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Expression of DC8 is associated with, but not dependent on embryogenesis

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Abstract

DC8 is a late embryogenesis-abundant (LEA) protein gene isolated from carrot (Daucus carota). Deletion analysis of the DC8 promoter was performed to determine the sequences required for ABA and seed-specific regulation of DC8 transcription. To investigate the mechanism of DC8 expression during seed development, chimeric gene constructs containing DC8 promoter fragments fused to a promoterless beta-glucuronidase gene (DC8: GUS) were introduced into carrot, tobacco (Nicotiana tobacum) and Arabidopsis thaliana plants. Seed-specific DC8 expression patterns was conserved among the three plant species. However, differences among the species in the patterns of DC8 expression in the embryo and endosperm that correlated with differences in the rates of embryo and endosperm growth were found. Lack of correspondence between DC8 activation and embryo development among the seeds of the three species suggests that DC8 expression, which is associated with seed maturation, is not coupled to the embryo development program. The presence of DC8 activity in carrot callus and endosperm is consistent with the notion that DC8 expression is independant of embryo morphogenesis. A similar DC8 activity time-course during callus induction and seed development suggests that explantation and 2,4-D treatment initiates a course of events similar to that in the carrot ovule. After fertilization, two pathways one leading to embryo development and another to seed maturation are initiated, but they are not closely linked. As a result we find DC8, part of the maturation program, being activated at different embryonic stages in different plant species.

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References

  1. Baumlein H, Misera S, Luerben H, Kolle Horstmann KC, Wobus U, Muller AJ: The FUS3 gene of Arabidopsis thaliana is a regular of gene expression during late embryogenesis. Plant J 6: 379–387 (1994).

    Article  Google Scholar 

  2. Borkird C, Choi JH, Kin ZH, Franz G, Hatzopoulos P, Chorneau R, Bonas U, Pelegri F, Sung ZR: Developmental regulation of embryonic genes in plants. Proc Natl Acad Sci USA 85: 6399–6403 (1988).

    Google Scholar 

  3. Cheng J, Seeley KA, Sung ZR: RML1 and RML2, Arabidopsis genes required for cell proliferation at the root tip. Plant Physiol 107: 365–376 (1995).

    PubMed  Google Scholar 

  4. Choi JH, Liu L, Borkird C, Sung ZR: Cloning of genes developmentally regulated during plant embryogenesis. Proc Natl Acad Sci USA 84: 1906–1910 (1987).

    Google Scholar 

  5. Clarke MC, Wei W, Lindsey K: High-frequency transformation of Arabidopsis thaliana by Agrobacterium tumfaciens. Plant Mol Biol Rep 10: 178–189 (1992).

    Google Scholar 

  6. Cox KH, Goldberg RB: Analysis of plant gene expression. In: ChShaw (ed) Plant Molecular Biology: A Practical Approach, pp. 1–34. IRL Press, Oxford (1988).

    Google Scholar 

  7. Dure LIII, Crouch M, Harada J, Ho TD, Mundy J, Quatrano R, Thomas T, Sung ZR: Common amino acid sequence domains among the LEA proteins of higher plants. Plant Mol Biol 12: 475–486 (1989).

    Google Scholar 

  8. Finkelstein RR, Tenbarge KM, Shumway JE, Crouch ML: Role of ABA in maturtion of rapeseed embryos. Plant Physiol 78: 630–636 (1985).

    Google Scholar 

  9. Franz G, Hatzopoulos P, Jones TJ, Krauss M, Sung ZR: Molecular and genetic analysis of an embryogenic gene, DC8, from Daucus carota L. Mol Gen Genet 218: 143–151 (1989).

    Article  PubMed  Google Scholar 

  10. Galau GA, Hughes DW: Coordinate accumulation of homologous transcripts of seven cotton Lea gene families during embryogenesis and germination. Devel Biol 123: 213–221 (1987).

    Google Scholar 

  11. Galau GA, Jakobsen KS, Hughes DW: The controls of late dicot embryogenesis and early germination. Plant Physiol 81: 280–288 (1991).

    Article  Google Scholar 

  12. Gamborg OL, Miller RA, Chuama K: Nutritional requirements of suspension culture of soybean root cells. Exp Cell Res 50: 151–158 (1968).

    PubMed  Google Scholar 

  13. Goldberg RB, Barker SJ, Perez-Grau L: Regulation of gene expression during plant embryogenesis. Cell 56: 149–160 (1989).

    Article  PubMed  Google Scholar 

  14. Goupil P, Hatzopoulos P, Franz G, Hempel FD, You R, Sung ZR: Transcriptional regulation of a seed-specific carrot gene, DC8. Plant Mol Biol 18: 1049–1063 (1992).

    PubMed  Google Scholar 

  15. Gray D, Ward JA, Steckel JRA: Endosperm and embryo development in Daucus carota L. J Exp Bot 35: 459–465 (1984).

    Google Scholar 

  16. Guilinan MJ, Marcotte WR, Quantrano RS: A plant leucine zipper protein that recognizes an abscisic acid response element. Science 250: 267–271 (1990).

    PubMed  Google Scholar 

  17. Hatzopoulos P: Developmental and abscisic acid regulation of gene expression during embryogenesis. In: A KalliopiRoubelakis-Angelakis, KThan ThanhVan (eds) Morphogenesis in Plants: Molecular Approaches, pp. 145–159. Plenum Press, New York (1993).

    Google Scholar 

  18. Hatzopoulos P, Fong F, Sung ZR: Abscisic acid regulation of DC8, a carrot embryonic gene. Plant Physiol 94: 690–695 (1990a).

    Google Scholar 

  19. Hatzopoulos P, Franz G, Choy L, Sung ZR: Interaction of nuclear factors with upstream sequences of a lipid body membrane protein gene from carrot. Plant Cell 2: 457–467 (1990b).

    Article  PubMed  Google Scholar 

  20. Horsch RB, Fry JE, Hoffmann NL, Eicholtz D, Rogers SG, Fraley TR: Simple and general method for transferring genes into plants. Science 227: 1229–1231 (1985).

    Google Scholar 

  21. Hughes DW, Galau GA: Developmental and environmental induction of Lea and Lea A mRNAs and the post-abscission program during embryo culture. Plant Cell 3: 605–618 (1991).

    Article  PubMed  Google Scholar 

  22. Jefferson RA, Kavanagh TA, Bevan MW: GUS fusiuons: glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901–3907 (1987).

    PubMed  Google Scholar 

  23. Jos JS, Singh SP: Gametophyte development and embryogeny in the genus Nicotiana. Indian Bot Soc J 46: 117–128 (1968).

    Google Scholar 

  24. Koornneef M, Nanhart CJ, Hilhorst HWM, Karssen CM: In vivo inhibition of seed development and reserve protein accumulation in recombinants of abscisic acid biosynthesis and responsiveness mutants in Arabidopsis thaliana. Plant Physiol 90: 463–469 (1989).

    Google Scholar 

  25. Kosugi S, Ohashi Y, Nakajima K, Arai Y: An improved assay for beta-glucuronidase in transfomred cells: methanol almost completely suppresses a putative endogenous beta-glucuronidase activity. Plant Sci 70: 133–140 (1990).

    Article  Google Scholar 

  26. Mansfield SG, Briarty LG: Endosperm cellularization in Arabidopsis thaliana L. Arabidopsis Inf Serv 27: 65–72 (1992).

    Google Scholar 

  27. Marcotte WR, Bayley CC, Quatrano RS: Regulation of a wheat promoter by abscisic acid in rice protoplasts. Nature 335: 454–457 (1988).

    Article  Google Scholar 

  28. Marcotte WR, Bayley CC, Quatrano RS: Abscisic acid-responsive sequences from the Em gene of wheat. Plant Cell 1: 969–979 (1989).

    Article  PubMed  Google Scholar 

  29. McCarty DR, Hattori T, Carson CB, Vasil V, Lazon M, Vasil IK: The viviparous-1 developmental gene of maize encodes a novel transcriptional activator. Cell 66: 895–905 (1991).

    Article  PubMed  Google Scholar 

  30. Mundy J, Chua N-H: Abscisic acid and water-stress induce the expression of a novel rice gene. EMBO J 7: 2279–2286 (1988).

    PubMed  Google Scholar 

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

    Google Scholar 

  32. Paiva R, Kriz AL: Effect of abscisic acid on embryo-specific gene expression during normal and precocious germination in normal and viviparous maize (Zea mays) embryos. Planta 192: 332–339 (1994).

    Article  Google Scholar 

  33. Parcy F, Valon C, Raynal M, Gaubier-Comella P, Delseny M, Giraudat J: Regulation of gene expression programs during Arabidopsis seed development: roles of the ABI3 locus and of endogenous abscisic acid. Plant Cell 6: 1567–1582 (1994).

    Article  PubMed  Google Scholar 

  34. Quatrano RS: The role of hormones during seed development. In: PJDavies (ed) Plant Hormones and Their Role in Plant Growth and Development, pp. 494–514. Kluwer Academic Publishers, Dordrecht, Netherlands (1987).

    Google Scholar 

  35. Schmidt RJ, Ketudat M, Aukerman MJ, Hosche KG: opaque-2 is a transcriptional activator that recognizes a specific target site in 22-kd zein genes. Plant Cell 4: 689–700 (1992).

    Article  PubMed  Google Scholar 

  36. Schulze-Lefert P, Dangle JL, Beker-Andre M, Hahlbrock K, Schulz W: Inducible in vivo DNA footprints define sequences necessary for UV light activation of the parsley chalcone synthase gene. EMBO J 8: 651–656 (1989).

    PubMed  Google Scholar 

  37. Seeley KA, Byrne DH, Colbert JT: Red light-independent instability of oat phytochrome mRNA in vivo. Plant Cell 4: 29–38 (1992).

    Article  PubMed  Google Scholar 

  38. Shen Q, Ho T-HD: Functional dissection of an abscisic acid (ABA)-inducible gene reveals two independent ABA-responsive complexes each containing a G-box and a novel cis-acting element. Plant Cell 7: 295–307 (1995).

    Article  PubMed  Google Scholar 

  39. Sung ZR: Relationship of indole-3-acetic and tryptophan concentrations in normal and 5-methyltryptophan-resistant cell lines of wild carrots. Planta 145: 339–345 (1979).

    Google Scholar 

  40. Sung ZR: Development biology of plant embryogenesis. In: Freeling M (ed), UCLA Symposia on Molecular and Cellular Biology, pp. 115–128. Alan R. Liss, New York (1985).

    Google Scholar 

  41. Tabata T, Kakase H, Takayama S, Mikami K, Nakatsuka A, Kawata T, Kakayama T, Iwabuchi M: A protein that binds to a cis-acting element of wheat histone genes has a leucine zipper motif. Science 245: 965–967 (1989).

    PubMed  Google Scholar 

  42. Valvekens D, Montagu MV, Lijsebettens MV: Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants by using kanamycin selection. Proc Natl Acad Sci USA 85: 5536–5540 (1988).

    Google Scholar 

  43. West MAL, Yee KM, Danao J, Zimmerman JL, Fischer RL, Goldberg RB, Harada JJ. Leafy cotyledon in an essential regulator of late embryongenesis and cotyledon identity in Arabidopsis. Plant Cell 6: 1731–1735 (1994).

    Article  PubMed  Google Scholar 

  44. Yadegari R, dePaiva G, Laux T, Kolunow AM, Apuya N, Zimmerman JL, Fischer RL, Harada JJ, Goldberg RB: Cell differentiation and morphogenesis are uncoupled in Arabidopsis raspberry embryos. Plant Cell 6: 1713–1729 (1994).

    Article  PubMed  Google Scholar 

  45. Yamaguchi-Shinozaki K, Mino M, Mundy J, Chua N-H: Analysis of an ABA-responsive rice gene promoter in transgenic tobacco. Plant Mol Biol 15: 905–912 (1990).

    Google Scholar 

  46. Zimmerman JL: Somatic embryogenesis: a model for early development in higher plants. Plant Cell 5: 1411–1123 (1993).

    Article  PubMed  Google Scholar 

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Author notes

  1. Jin-Chen Cheng, Kevin Andrew Seeley, Pascale Goupil & Zinmay Renee Sung

    Present address: Physiologie de la Differentiation et Biotechnologies Végétales, Université des Sciences et Technologies de Lille Flandres Artois, Bat. SN2, 59655, Villeneuve d'Asco Cedex, France

Authors and Affiliations

  1. Department of Plant Biology, University of California Berkeley, 1/1 Koshland Hall, 94720, CA, USA

    Jin-Chen Cheng, Kevin Andrew Seeley, Pascale Goupil & Zinmay Renee Sung

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  1. Jin-Chen Cheng
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  3. Pascale Goupil
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  4. Zinmay Renee Sung
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Cheng, JC., Seeley, K.A., Goupil, P. et al. Expression of DC8 is associated with, but not dependent on embryogenesis. Plant Mol Biol 31, 127–141 (1996). https://doi.org/10.1007/BF00020612

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  • DOI: https://doi.org/10.1007/BF00020612

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