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Characterization of the KNOX class homeobox genes Oskn2 and Oskn3 identified in a collection of cDNA libraries covering the early stages of rice embryogenesis

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Abstract

For identification of genes involved in embryogenesis in the model cereal rice, we have constructed a collection of cDNA libraries of well-defined stages of embryo development before, during and after organ differentiation. Here, we focus on the possible role of KNOX (maize Knotted1-like) class homeobox genes in regulation of rice embryogenesis. Three types of KNOX clones were identified in libraries of early zygotic embryos. Two of these, Oskn2 and Oskn3, encode newly described KNOX genes, whereas the third (Oskn1) corresponds to the previously described OSH1 gene. In situ hybridizations showed that during the early stages of embryo development, all three KNOX genes are expressed in the region where the shoot apical meristem (SAM) is organizing, suggesting that these genes are involved in regulating SAM formation. Whereas OSH1 was previously proposed to function also in SAM maintenance, Oskn3 may be involved in patterning organ positions, as its expression was found to mark the boundaries of different embryonic organs following SAM formation. The expression pattern of Oskn2 suggested an additional role in scutellum and epiblast development. Transgenic expression of Oskn2 and Oskn3 in tobacco further supported their involvement in cell fate determination, like previously reported for Knotted1 and OSH1 ectopic expression. Whereas Oskn3 transformants showed the most pronounced phenotypic effects during vegetative development, Oskn2 transformants showed relatively mild alterations in the vegetative phase but a more severly affected flower morphology. The observation that the KNOX genes produce similar though distinct phenotypic reponses in tobacco, indicates that their gene products act on overlapping but different sets of target genes, or that cell-type specific factors determine their precise action.

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References

  1. 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 

  2. Bertolino E, Reimund B, Wildt-Perinic D, Clerc RG:A novel homeobox protein which recognizes a TGT core and functionally interferes with a retinoid-responsive motif. J Biol Chem 270: 31178–31188 (1995).

    Google Scholar 

  3. Bürglin TR: A comprehensive classification of homeobox genes. In: Duboule D (ed) Guidebook to the Homeobox Genes, pp. 25–71. Oxford University Press, Oxford (1994).

  4. Bürglin TR: Analysis of TALE superclass homeobox genes (MEIS, PBC, KNOX, Iroquois, TGIF) reveals a novel domain conserved between plants and animals. Nucl Acids Res 25: 4173–4180 (1997).

    Google Scholar 

  5. Cavener DR, Ray SC: Eukaryotic start and stop translation sites. Nucl Acids Res 19: 3185–3192 (1991).

    Google Scholar 

  6. Deblaere R, Bytebier B, De Greve H, Deboeck F, Schell J, Van Montagu M, Leemans J: Efficient cotipine Ti plasmid-derived vectors for Agrobacterium-mediated gene transfer to plants. Nucl Acids Res 13: 4777–4788 (1985).

    Google Scholar 

  7. Dehio C, Grossmann K, Schell J, Schmülling T: Phenotype and hormonal status of transgenic tobacco plants overexpressing the rolA gene of Agrobacterium rhizogenes T-DNA. Plant Mol Biol 23: 1199–1210 (1993).

    Google Scholar 

  8. Devos KM, Gale MD: Comparative genetics in the grasses. Plant Mol Biol 35: 3–15 (1997).

    Google Scholar 

  9. Dockx J, Quaedvlieg N, Keultjes G, Kock P, Weisbeek P, Smeekens S: The homeobox gene ATK1 of Arabidopsis thaliana is expressed in the shoot apex of the seedling and in flowers and inflorescence stems of mature plants. Plant Mol Biol 28: 723–737 (1995).

    Google Scholar 

  10. Endrizzi K, Moussian B, Haecker A, Levin JZ, Laux T: The SHOOT MERISTEMLESS gene is required for maintenance of undifferentiated cells in Arabidopsis shoot and floral meristems and acts at a different regulatory level than the meristem genes WUSCHEL and ZWILLE. Plant J 10: 967–979 (1996).

    Google Scholar 

  11. Gehring WJ, Müller M, Affolter M, Percival-Smith A, Billeter M, Qian YQ, Otting G, Wüthrich K: The structure of the homeodomain and its functional implications. Trends Genet 6: 323–329 (1990).

    Google Scholar 

  12. Hong SK, Aoki T, Kitano H, Satoh H, Nagato Y: Phenotypic diversity of 188 rice embryo mutants. Dev Genet 16: 298–310 (1995).

    Google Scholar 

  13. Hörsch RB, Fry J, Hoffmann N, Neidermeyer J, Rogers SG, Fraley RT: Leaf disc transformation. In: Gelvin SB, Schilperoort RA, Verma DPS (eds) Plant Molecular Biology Manual, pp. A5/1-A5/9. Kluwer Academic Publishers, Dordrecht, Netherlands (1991).

    Google Scholar 

  14. Izawa T, Shimamoto K: Becoming a model plant: the importance of rice to plant science. Trends Plant Sci 1: 95–99 (1996).

    Google Scholar 

  15. 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 

  16. Jones TJ, Rost TL: Histochemistry and ultrastructure of rice (Oryza sativa) zygotic embryogenesis. Am J Bot 76: 504–520 (1989).

    Google Scholar 

  17. Jones TJ, Rost TL: The developmental anatomy and ultrastructure of somatic embryos from rice (Oryza sativa L.) scutellum epithelial cells. Bot Gaz 150: 41–49 (1989).

    Google Scholar 

  18. Kano-Murakami Y, Yanai T, Tagiri A, Matsuoka M: A rice homeotic gene, OSH1, causes unusual phenotypes in transgenic tobacco. FEBS Lett 334: 365–368 (1993).

    Google Scholar 

  19. Kawahara R, Komamine A, Fukuda H: Isolation and characterization of homeobox containing genes of carrot. Plant Mol Biol 27: 155–164 (1995).

    Google Scholar 

  20. Kerstetter R, Laudencia-Chingcuanco D, Smith LG, Hake S: Loss-of-function mutations in the maize homeobox gene, knotted1, are defective in shoot meristem maintenance. Development 124: 3045–3054 (1997).

    Google Scholar 

  21. 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 

  22. Kidou S, Ejiri S: Isolation, characterization and mRNA expression of four cDNAs encoding translation elongation factor 1A from rice (Oryza sativa L.). Plant Mol Biol, 36: 137–148 (1998).

    Google Scholar 

  23. Kitano H, Tamura Y, Satoh H, Nagato Y: Hierarchical regulation of organ differentiation during embryogenesis in rice. Plant J 3: 607–610 (1993).

    Google Scholar 

  24. 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. Dev Genet 16: 349–357 (1995).

    Google Scholar 

  25. Korfhage U, Trezzini GF, Meier I, Hahlbrock K, Somssich IE: Plant homeodomain protein involved in transcriptional regulation of a pathogen defense-related gene. Plant Cell 6: 695–708 (1994).

    Google Scholar 

  26. Krishnan BH, White JA: Protein body formation and immunocytochemical localization of globulins and glutelins in developing rice (Oryza sativa L.) embryos. Crop Sci 37: 932–939 (1997).

    Google Scholar 

  27. Lincoln C, Long JA, Yamaguchi J, Serikawa KA, </del> Hake S: a knotted1-like homeobox gene in Arabidopsis is expressed in the vegetative meristem and dramatically alters leaf morphol271 ogy 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 PZ, Porat R, Nadeau JA, Oneill 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. Manak JR, Scott MP: A class act: conservation of homeodomain protein functions. Development (Suppl): 61–77 (1994).

  31. Matsuoka M, Ichikawa H, Saito A, Tada Y, Fujimura T, Kano Murakami Y: Expression of a rice homeobox gene causes altered morphology of transgenic plants. Plant Cell 5: 1039–1048 (1993).

    Google Scholar 

  32. Matsuoka M, Tamaoki M, Tada Y, Fuyjimura T, Tagiri A, Yamamoto N, Kano Murakami Y: Expression of rice OSH1 gene is localized in developing vascular strands and its ectopic expression in transgenic rice causes altered morphology of leaf. Plant Cell Rep 14: 555–559 (1995).

    Google Scholar 

  33. McHale NA: LAM-1 and FAT genes control development of the leaf blade in Nicotiana sylvestris. Plant Cell 5: 1029–1038 (1993)

    Google Scholar 

  34. Meijer AH, Scarpella E, van Dijk EL, Qin L, Taal AJC, Rueb S, Harrington SE, McCouch SR, Schilperoort RA, Hoge JHC: Transcriptional repression by Oshox1, a novel homeodomain leucine zipper protein from rice. Plant J 11: 263–276 (1997).

    Google Scholar 

  35. Meisel L, Lam E: The conserved ELK-homeodomain of KNOTTED-1 contains two regions that signal nuclear localization. Plant Mol Biol 30: 1–14 (1996).

    Google Scholar 

  36. Memelink J: Two yeast/Escherichia coli Lambda/plasmid vectors designed for yeast one-and two-hybrid screens that allow directional cDNA cloning. Technical Tips Online (http://www.elsevier.com.locate/tto) T01111: 1–2 (1997).

  37. Michael T, Spena A: The plant oncogenes rolA, B, and C from Agrobacterium rhizogenes. Effects on morphology, development, and hormone metabolism. Meth Mol Biol 44: 207–222 (1995).

    Google Scholar 

  38. Murashige T, Skoog F: A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15: 473–497 (1962).

    Google Scholar 

  39. Odell JT, Hoopes JL, Vermerris W: Seed-specific gene activation mediated by the Cre/lox site-specific recombination system. Plant Physiol 106: 447–458 (1994).

    Google Scholar 

  40. Okita TW, Hwang YS, Hnilo J, Kim WT, Aryan AP, Larson R, Krishnan HB: Structure and expression of the rice glutelin multigene family. J Biol Chem 264: 12573–12581 (1989).

    Google Scholar 

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

    Google Scholar 

  42. 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 

  43. Rueb S, Leneman M, Schilperoort RA, Hensgens LA: Effi-cient plant regeneration through somatic embryogenesis from callus induced on mature rice embryos (Oryza sativa L.). Plant Cell Tiss Org Cult 36: 259–264 (1994).

    Google Scholar 

  44. Sato Y, Hong SK, Tagiri A, Kitano H, Yamamoto N, Nagato Y, Matsuoka M: A rice homeobox gene, OSH1, is expressed before organ differentiation in a specific region during early embryogenesis. Proc Natl Acad Sci USA 93: 8117–8122 (1996).

    Google Scholar 

  45. Sato Y, Tamaoki M, Murakami T, Yamamoto N, Kano Murakami Y, Matsuoka M: Abnormal cell divisions in leaf primordia caused by the expression of the rice homeobox gene OSH1 lead to altered morphology of leaves in transgenic tobacco. Mol Gen Genet 251: 13–22 (1996).

    Google Scholar 

  46. Schena M, Davis RW: HD-Zip proteins: members of an Arabidopsis homeodomain protein superfamily. Proc Natl Acad Sci USA 89: 3894–3898 (1992).

    Google Scholar 

  47. 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 

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

    Google Scholar 

  49. Sinha NR, Williams RE, Hake S: Overexpression of the maize homeobox gene, KNOTTED-1, causes a switch from determinate to indeterminate cell fates. Genes Dev 7: 787–795 (1993).

    Google Scholar 

  50. Smith LG, Jackson D, Hake S: Expression of knotted1 marks shoot meristem formation during maize embryogenesis. Dev Genet 16: 344–348 (1995).

    Google Scholar 

  51. Tamaoki M, Kusaba S, Kano Murakami Y, Matsuoka M: Ectopic expression of a tobacco homeobox gene, NTH15, dramatically alters leaf morphology and hormone levels in transgenic tobacco. Plant Cell Physiol 38: 917–927 (1997).

    Google Scholar 

  52. Tamaoki M, Tsugawa H, Minami E, Kayano T, Yamamoto N, Kano Murakami Y, Matsuoka M: Alternative RNA products from a rice homeobox gene. Plant J 7: 927–938 (1995).

    Google Scholar 

  53. Vollbrecht E, Kerstetter R, Lowe B, Veit B, Hake S: Homeobox genes in plant development: mutational and molecular analysis. In: Spadlling AC (ed) Evolutionary Conservation of Developmental Mechanisms, pp. 111–123. Wiley-Liss, New York (1993).

    Google Scholar 

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

    Google Scholar 

  55. Wang M, Oppedijk BJ, Caspers MPM, Lamers GEM, Boot MJ, Geerlings DNG, Bakhuizen R, Meijer AH, van Duijn B: Spatial and temporal regulation of DNA fragmentation in the aleurone of germinating Barley. J Exp Bot, 49: 1293–1301 (1998).

    Google Scholar 

  56. Zambryski P, Tempe J, Schell J: Transfer and function of TDNA genes from Agrobacterium Ti and Ri plasmid in plants. Cell 56: 193–201 (1989).

    Google Scholar 

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Postma-Haarsma, A.D., Verwoert, I.I., Stronk, O.P. et al. Characterization of the KNOX class homeobox genes Oskn2 and Oskn3 identified in a collection of cDNA libraries covering the early stages of rice embryogenesis. Plant Mol Biol 39, 257–271 (1999). https://doi.org/10.1023/A:1006153506868

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