Skip to content
BY-NC-ND 3.0 license Open Access Published by De Gruyter Open Access June 1, 2006

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

  • Kai Müller EMAIL logo , Jinxing Lin , Rainer Fischer and Dirk Prüfer
From the journal Open Life Sciences

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.

[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. http://dx.doi.org/10.1046/j.1365-313X.1999.00457.x10.1046/j.1365-313X.1999.00457.xSearch in Google Scholar

[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. http://dx.doi.org/10.1038/350241a010.1038/350241a0Search in Google Scholar

[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. 405–413 Search in Google Scholar

[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. http://dx.doi.org/10.1105/tpc.6.12.187710.1105/tpc.6.12.1877Search in Google Scholar

[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. http://dx.doi.org/10.1007/s00427005016110.1007/s004270050161Search in Google Scholar

[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. http://dx.doi.org/10.1126/science.107034310.1126/science.1070343Search in Google Scholar

[7] T.A. Dickinson: “Epiphylly in angiosperms”, Bot. Rev., Vol. 44, (1978), pp. 181–232. http://dx.doi.org/10.1007/BF0291907910.1007/BF02919079Search in Google Scholar

[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. http://dx.doi.org/10.1023/A:100638412256710.1023/A:1006384122567Search in Google Scholar

[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. http://dx.doi.org/10.1105/tpc.12.11.214310.1105/tpc.12.11.2143Search in Google Scholar

[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. http://dx.doi.org/10.1073/pnas.07262609910.1073/pnas.072626099Search in Google Scholar

[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. http://dx.doi.org/10.1016/S0960-9822(02)00721-210.1016/S0960-9822(02)00721-2Search in Google Scholar

[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. http://dx.doi.org/10.1105/tpc.11.9.165110.1105/tpc.11.9.1651Search in Google Scholar

[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. http://dx.doi.org/10.1023/A:101073981283610.1023/A:1010739812836Search in Google Scholar

[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. http://dx.doi.org/10.1105/tpc.6.12.185910.1105/tpc.6.12.1859Search in Google Scholar

[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. http://dx.doi.org/10.1046/j.1365-313x.2001.01064.x10.1046/j.1365-313x.2001.01064.xSearch in Google Scholar

[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. http://dx.doi.org/10.1016/S0092-8674(00)81051-X10.1016/S0092-8674(00)81051-XSearch in Google Scholar

[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. http://dx.doi.org/10.1104/pp.102.01556010.1104/pp.102.015560Search in Google Scholar PubMed PubMed Central

[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. http://dx.doi.org/10.1038/374727a010.1038/374727a0Search in Google Scholar PubMed

[19] J.X. Lin and K.J. Müller: “Structure and development of epiphylly in knox-transgenic tobacco”, Planta, Vol. 214, (2002), pp. 521–525. http://dx.doi.org/10.1007/s00425010064810.1007/s004250100648Search in Google Scholar PubMed

[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. Search in Google Scholar

[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. Search in Google Scholar

[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. Search in Google Scholar

[23] M. Bevan: “Binary Agrobacterium vectors for plant transformation”, Nucl. Acid Res., Vol. 12, (1984), pp. 8711–8721. Search in Google Scholar

[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. http://dx.doi.org/10.1073/pnas.83.8.257110.1073/pnas.83.8.2571Search in Google Scholar PubMed PubMed Central

[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. http://dx.doi.org/10.1023/A:100642561995310.1023/A:1006425619953Search in Google Scholar

[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. http://dx.doi.org/10.1101/gad.112000310.1101/gad.1120003Search in Google Scholar PubMed PubMed Central

[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. Search in Google Scholar

[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. http://dx.doi.org/10.1105/tpc.11.8.141910.1105/tpc.11.8.1419Search in Google Scholar PubMed PubMed Central

[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. http://dx.doi.org/10.1104/pp.117.3.77110.1104/pp.117.3.771Search in Google Scholar PubMed PubMed Central

[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. http://dx.doi.org/10.1105/tpc.8.8.127710.1105/tpc.8.8.1277Search in Google Scholar PubMed PubMed Central

[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. Search in Google Scholar

[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. Search in Google Scholar

[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. http://dx.doi.org/10.1073/pnas.05248409910.1073/pnas.052484099Search in Google Scholar PubMed PubMed Central

Published Online: 2006-6-1
Published in Print: 2006-6-1

© 2006 Versita Warsaw

This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.

Downloaded on 24.4.2024 from https://www.degruyter.com/document/doi/10.2478/s11535-006-0012-8/html
Scroll to top button