Abstract
ATHB13 is a new member of the homeodomain leucine zipper (HDZip) transcription factor family of Arabidopsis thaliana. Constitutive high-level expression of the ATHB13 cDNA in transgenic plants results in altered development of cotyledons and leaves, specifically in plants grown on media containing metabolizable sugars. Cotyledons and leaves of sugar-grown transgenic plants are more narrow and the junction between the petiole and the leaf blade less distinct, as compared to the wild type. High-level expression of ATHB13 affects cotyledon shape by inhibiting lateral expansion of epidermal cells in sugar-treated seedlings. Experiments with non-metabolizable sugars indicate that the alteration in leaf shape in the ATHB13 transgenics is mediated by sucrose sensing. ATHB13 further affects a subset of the gene expression responses of the wild-type plant to sugars. The expression of genes encoding β-amylase and vegetative storage protein is induced to higher levels in response to sucrose in the transgenic plants as compared to the wild type. The expression of other sugar-regulated genes examined is unaffected by ATHB13. These data suggest that ATHB13 may be a component of the sucrose-signalling pathway, active close to the targets of the signal transduction.
Similar content being viewed by others
References
Altmann, T. 1998. Recent advances in brassinosteroid molecular genetics. Curr. Opin. Plant Biol. 1: 378–383.
Aso, K., Kato, M., Banks, J.A. and Hasebe, M. 1999. Characterisation of homeodomain-leucine zipper genes in the fern Ceratopteris richardi and the evolution of homeodomain-leucine zipper gene family in vascular plants. Mol. Biol. Evol. 16: 544–552.
Baima, S., Nobili, F., Sessa, G., Lucchetti, S., Ruberti, I. and Morelli, G. 1995. The expression of the Athb-8 homeobox gene is restricted to provascular cells in Arabidopsis thaliana. Development 121: 4171–4182.
Baumann, E., Lewald, J., Saedler, H., Schulz, B. and Wisman, E. 1998. Successful PCR-based reverse genetic screens using a En-1-mutagenised Arabidopsis thaliana population generated via single seed descent. Theor. Appl. Genet. 97: 729–734.
Bechtold, N., Ellis, J. and Pelletier, G. 1993. In planta Agrobacterium mediated transfer by infiltration of adult Arabidopsis thaliana plants. C.R. Acad. Sci. Paris 316: 1194–1199.
Berger, S., Bell, E., Sadka, A. and Mullet, J.E. 1995. Arabidopsis thaliana Atvsp is homologous to soybean VspA and VspB, genes encoding vegetative storage protein acid phosphatases and is regulated similarly by methyl jasmonate, wounding, sugars, light and phosphate. Plant Mol. Biol. 27: 933–942.
Carabelli, M., Sessa, G., Baima, S., Morelli, G. and Ruberti, I. 1993. The Arabidopsis Athb-2 and -4 genes are strongly induced by far-red-rich light. Plant J. 4: 469–479.
Chan, R.L. and Gonzalez, D.H. 1994. A cDNA encoding an HD-zip protein from sunflower. Plant Physiol. 106: 1687–1688.
Chang, S., Pyryear, J. and Cairney, J. 1993. A simple and efficient method for isolating RNA from pine trees. Plant Mol. Biol. Rep. 11: 113–116.
Cheng, C.L., Acedo, G.N., Cristinsin, M. and Conkling, M.A. 1992. Sucrose mimics the light induction of Arabidopsis nitrate reductase gene transcription. Proc. Natl. Acad. Sci. USA 89: 1861–1864.
Church, G.M. and Gilbert, W. 1984. Genomic sequencing. Proc. Natl. Acad. Sci. USA 81: 1991–1995.
Crawford, N.M., Smith, M., Bellissimo, D. and Davis, R.W. 1988. Sequence and nitrate regulation of the Arabidopsis thaliana mRNA encoding nitrate reductase, a metalloflavoprotein with three functional domains. Proc. Natl. Acad. Sci. USA 85: 5006–5010.
Di-Cristina, M., Sessa, G., Dolan, L., Linstead, P., Baima, S., Ruberti, I. and Morelli, G. 1996. The Arabidopsis Athb-10 (GLABRA2) is an HD-zip protein required for regulation of root hair development. Plant J. 10: 393–402.
Dijkwel, P.P., Huijser, C., Weisbeek, P.J., Chua, N.H. and Smeekens, S.C.M. 1997. Sucrose control of phytochrome A signaling in Arabidopsis. Plant Cell 9: 583–595.
Dijkwel, P.P., Kock, P.A.M., Bezemer, R., Weisbeek, P.J. and Smeekens, S.C.M. 1996. Sucrose represses the developmentally controlled transient activation of plastocyanin gene in Arabidopsis thaliana seedlings. Plant Physiol. 110: 455–463.
Double, D. 1994. Guidebook to Homeobox Genes, Oxford University Press, Oxford.
Elomaa, P., Homkanen, J., Puska, R., Seppänen, P., Helariutta, Y., Mehto, M., Kotilainen, M., Nevaleinen, L. and Teeri, T.H. 1993. Agrobacterium-mediated transfer of antisense chalcone synthase cDNA to Gerbera hybrida inhibits flower pigmentation. Bio/technology 11: 508–511.
Feinbaum, R.L. and Ausubel, F.M. 1988. Transcriptional regulation of the Arabidopsis thaliana chalcone synthase gene. Mol. Cell Biol. 8: 1985–1992.
Frank, W., Phillips, J., Salamini, F. and Bartels, D. 1998. Two dehydration-inducible transcripts from the resurrection plant Craterostigma plantagineum encode interacting homeodomain-leucine zipper proteins. Plant J. 15: 413–421.
Garber, R.L., Kuroiwa, A. and Gehring, W.J. 1983. Genomic and cDNA clones of the homeotic locus Antennapedia in Drosophila. EMBO J. 2: 2027–2036.
Halford, N.G. and Hardie, D.G. 1998. SNF1-related protein kinases: global regulators of carbon metabolism in plants? Plant Mol. Biol. 37: 735–748.
Hattori, T., Nakagawa, S. and Nakamura, K. 1990. High-level expression of tuberous root storage protein genes of sweet potato in stems of plantlets grown in vitro on sucrose medium. Plant Mol. Biol. 14: 595–604.
Hauser, M.T., Morikami, A. and Benfey, P.N. 1995. Conditional root expansion mutants of Arabidopsis. Development 121: 1237–1252.
Jang, J.C. and Sheen J. 1997. Sugar sensing in higher plants. Trends Plant Sci. 2: 208–214.
Jang, J.C., Leon, P., Zhou, L. and Sheen, J. 1997. Hexokinase as a sugar sensor in higher plants. Plant Cell 9: 5–19.
Johannesson, H., Wang, Y. and Engström, P. 2000. DNA-binding and dimerisation preferences of Arabidopsis homeodomain-leucine zipper transcription factors in vitro.Plant Mol. Biol., in press.
Karlin-Neumann, G.A., Sun, L. and Tobin, E. 1988. Expression of light-harvesting chlorophyll a/b-protein genes is phytochrome-regulated in etiolated Arabidopsis thaliana seedlings. Plant Physiol. 88: 1323–1331.
Kawahara, R., Komamine, A. and Fukuda, H. 1995. Isolation and characterisation of homeobox-containing genes of carrot. Plant Mol. Biol. 27: 155–164.
Kim, G.T., Tsukaya, H. and Uchimiya, H. 1998. The ROTUNDIFOLIA3 gene of Arabidopsis thaliana encodes a new member of the cytochrome P-450 family that is required for the regulated polar elongation of leaf cells. Genes Dev. 12: 2381–2391.
Koch, K.E. 1996. Carbohydrate-modulated gene expression in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 509–540.
Kubo, H., Peeters, A.J. M., Arts, M.G.M., Pereira, A. and Koornneef, M. 1999. ANTHOCYANINLESS2, a homeobox gene affecting anthocyanin distribution and root development in Ara-bidopsis. Plant Cell 11: 1217–1226.
Lee, Y.H. and Chun, J.Y. 1998. A new homeodomain-leucine zipper gene from Arabidopsis thaliana induced by water stress and abscisic acid treatment. Plant Mol. Biol. 37: 377–384.
Lister, C. and Dean. C. 1993. Recombinant inbred lines for mapping RFLP and phenotypic markers in Arabidopsis thaliana. Plant J. 4: 745–750.
Liu, X.J., Prat, S., Willmitzer, L. and Frommer, W.B. 1990. cis regulatory elements directing tuber-specific and sucrose-inducible expression of a chimeric class I patatin promoter/GUS-gene fusion. Mol. Gen. Genet. 223: 401–406.
Lu, P., Porat R., Nadeau, J.A. and O'Neill, S.D. 1996. 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.
Malamy, J.E. and Benfey, P.N. 1997. Organisation and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124: 33–44.
Martin, T., Hellmann, H., Schmidt, R., Willmitzer, L. and Frommer, W.B. 1997. Identification of mutants in metabolically regulated gene expression. Plant J. 11: 53–62.
Mason, H.S., Dewald, D.B., Creelman, R.A. and Mullet, J.E. 1992. Coregulation of soybean vegetative storage protein gene expression by methyl jasmonate and soluble sugars. Plant Physiol. 98: 859–867.
Mattsson, J. 1995. Homeobox genes in plants. Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 140, Uppsala, Acta Universitas Upsalaiensis.
Mattsson, J., Söderman, E., Svenson, M., Borkird, C. and Engström, P. 1992. A new homeobox-leucine zipper gene from Arabidopsis thaliana. Plant Mol. Biol. 18: 1019–1022.
McGinnis, W., Levine, M.S., Hafen, E., Kuroiwa, A. and Gehring, W.J. 1984. A conserved DNA sequence in homoeotic genes of the Drosophila Antennapedia and bithorax complexes. Nature 308: 428–433.
Meijer, A.H., Scarpella, E., van Dijk, E.L., Qin, L., Taal, A.J., Rueb, S., Harrington, S.E., McCouch, S.R., Schilperoort, R.A. and Hoge, J.H. 1997. Transcriptional repression by Oshox1, a novel homeodomain leucine zipper protein from rice. Plant J. 11: 263–276.
Meissner, R. and Theres, K. 1995. Isolation and characterization of the tomato homeobox gene THOM1. Planta 195: 541–547.
Mita, S., Hirano, H. and Nakamura, K. 1997a. Negative regulation in the expression of a sugar-inducible gene in Arabidopsis thaliana: a recessive mutation causing enhanced expression of a gene for β-amylase. Plant Physiol. 114: 575–582.
Mita, S., Murano, N., Akaike, M. and Nakamura, K. 1997b. Mutants of Arabidopsis thaliana with pleiotropic effects on the expression of the gene for β-amylase and on the accumulation of anthocyanin that are inducible by sugars. Plant J.11: 841–851.
Mita, S., Suzuki-Fujii, K. and Nakamura, K. 1995. Sugar-inducible expression of a gene for β-amylase in Arabidopsis thaliana. Plant Physiol. 107: 895–904.
Moon, Y.H., Choi, D., Kim, J.C., Han, T.J., Cho, S.H., Kim, W.T. and Lee, K.W. 1996. Isolation and characterisation of a homeodomain leucine zipper gene, Gmh1, from soybean somatic embryo. Mol. Cells 6: 366–373.
Muranaka, T., Banno, H. and Machida, Y. 1994. Characterization of tobacco protein kinase NPK5, a homolog of Saccharomyces cerevisiae SNF1 that constitutively activates expression of the glucose-repressible SUC2 gene for a secreted invertase of S. cerevisiae. Mol. Cell Biol. 14: 2958–2965.
Nakamura, K., Otho, M., Yoshida, N. and Nakamura, K. 1991. Sucrose induced accumulation of β-amylase occurs concomitant with the accumulation of starch and soporamin in leaf petiole cuttings of sweet potato. Plant Physiol. 96: 902–909.
Newman, T., de Bruijn, F.J., Green, P., Keegstra, K., Kende, H., McIntosh, L., Ohlrogge, J., Raikhel, N., Somerville, S., Thomashow, M. et al. 1994. Genes galore: a summary of methods for accessing results from large-scale partial sequencing of anonymous Arabidopsis cDNA clones. Plant Physiol. 106: 1241–1255.
Nordin, K., Heino, P. and Palva, E.T. 1991. Separate signal pathways regulate the expression of a low-temperature-induced gene in Arabidopsis thaliana (L.) Heynh. Plant Mol. Biol. 16: 1061–1071.
Odell, J.T., Nagy, F. and Chua, H. H. 1985. Identification of DNA sequences required for activity of the cauliflower mosaic virus 35S promoter. Nature 313: 810–812.
Pego, J.V., Weisbeek, P.J. and Smeekens, S.C. 1999. Mannose inhibits Arabidopsis germination via a hexokinase-mediated step. Plant Physiol. 119: 1017–1023
Rerie, W.G., Feldmann, K.A. and Marks, M.D. 1994. The GLABRA2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis. Genes Dev. 8: 1388–1399.
Rook, F., Gerrits, N., Kortstee, A., van Kampen, M., Borrias, M., Weisbeek, P. and Smeekens, S. 1998. Sucrose-specific signalling represses translation of the Arabidopsis ATB2 transcription factor gene. Plant J. 15: 253–263.
Ruberti, I., Sessa, G., Lucchetti, S. and Morelli, G. 1991. A novel class of plant proteins containing a homeodomain with a closely linked leucine zipper motif. EMBO J. 10: 1787–1791.
Sambrook, J., Fritsch, E.F. and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed., Cold Spring Harbor Laboratory Press, Plainview, NY.
Schena, M., Lloyd, A.M. and Davis, R.W. 1993. The HAT4 gene of Arabidopsis encodes a developmental regulator. Genes Dev. 7: 67–379.
Scott, M.P. and Weiner, A.J. 1984. Structural relationships among genes that control development: sequence homology between the Antennapedia, Ultrabithorax, andfushi tarazu loci of Drosophila. Proc. Natl. Acad. Sci. USA 81: 4115–4119.
Sheen, J., Zhou, L. and Jang, J.C. 1999. Sugars as signaling molecules. Curr. Plant Biol. 2: 410–418.
Sessa, G., Carabelli, M., Ruberti, I., Lucchetti, S., Baima, S. and Morelli, G. 1994. Identification of distinct families of HD-Zip proteins in Arabidopsis thaliana. In: P. Puigdoménech and G. Coruzzi (Eds.), Analysis of Plant Development and Metabolism, Springer-Verlag, Berlin/Heidelberg, pp. 411–426.
Sessa, G., Morelli, G. and Ruberti, I. 1993. The Athb-1 and-2 HD-Zip domains homodimerize forming complexes of different DNA binding specificities. EMBO J. 12: 3507–3517.
Sessa, G., Morelli, G. and Ruberti, I. 1997. DNA-binding specificity of the homeodomain-leucine zipper domain. J.Mol. Biol. 274: 303–309.
Sheen, J. 1990. Metabolic repression of transcription in higher plants. Plant Cell 2: 1027–1038.
Smeekens, S. and Rook, F. 1997. Sugar sensing and sugar mediated signal transduction in plants. Plant Physiol. 115: 7–13.
Söderman, E., Mattsson, J., Svenson, M Borkird, C. and Engström P. 1994. Expression patterns of novel genes encoding homeodomain leucine-zipper proteins in Arabidopsi thaliana. Plant. Mol. Biol. 26: 145–154.
Söderman, E., Mattsson, J. and Engström, P. 1996. The Arabidopsis homeobox gene ATHB-7 is induced by water deficit and by abscisic acid. Plant J. 10 375–381.
Steindler, C., Matteucci, A., Sessa, G., Weimar, T., Ohgishi, M., Aoyama, T., Morelli, G. and Ruberti, I. 1999. Shade avoidance responses are mediated by the ATHB-2 HD-Zip protein, a negative regulator of gene expression. Development 126: 5–4245
Sterky, F., Regan, S., Karlsson, J., Hertzberg, M., Rohde, A., Holmberg, A., Amini, B., Bhalerao, R., Larsson, M., Villarroel, R., Van Montagu, M., Sandberg, G., Olsson, O., Teeri, T.T., Boerjan, W., Gustafsson, P., Uhlen, M., Sundberg, B. and Lundeberg, J. 1998. Gene discovery in the wood-forming tissues of poplar: analysis of 5,692 expressed sequence tags. Proc. Natl. Acad. Sci. USA 95: 13330–13335.
Tsuge, T., Tsukaya, H. and Uchimiya, H. 1996. Two independent and polarized processes of cell elongation regulate leaf blade expansion in Arabidopsis thaliana (L.) Heynh. Development 122: 1589–1600.
Tsukaya, H., Ohshima, T., Naito, S., Chino, M. and Komeda, Y. 1991. Sugar-dependent expression of the CHS-A gene for chalcone synthase from petunia in transgenic Arabidopsis. Plant Physiol. 97: 1414–1421.
Tsukaya, H., Tsuge, T. and Uchimiya, H. 1994. The cotyledon: a superior system for studies of leaf development. Planta 195: 309–312.
Utsugi, S., Sakamoto, W., Murata, M. and Motoyoshi, F. 1998. Ara-bidopsis thaliana vegetative storage protein (VSP) genes: gene organisation and tissue-specific expression. Plant Mol. Biol. 38: 565–576.
Zhong R. and Ye ZH. 1999. IFL1, a gene regulating interfascicular fiber differentiation in Arabidopsis, encodes a homeodomain-leucine zipper protein. Plant Cell 11: 2139–2152.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Hanson, J., Johannesson, H. & Engström, P. Sugar-dependent alterations in cotyledon and leaf development in transgenic plants expressing the HDZhdip gene ATHB13. Plant Mol Biol 45, 247–262 (2001). https://doi.org/10.1023/A:1006464907710
Issue Date:
DOI: https://doi.org/10.1023/A:1006464907710