Central European Journal of Biology

, Volume 1, Issue 2, pp 263–274 | Cite as

How repeated epiphylly correlates with gene expression of resident knox1 in the leaves of tobacco epiphyllous shoots

  • Kai J. Müller
  • Jinxing Lin
  • Rainer Fischer
  • Dirk Prüfer
Research Article
  • 29 Downloads

Abstract

The tobacco knox1 genes tokn1 and tokn2 were isolated and their neomorphic capacities were tested while expressed in tobacco and potato. In addition, their neomorphic capacities were compared to barley bkn3 transgenic plant material. While tokn2 and bkn3 induced epiphylly in tobacco and supercompound leaves in potato, tokn1 failed to produce such prominent knox1 specific phenotypes. In wild type tobacco, alleles of the tokn genes were found to be expressed within distinct zones of the shoot apical meristem (SAM), leaving out regions that correlated with leaf founder cells [1]. In contrast, the expression of the tokn genes was detected throughout the meristem and in leaf primordia of epiphyllous shoots that developed in tobacco over-expressing the barley hooded gene bkn3. It was determined that such extended expression domains of resident tobacco knox1 genes were mediated through an enhanced expression domain of bkn3 within the tissue confined to the epiphylls, and this contributed to “repeated epiphylly”, i.e. an iterated development of epiphyllous shoots on leaves of progenitor epiphylls.

Keywords

Leaf development epiphylly compound leaf plant unit iteration Hooded 

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References

  1. [1]
    A. Nishimura, M. Tamaoki, Y. Sato and M. Matsuoka: “The expression of tobacco knotted1-type class 1 homeobox genes corresponds to regions predicted by the cytohistological zonation model”, Plant J., Vol. 18, (1999), pp. 337–347.PubMedCrossRefGoogle Scholar
  2. [2]
    E. Vollbrecht, B. Veit, N. Sinha and S. Hake: “The developmental gene Knotted-1 is a member of a maize homeobox gene family”, Nature, Vol. 350, (1991), pp. 241–243.PubMedCrossRefGoogle Scholar
  3. [3]
    D. Jackson, B. Veit and S. Hake: “Expression of maize KNOTTED-1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot”, Development, Vol. 120, (1994), pp. 405–413Google Scholar
  4. [4]
    R. Kerstetter, E. Vollbrecht, B. Lowe, B. Veit, J. Yamaguchi and S. Hake: “Sequence analysis and expression patterns divide the maize knotted1-like homeobox genes into two classes”, Plant Cell, Vol. 6, (1994), pp. 1877–1887.PubMedCrossRefGoogle Scholar
  5. [5]
    T.R. Bürglin: “The PBC domain contains a MEINOX domain — Co-evolution of HOX and TALE homeobox genes”, Dev. Genes. Evol., Vol. 208, (1998), pp. 113–116.PubMedCrossRefGoogle Scholar
  6. [6]
    G. Bharathan, T.E. Goliber, C. Moore, S. Kessler, T. Pham and N.R. Sinha: “Homologies in leaf form inferred from KNOXI gene expression during development”, Science, Vol. 296, (2002), pp. 1858–1860.PubMedCrossRefGoogle Scholar
  7. [7]
    T.A. Dickinson: “Epiphylly in angiosperms”, Bot. Rev., Vol. 44, (1978), pp. 181–232.CrossRefGoogle Scholar
  8. [8]
    L. Reiser, P. Sanchez-Baracald and S. Hake: “Knots in the family tree: Evolutionary relationships and functions of knox homeobox genes”, Plant Mol. Biol., Vol. 42, (2000), pp. 151–166.PubMedCrossRefGoogle Scholar
  9. [9]
    H. Yu, H. Yang Shu and J. Goh Chong: “DOH1, a class 1 knox gene, is required for maintenance of the basic plant architecture and floral transition in orchid”, Plant Cell, Vol. 12, (2000), pp. 2143–2159.PubMedCrossRefGoogle Scholar
  10. [10]
    S.P. Venglat, T. Dumonceaux, K. Rozwadowski, L. Parnell, V. Babic, W. Keller, R. Martienssen, G. Selvaraj and R. Datla: “The homeobox gene BREVIPEDICELLUS is a key regulator of inflorescence architecture in Arabidopsis”, Proc. Nat. Acad. Sci. U.S.A., Vol. 99, (2002), pp. 4730–4735.CrossRefGoogle Scholar
  11. [11]
    J.F. Golz, E.J. Keck and E. Hudson: “Spontaneous mutations in KNOX genes give rise to a novel floral structure in Antirrhinum”, Current Biol., Vol. 12, (2002), pp. 515–522.CrossRefGoogle Scholar
  12. [12]
    N. Sentoku, Y. Sato, N. Kurata, Y. Ito, H. Kitano and M. Matsuoka: “Regional expression of the rice KN1-type homeobox gene family during embryo, shoot, and flower development”, Plant Cell, Vol. 11, (1999), pp. 1651–1663.PubMedCrossRefGoogle Scholar
  13. [13]
    J. Hofer, C. Gourlay, A. Michael and T.H.N. Ellis: “Expression of a class 1 knotted1-like homeobox gene is down-regulated in pea compound leaf primordia”, Plant Mol. Biol., Vol. 45, (2001), pp. 387–398.PubMedCrossRefGoogle Scholar
  14. [14]
    C. Lincoln, J. Long, J. Yamaguchi, K. Serikawa and S. Hake: “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, Vol. 6, (1994), pp. 1859–1876.PubMedCrossRefGoogle Scholar
  15. [15]
    J. Müller, Y.M. Wang, R. Franzen, L. Santi, F. Salamini and W. Rohde: “In vitro interactions between barley TALE homeodomain proteins suggest a role for protein-protein associations in the regulation of Knox gene function”, Plant J., Vol. 27, (2001), pp. 13–23.PubMedCrossRefGoogle Scholar
  16. [16]
    D. Hareven, T. Gutfinger, A. Parnis, Y. Eshed and E. Lifschitz: “The making of a compound leaf — genetic manipulation of leaf architecture in tomato”, Cell, Vol. 84, (1996), pp. 735–744.PubMedCrossRefGoogle Scholar
  17. [17]
    F.M. Rosin, J.K. Hart, H.T. Horner, P.J. Davies and D.J. Hannapel: “Overexpression of a knotted-like homeobox gene of potato alters vegetative development by decreasing gibberellin accumulation”, Plant Phys., Vol. 132, (2003), pp. 106–117.CrossRefGoogle Scholar
  18. [18]
    K.J. Müller, N. Romano, O. Gerstner, F. Garcia-Maroto, C. Pozzi, F. Salamini and W. Rohde: “The barley Hooded mutation caused by a duplication in a homeobox gene intron”, Nature, Vol. 374, (1995), pp. 727–730.PubMedCrossRefGoogle Scholar
  19. [19]
    J.X. Lin and K.J. Müller: “Structure and development of epiphylly in knox-transgenic tobacco”, Planta, Vol. 214, (2002), pp. 521–525.PubMedCrossRefGoogle Scholar
  20. [20]
    N.R. Sinha, R.E. Williams and S. Hake: “Overexpression of the maize homeobox gene, KNOTTED-1, causes a switch from determinate to indeterminate cell fates”, Genes & Dev., Vol. 7, (1993), pp. 787–795.Google Scholar
  21. [21]
    K.J. Müller: Die Homöoboxgene der Knox-Familie in Gerste (Hordeum vulgare L.): Molekulare Charakterisierung, transgene Expression und Assoziationsversuche mit homöotischen Mutationen, Thesis (Ph.D), University of Cologne, 1997.Google Scholar
  22. [22]
    R. Töpfer, V. Matzeit, B. Gronenborn, J. Schell and H.H. Steinbiss: “A set of plant expression vectors for transcriptional and translational fusions”, Nucleic Acids Res., Vol. 15, (1987), p. 5890.PubMedGoogle Scholar
  23. [23]
    M. Bevan: “Binary Agrobacterium vectors for plant transformation”, Nucl. Acid Res., Vol. 12, (1984), pp. 8711–8721.Google Scholar
  24. [24]
    R.B. Horsch, H.J. Klee, S. Stachel, S.C. Winans, E.W. Nester, S.G. Rogers and R.T. Fraley: “Analysis of Agrobacterium tumefaciens virulence mutants in leaf discs”, Proc. Natl. Acad. Sci. U.S.A., Vol. 83, (1986), pp. 2571–2575.PubMedCrossRefGoogle Scholar
  25. [25]
    J. Schmitz, R. Franzen, T.H. Ngyuen, F. Garcia-Maroto, C. Pozzi, F. Salamini and W. Rohde: “Cloning, mapping and expression analysis of barley MADS-box genes”, Plant Mol. Biol., Vol. 42, (2000), pp. 899–913.PubMedCrossRefGoogle Scholar
  26. [26]
    G. Mele, N. Ori, Y. Sato and S. Hake: “The knotted1-like homeobox gene BRE-VIPEDICELLUS regulates cell differentiation by modulating metabolic pathways”, Genes & Dev., Vol. 17, (2003), pp. 2088–2093.CrossRefGoogle Scholar
  27. [27]
    A. Nishimura, M. Tamaoki, T. Sakamoto and M. Matsuoka: “Over-expression of tobacco knotted1-type class1 homeobox genes alters various leaf morphology”, Plant Cell Physiol., Vol. 41, (2000), pp. 583–590.PubMedGoogle Scholar
  28. [28]
    T.A. Sakamoto, M. Nishimura, M. Tamaoki, H. Kuba, H. Tanaka, S. Iwahori and M. Matsuoka: “The conserved KNOX domain mediates specificity of tobacco KNOTTED1-type homeodomain proteins”, Plant Cell, Vol. 11, (1999), pp. 1419–1431.PubMedCrossRefGoogle Scholar
  29. [29]
    B.B. Janssen, L. Lund and N. Sinha: “Overexpression of a Homeobox Gene, LeT6, Reveals Indeterminate Features in the Tomato Compound Leaf”, Plant Phys., Vol. 117, (1998), pp. 771–786.CrossRefGoogle Scholar
  30. [30]
    G. Chuck, C. Lincoln and S. Hake: “KNAT1 induces lobed leaves with ectopic meristems when over-expressed in Arabidopsis”, Plant Cell, Vol. 8, (1996), pp. 1277–1289.PubMedCrossRefGoogle Scholar
  31. [31]
    M. Lenhard, G. Jürgens and T. Laux: “The WUSCHEL and SHOOTMERISTEMLESS genes fulfil complementary roles in Arabidopsis shoot meristem regulation”, Development, Vol. 129, (2002), pp. 3195–3206.PubMedGoogle Scholar
  32. [32]
    W.J. Lucas, S. Bouché-Pillon, D.P. Jackson, L. Nguyen, L. Baker, B. Ding and S. Hake: “Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata”, Science, Vol. 270, (1995), pp. 1980–1983.PubMedGoogle Scholar
  33. [33]
    J.Y. Kim, Z.A. Yuan, M. Cilia, Z. Khalfan-Jagani and D. Jackson: “Intercellular trafficking of a KNOTTED1 green fluorescent protein fusion in the leaf and shoot meristem of Arabidopsis”, Proc. Natl. Acad. Sci. U.S.A., Vol. 99, (2002), pp. 4103–4108.PubMedCrossRefGoogle Scholar

Copyright information

© Versita Warsaw and Springer-Verlag Berlin Heidelberg 2006

Authors and Affiliations

  • Kai J. Müller
    • 1
  • Jinxing Lin
    • 2
  • Rainer Fischer
    • 1
  • Dirk Prüfer
    • 3
  1. 1.Fraunhofer Institute for Molecular Biology and Applied Ecology (IME)AachenGermany
  2. 2.Institute of BotanyChinese Academy of SciencesBeijingChina
  3. 3.Institute for Biochemistry and Biotechnology of PlantsUniversity of MünsterMünsterGermany

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