position-dependent cell differentiation in the root epidermis of Arabidopsis thaliana. Development 122: 1253–1260 (1996).

    Google Scholar 

  34. Masucci JD et al.: Hormones act downstream of TTGand GL2 to promote root hair outgrowth during epidermis development in the Arabidopsis root. Plant Cell 8: 1505–1517 (1996).

    Google Scholar 

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

    Google Scholar 

  36. Meyerowitz E: In situ hybridization to RNA in plant tissue. Plant Mol Biol Rep 5: 242–250 (1985).

    Google Scholar 

  37. Modrusan Z, Reiser L, Feldmann KA, Fischer RL, Haughn GW: Homeotic transformation of ovules into carpel-like structures in Arabidopsis. Plant Cell 6: 333–349 (1994).

    Google Scholar 

  38. Müller KJ, Romano N, Gerstner O, Garcia-Maroto F, Pozzi C, Salamini F, Rohde W: The barley Hooded mutation caused by a duplication in a homeobox gene intron. Nature 374: 727–730 (1995).

    Google Scholar 

  39. Nasmyth KA, Tachell K., Hall BD, Astell C, Smith M: Physical analysis of mating-type loci in S. cerevisiae. Nature 289: 244–250 (1981).

    Google Scholar 

  40. Nielsen AL, Pallisgaard N, Pedersen FS, Jørgensen P: Murine helix-loop-helix transcriptional activator proteins binding to the E-box motif of the Akv murine leukemia virus enhancer identified by cDNA cloning. Mol Cell Biol 12: 3449–3459 (1992).

    Google Scholar 

  41. Pallisgaard N, Pedersen FS, Birkelund S, Jørgensen P: A common multiple cloning site in a set of vectors for expression of eukaryotic genes in mammalian, insect and bacterial cells. Gene 138: 115–118 (1994).

    Google Scholar 

  42. Patriarca EJ, Taté R, Fedorova E, Riccio A, Defez R, Iaccarino M: Down-regulation of the Rhizobium ntr system in the determinate nodule of Phaseolus vulgaris identifies a specific developmental zone. Mol Plant-Microbe Interact 9: 243–251 (1996).

    Google Scholar 

  43. Perego M, Higgins CF, Pearce SR, Gallagher MP, Hoch JA: The oligopeptide transport system of Bacillus subtilis plays a role in the initiation of sporulation. Mol Microbiol 5: 173–185 (1991).

    Google Scholar 

  44. Pirrotta V, Manet E, Hardon E, Bickel SE, Benson M: Structure and sequence of the Drosophila zeste gene. EMBO J 6: 791–799 (1987).

    Google Scholar 

  45. Qian S, Varjavand B, Pirrotta V: Molecular analysis of the zeste-white interaction reveals a promoter-proximal element essential for distant enhancer-promoter communication. Genetics 131: 79–80 (1992).

    Google Scholar 

  46. Quaedvlieg N, Dockx J, Rook F, Weisbeek P, Smeekens S: The homeobox gene ATH1 of Arabidopsis is derepressed in the photomorphogenic mutants cop1 and det1. Plant Cell 7: 117–129 (1995).

    Google Scholar 

  47. Ramlov KB, Laursen NB, Stougaard J, Marcker KA: Sitedirected mutagenesis of the organ-specific element in the soybean leghemoglobin Ibc3 gene promoter. Plant J 4: 577–580 (1993).

    Google Scholar 

  48. Reiser L, Modrusan Z, Margossian L, Samach A, Ohad N, Haughn GW, Fischer RL: The BELL1 gene encodes a homeodomain protein involved in pattern formation in the Arabidopsis ovule primordium. Cell 83: 735–742 (1995).

    Google Scholar 

  49. Rerie WG, Feldmann KA, Marks MD: The GLABRA2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis. Genes Dev 8: 1388–1399 (1994).

    Google Scholar 

  50. 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).

    Google Scholar 

  51. Schena M, Davis RW: Structure of homeobox-leucine zipper genes suggests amodel for the evolution of gene families. Proc Natl Acad Sci USA 91: 8393–8397 (1994).

    Google Scholar 

  52. Schena M, Davies RW: HD-Zip proteins: members of an Arabidopsis homeodomain protein superfamily. Plant Mol Biol 18: 1019–1022 (1992).

    Google Scholar 

  53. Schindler U, Beckmann H, Cashmore AR: HAT3.1, a novel Arabidopsis homeodomain protein containing a conserved cysteine-rich region. Plant J 4: 137–150 (1993).

    Google Scholar 

  54. Schneeberger RG, Becraft PW, Hake S, Freeling M: Ectopic expression of the knox homeo box gene rough sheath1 alters cell fate in the maize leaf. Genes Dev 9: 2292–2304 (1995).

    Google Scholar 

  55. Schummer M, Scheurlen I, Schaller C, Galliot B: HOMHOX genes are present in hydra Chlorohydra viridissima and are differentially expressed during regeneration. EMBO J 11: 1815–1823 (1992).

    Google Scholar 

  56. Söderman E, Mattsson J, Svenson M, Borkird C, Engstrom P: Expression patterns of novel genes encoding homeodomain leucine-zipper proteins in Arabidopsis thaliana. Plant Mol Biol 26: 145-154 (1994).

    Google Scholar 

  57. Stougaard J, Jørgensen JE, Christensen T, Kuhle A, Marcker KA: Interdependence and nodule specificity of cis-acting regulatory elements in the soybean leghemoglobin Ibc3 and N23 gene promoters. Mol Gen Genet 220: 353–360 (1990).

    Google Scholar 

  58. Tanda S et al. Retrotransposon-induced overexpression of a homeobox gene causes defects in eye morphogenesis in Drosophila. EMBO J 10: 407–417 (1991).

    Google Scholar 

  59. Vollbrecht E, Veit B, Sinha N, Hake S: The developmental gene Knotted-1 is amember of amaize homeobox gene family. Nature 350: 241–243 (1991).

    Google Scholar 

  60. Wiborg O, Hyldig-Nielsen JJ, Jensen EØ, Paludan K, Marcker K: The nucleotide sequences of two leghemoglobin genes from soybean. Nucl Acids Res 10: 3487–3494 (1982).

    Google Scholar 

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Authors and Affiliations

  1. Laboratory of Gene Expression, Department of Molecular and Structural Biology, University of Aarhus, Gustav Wiedsvej 10, 8000, Aarhus C, Denmark

    Jan-Elo Jørgensen, Mette Grønlund, Niels Pallisgaard, Knud Larsen, Kjeld A. Marcker & Erik østergaard Jensen

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  1. Jan-Elo Jørgensen
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  2. Mette Grønlund
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Jørgensen, JE., Grønlund, M., Pallisgaard, N. et al. A new class of plant homeobox genes is expressed in specific regions of determinate symbiotic root nodules. Plant Mol Biol 40, 65–77 (1999). https://doi.org/10.1023/A:1026463506376

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