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Plant Molecular Biology

, Volume 20, Issue 2, pp 255–266 | Cite as

Temporal and spatial regulation of a novel gene in barley embryos

  • Laura M. Smith
  • Jane Handley
  • Yi Li
  • Helen Martin
  • Linda Donovan
  • Dianna J. Bowles
Research Article

Abstract

The temporal and spatial pattern of expression of a novel barley gene is described. The gene has been identified through the differential screening of a cDNA library constructed to poly(A)+ RNA of zygotic embryos. Transcripts corresponding to the cDNA, pZE40, become abundant in the non-axial tissues of the developing embryo within 8–10 days after anthesis, when steady-state levels are high in the scutellum, coleoptile and coleorhiza, with the exception of the scutellar epithelium. This expression pattern is maintained throughout maturation of the embryo until levels eventually decline as the grain desiccates. On germination, there is a transient re-appearance of mRNA to pZE40, with accumulation specifically restricted to the scutellum of the seedling. In situ hybridization has enabled the detection of transcripts elsewhere in the barley plant, in highly localized groups of cells. The timing and cell specificity of expression suggests the gene product is involved in the synthesis and/or transport of metabolites.

Key words

barley (Hordeum vulgarezygotic embryogenesis plant development gene expression 

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References

  1. 1.
    Avigad G: Sucrose and other disaccharides. In: Loewus FA, Tanner W (eds) Encyclopedia of Plant Physiology, New Series, vol. 13A: Plant Carbohydrates I pp. 217–347. Springer-Verlag, New York (1982).Google Scholar
  2. 2.
    Aviv H, Leder P: Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc Natl Acad Sci USA 69: 1408–1412 (1972).Google Scholar
  3. 3.
    Bartels D, Singh M, Salamini F: Onset of desiccation tolerance during development of the barley embryo. Planta 175: 485–492 (1988).Google Scholar
  4. 4.
    Bennetzen JL, Hall BD: Codon selection in yeast. J Biol Chem 257: 3026–3031 (1982).Google Scholar
  5. 5.
    Bewley JD, Black M: Physiology and Biochemistry of Seeds I: Development, Germination and Growth. Springer-Verlag, New York (1978).Google Scholar
  6. 6.
    deBoer HA, Kastein RA: Biased codon usage: an exploration of its role in optimization of translation. In: Reznikoff W, Gold L (eds) Maximizing Gene Expression, pp. 225–285. Butterworths, Boston (1986).Google Scholar
  7. 7.
    Bowles DJ: Defence-related proteins of higher plants. Annu Rev Biochem 59: 873–907 (1990).Google Scholar
  8. 8.
    Bowles DJ: Embryogenesis. In: Marshall & Grace (eds) The Environmental Physiology of Seed and Fruit Production. Cambridge University Press, Cambridge, in press.Google Scholar
  9. 9.
    Campbell WH, Gowri G: Codon usage in higher plants green algae, and Cyanobacteria. Plant Physiol 92: 1–11 (1990).Google Scholar
  10. 10.
    Cardini CE, Leloir LF, Chiriboga J: The biosynthesis of sucrose. J Biol Chem 214: 149–155 (1955).Google Scholar
  11. 11.
    Chandler PM, Zwar JA, Jacobsen JV, Higgins TJV, Inglis AS: The effects of gibberellic acid and abscisic acid on α-amylase mRNA levels in barley aleurone layers studies using an α-amylase cDNA clone. Plant Mol Biol 3: 407–418 (1984).Google Scholar
  12. 12.
    Clark AJ, Higgins P, Martin H, Bowles DJ: An embryospecific protein of barley (Hordeum vulgare). Eur J Biochem 199: 115–121 (1991).Google Scholar
  13. 13.
    Edelman J, Shibko SI, Keys AJ: The role of the scutellum of cereal seedlings in the synthesis and transport of sucrose. J Exp Bot 10: 178–189 (1959).Google Scholar
  14. 14.
    Engell K: Embryology of barley: time-course and analysis of controlled fertilization and early embryo formation based on serial sections. Nord J Bot 9: 265–280 (1989).Google Scholar
  15. 15.
    Fincher GB, Lock PA, Morgan MM, Lingelbach K, Wettenhall REH et al.: Primary structure of the (1–3, 1–4)-β-D-glucan 4-glucanohydrolase from barley aleurone. Proc Natl Acad Sci USA 83: 2081–2085 (1986).Google Scholar
  16. 16.
    Fincher GB: Molecular and cellular biology associated with endosperm mobilization in germinating cereal grains. Annu Rev Plant Physiol Plant Mol Biol 40: 305–346 (1989).Google Scholar
  17. 17.
    Galau GA, Bijaisoradat N, Hughes DW: Accumulation kinetics of cotton late embryogenesis-abundant mRNAs and storage protein mRNAs: Coordinate regulation during embryogenesis and the role of abscisic acid. Develop Biol 123: 198–212 (1987).Google Scholar
  18. 18.
    Gifford RM, Evans LT: Photosynthesis, carbon partioning and yield. Ann Rev Plant Physiol 32: 485–509 (1981).Google Scholar
  19. 19.
    Harada JJ, Baden CS, Comai L: Spatially regulated genes expressed during seed germination and post-germinative development are activated during embryogenesis. Mol Gen Genet 212: 466–473 (1988).Google Scholar
  20. 20.
    Harada JJ, Delisle AJ, Baden CS, Crouch ML: Unusual sequence of an ABA-inducible mRNA which accumulates late in Brassica napus seed development. Plant Mol Biol 12: 395–401 (1989).Google Scholar
  21. 21.
    Higgins P, Bowles DJ: Comparative analysis of translatable mRNA populations in zygotic and pollen-derived embryos of barley (Hordeum vulgare L.). Plant Sci 69: 239–247 (1990).Google Scholar
  22. 22.
    Hughes DW, Galau GA: Temporally modular gene expression during cotyledon development. Genes Develop 3: 358–369 (1989).Google Scholar
  23. 23.
    Hughes DW, Galau GA: Developmental and environmental induction of Lea and Lea A mRNAs and the post abscision program during embryo culture. Plant Cell 3: 605–618 (1991).Google Scholar
  24. 24.
    Hoj PB, Hartman DJ, Morrice NA, Doan DNP, Fincher GB. Purification of (1–3, 1–4) β-glucan endohydrolase isoenzyme II from germinated barley and determination of its primary structure from a cDNA clone. Plant Mol Biol 13: 31–42 (1989).Google Scholar
  25. 25.
    Jakobsen K, Klemsdal SS, Aalen RB, Bosnes M, Alexander D, Olsen OA: Barley aleurone cell development: molecular cloning of aleurone-specific cDNAs from immature grains. Plant Mol Biol 12: 285–293 (1989).Google Scholar
  26. 26.
    Jones TJ, Rost TL: Histochemistry and ultrastructure of rice zygotic embryogenesis. Am J Bot 76: 504–520 (1989).Google Scholar
  27. 27.
    Langridge P, Pintor-Toro JA, Feix G: Zein precursor mRNAs from maize endosperm. Mol Gen Genet 187: 432–438 (1982).Google Scholar
  28. 28.
    Lehrach H, Diamond D, Wozney JM, Boedtker H: RNA molecular weight determinations by gel electrophoresis under denaturing conditions; a critical reexamination. Biochemistry 16: 4743–4750 (1977).Google Scholar
  29. 29.
    Leloir LF, Cardini CE: The biosynthesis of sucrose. J Am Chem Soc 75: 4118–4123 (1953).Google Scholar
  30. 30.
    Leloir LF, Cardini CE: The biosynthesis of sucrose phosphate. J Biol Chem 214: 157–165 (1955).Google Scholar
  31. 31.
    Logemann J, Schell J, Willmitzer L: Improved method for the isolation of RNA from plant tissues. Anal Biochem 163: 16–20 (1987).Google Scholar
  32. 32.
    Maniatis T, Fritsch EF, Sambrook J: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY (1983).Google Scholar
  33. 33.
    M'Batchi B, Delrot S: Stimulation of sugar exit from leaf tissues of Vicia faba. Planta 174: 540–548 (1988).Google Scholar
  34. 34.
    McFadden GT, Ahluwalia B, Clarke AE, Fincher GB: Expression sites and developmental regulation of genes encoding (1–3, 1–4)-β-glucanases in germinating barley. Planta 173: 500–508 (1988).Google Scholar
  35. 35.
    MacGregor AW, MacDougall FH, Mayer C, Daussant J: Changes in levels of α-amylase components in barley tissues during germination and early seedling growth. Plant Physiol 75: 203–206 (1984).Google Scholar
  36. 36.
    Merry J: Studies on the embryo of Hordeum sativum. I. The development of the embryo. Bull Torrey Bot Club 68: 586–598 (1981).Google Scholar
  37. 37.
    Mundy J, Brandt A, Fincher GB: Messenger RNA from the scutellum and aleurone of germinating barley encode (1–3, 1–4)-β-D-glucanase, a-amylase and carboxypeptidase. Plant Physiol 79: 867–871 (1985).Google Scholar
  38. 38.
    Morris PC, Bowles DJ: Abscisic acid and embryogenesis. Brit Plant Growth Regul Monogr 15: 65–75 (1987).Google Scholar
  39. 39.
    Morris PC, Mattock SE, Jones MGK, Bowles DJ: Changes in the levels of wheat and barley germ agglutinin during embryogenesis in vivo, in vitro and during germination. Planta 166: 407–413 (1985).Google Scholar
  40. 40.
    Morris PC, Weiler EW, Mattock SE, Jones MGK, Lenton JR, Bowles DJ: Determination of endogenous abscisic acid levels in immature cereal embryos during in vitro culture. Planta 173: 110–116 (1988).Google Scholar
  41. 41.
    Murray EE, Lotzer J, Eberle M: Codon usage in plant genes. Nucl Acids Res 17: 477–498 (1989).Google Scholar
  42. 42.
    Norstog K: Early development of the barley embryo: fine structure. Am J Bot 59: 123–132 (1972).Google Scholar
  43. 43.
    Okamoto K, Kitano H, Akazawa T: Biosynthesis and excretion of hydrolases in germinating cereal seeds. Plant Cell Physiol 21: 201–204 (1980).Google Scholar
  44. 44.
    Olsen O-A, Jakobsen KS, Schmelzer E: Development of barley aleurone cells: temporal and spatial patterns of accumulation of cell-specific mRNAs. Planta 181: 462–466 (1990).Google Scholar
  45. 45.
    Pogson BJ, Ashford AE, Gubler F: Immunoflurorescence localization of α-anylase in the scutellum germ aleurone and normal aleurone of germinated barley grains. Protoplasma 151: 128–136 (1989).Google Scholar
  46. 46.
    Raikhel NV, Bednarck SY, Wilkins TA: Cell-type specific expression of wheat germ agglutinin gene in embryos and young seedlings of Triticum aestivum. Planta 126: 406–414 (1988).Google Scholar
  47. 47.
    Ranki H: Secretion of alpha anylase by the epithelium of barley scutellum. J Inst Brew 96: 307–310 (1990).Google Scholar
  48. 48.
    Rogers JC: Two barley a-amylase gene families are regulated differently in aleurone cells. J Biol Chem 260: 3731–3738 (1985).Google Scholar
  49. 49.
    Sakri FAK, Shannon JC: Movement of 14C-labelled sugars into kernels of wheat (Triticum aestivum L.). Plant Physiol 55: 881–889 (1975).Google Scholar
  50. 50.
    Sharp PM, Tuohy TMF, Mosurski KR: Codon usage in yeast: cluster analysis clearly differentiates highly and lowly expressed genes. Nucl Acids Res 14: 5125–5143 (1986).Google Scholar
  51. 51.
    Smart IM, Loi L, Fincher GB: Development of (1–3,1–4)-β-D-glucan endohydrolase isoenzymes in isolated scutella and aleurone layers of barley (Hordeum vulgare). Plant Physiol 80: 310–314 (1986).Google Scholar
  52. 52.
    Slakeski N, Baulcombe DC, Devos KM, Ahluwalia B, Doan DNP, Fincher G: Structure and tissue-specific regulation of genes encoding barley 1–3, 1–4 β-glucan endohydrolases. Mol Gen Genet 224: 437–449 (1990).Google Scholar
  53. 53.
    Sung ZR, Okimoto R: Co-ordinate gene expression during somatic embryogenesis in carrot. Proc Natl Acad Sci USA 80: 2661–2665 (1983).Google Scholar
  54. 54.
    Sung ZR, Okimoto R: Embryonic proteins in somatic embryos of carrot. Proc Natl Acad Sci USA 78: 3683–3687 (1981).Google Scholar
  55. 55.
    Turgeion R: Efflux of sucrose form minor veins of tobacco leaves. Planta 161: 120–128 (1984).Google Scholar
  56. 56.
    deVries SC, Booig H, Meyerink P, Huisman G, Wilde HD, Thomas TL, vanKammen A: Acquisition of embryogenic potential in carrot suspension cultures. Planta 176: 196–204 (1988).Google Scholar
  57. 57.
    Wilkins TA, Rajkhel NV: Expression of rice lectin is governed by two temporally and spatially regulated mRNAs in developing embryos. Plant Cell 1: 541–549 (1989).Google Scholar

Copyright information

© Kluwer Academic Publishers 1992

Authors and Affiliations

  • Laura M. Smith
    • 1
  • Jane Handley
    • 1
  • Yi Li
    • 1
  • Helen Martin
    • 1
  • Linda Donovan
    • 1
  • Dianna J. Bowles
    • 1
  1. 1.Centre for Plant Biochemistry and BiotechnologyUniversity of LeedsLeedsUK

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