Abstract
Transgenic tobacco plants were generated carrying a rice homeobox gene,OSH1, controlled by the promoter of a gene encoding a tobacco pathogenesis-related protein (PR1a). These lines were morphologically abnormal, with wrinkled and/or lobed leaves. Histological analysis of shoot apex primordia indicated arrest of lateral leaf blade expansion, often resulting in asymmetric and anisotropic growth of leaf blades. Other notable abnormalities included abnormal or arrested development of leaf lateral veins. Interestingly,OSH1 expression was undetectable in mature leaves with the aberrant morphological features. Thus,OSH1 expression in mature leaves is not necessary for abnormal leaf development. Northern blot and in situ hybridization analyses indicate thatPR1a-OSH1 is expressed only in the shoot apical meristem and in very young leaf primordia. Therefore, the aberrant morphological features are an indirect consequence of ectopicOSH1 gene expression. The only abnormality observed in tissues expressing the transgene was periclinal (rather than anticlinal) division in mesophyll cells during leaf blade initiation. This generates thicker leaf blades and disrupts the mesophyll cell layers, from which vascular tissues differentiate. TheOSH1 product appears to affect the mechanism controlling the orientation of the plane of cell division, resulting in abnormal periclinal division of mesophyll cell, which in turn results in the gross morphological abnormalities observed in the transgenic lines.
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Affolter M, Schier A, Gehring WJ (1990) Homeodomain proteins and regulation of gene expression. Curr Opin Cell Biol 2:485–495
Andrew DJ, Scott MP (1992) Downstream of the homeotic genes. New Biol 4:5–15
Antoniw JF, White RF (1980) The effects of aspirin and polyacrylic acid on soluble leaf proteins and resistance to virus infection in five cultivars of tobacco. Phytopath Z 98:331–341
Antoniw JF, Ritter CE, Pierpoint WS, Van Loon LC (1980) Comparison of three pathogenesis-related proteins from plants of two cultivars of tobacco infected with TMV. J Gen Virol 47:79–87
Avery GS (1933) Structure and development of the tobacco leaf. Am J Bot 20:565–592
Bellmann R, Werr W (1992) Zmhox1a, the product of a novel maize homeobox gene, interacts with theShrunken 26 bpfeedback control element. EMBO J 11:3367–3374
Carabelli M, Sessa G, Baima S, Moralli G, Ruberti I (1993) TheArabidopsis Athb-2 and-4 genes are strongly induced by far-red-rich light. Plant J 4:469–479
Gunning BES (1982) The cytokinetic apparatus; its development and spatial regulation. In: Lloyd CW (ed) The cytoskeleton in plant growth and development, Academic Press, New York, pp 229–292
Gunning BES, Sammut M (1990) Rearrangements of microtubules involved in establishing cell division planes start immediately after DNA synthesis and are completed just before mitosis. Plant Cell 2:1273–1283
Hayashi S, Scott M (1990) What determines the specificity of action ofDrosophila homeodomain proteins? Cell 63:883–894
Jackson D, Veit B, Hake S (1994) Expression of maizeKNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development 120:405–413
Jegalian BG, De Robertis EM (1992) Homeotic transformations in the mouse induced by overexpression of a humanHox3.3 transgene. Cell 71:901–910
Kano-Murakami Y, Yanai T, Tagiri A, Matsuoka M (1993) A rice homeotic gene,OSH1, causes unusual phenotypes in transgenic tobacco. FEBS Lett 334:365–368
Kessel M, Balling R, Gruss P (1990) Variations of cervical vertebrae after expression of aHox-1.1 transgene in mice. Cell 61:301–308
Kouchi H, Hata S (1993) Isolation and characterization of novel nodulin cDNAs representing genes expressed at early stages of soybean nodule development. Mol Gen Genet 238:106–119
Matsuoka M, Sanada Y (1991) Expression of photosynthetic genes from the C4 plant, maize, in tobacco. Mol Gen Genet 225:411–419
Matsuoka M, Asou S, Ohashi Y (1988) Regulation mechanisms of the synthesis of pathogenesis-related proteins in tobacco leaves. Plant Cell Physiol 29:1185–1192
Matsuoka M, Ichikawa H, Saito A, Tada Y, Fujimura T, Kano-Murakami Y (1993) Expression of a rice homeobox gene causes altered morphology of transgenic plants. Plant Cell 5:1039–1048
Matsuoka M, Tamaoki M, Tada Y, Fujimura T, Tagiri A, Yamamoto N, Kano-Murakami Y (1995) Expression of riceOSH1 gene is localized in developing vascular strands and its ectopic expression in transgenic rice causes altered morphology of leaf. Plant Cell Rep, in press
Mattsson J, Söderman E, Svenson M, Borkird C, Engström P (1992) A new homeobox-leucine zipper gene fromArabidopsis thaliana. Plant Mol Biol 18:1019–1022
McGinnis W, Levine MS, Hafen E, Kuroiwa A, Gehring WJ (1984) A conserved DNA sequence in homeotic genes of theDrosophila Antennapedia and Bithorax complexes. Nature 308:428–433
McHale NA (1993)LAM-1 andFAT genes control development of the leaf blade inNicotiana sylvestris. Plant Cell 5:1029–1038
Ohashi Y, Matsuoka M (1985) Synthesis of stress proteins in tobacco leaves. Plant Cell Physiol 26:473–480
Poethig RS, Sussex IM (1985) The developmental morphology and growth dynamics of the tobacco leaf. Planta 165:158–169
Ruberti I, Sessa G, Lucchetti S, Morelli G (1991) A novel class of plant proteins containing a homeodomain with a closely linked leucine zipper motif. EMBO J 10:1787–1791
Sass AE (1958) Botanical micro technique, 3rd edn. Iowa State University Press, Ames
Schena M, Davis RW (1992) HD-zip proteins: members of anArabidopsis homeodomain protein superfamily. Proc Natl Acad Sci USA 89:3894–3898
Schena M, Lloyd AM, Davis RW (1993) TheHAT4 gene ofArabidopsis encodes a developmental regulator. Genes Dev 7:367–379
Schindler U, Beckmann H, Cashmore AR (1993)HAT3.1, a novelArabidopsis homeodomain protein containing a conserved cysteine-rich region. Plant J 4:137–150
Scott MP, Weiner AJ (1984) Structural relationships among genes that control development: sequence homology between theAntennapedia, Ultrabithorax, andfushi tarazu loci ofDrosophila. Proc Natl Acad Sci USA 81:4115–4119
Scott MP, Tamkun JW, Hartzell GW III (1989) The structure and function of the homeodomain. Biochim Biophys Acta 989:25–48
Sinha NR, Williams RE, Hake S (1993) Overexpression of the maize homeo box gene,KNOTTED-1, causes a switch from determinate to indeterminate cell fates. Genes Dev 7:787–795
Smith LG, Greene B, Veit B, Hake S (1992) A dominant mutation in the maize homeobox gene,Knotted-1, causes its ectopic expression in leaf cells with altered fates. Development 116:21–30
Vollbrecht E, Veit B, Sinha N, Hake S (1991) The developmental geneknotted-1 is a member of a maize homeobox gene family. Nature 350:241–243
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Sato, Y., Tamaoki, M., Matsuoka, M. et al. Abnormal cell divisions in leaf primordia caused by the expression of the rice homeobox geneOSH1 lead to altered morphology of leaves in transgenic tobacco. Molec. Gen. Genet. 251, 13–22 (1996). https://doi.org/10.1007/BF02174339
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DOI: https://doi.org/10.1007/BF02174339