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Spatial and temporal expression of Cab mRNAs in cotyledons of the developing soybean seedling

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Abstract

Changes in the temporal and spatial distribution of the mRNAs for the chlorophyll-a/b-binding-protein gene (Cab) in cotyledons from developing soybean (Glycine max (L.) Merr.) seedlings were studied. Cab mRNAs could be detected in the polysomal polyadenylated poly(A)+ mRNA population of cotyledons within 3 d after start of imbibition, prior to their emergence from soil, and declined prior to the onset of cotyledonary senescence. The Cab mRNA levels were compared to the levels of rbcS (ribulose-1,5-bisphosphate carboxylase small subunit) mRNAs in cotyledons and distinct differences in their expression programs were noted. Quantitative analyses with S1 nuclease were used to monitor the accumulation of the mRNAs of individual members of the Cab gene family. Cab 3, Cab 4, and Cab 5 mRNAs were differentially regulated in the cotyledons during post-germinative development. Cab 4 was the most abundant Cab gene mRNA representing approx. 4.3% of the cotyledonary polysomal poly(A)+ mRNA population. In-situ hybridizations using methacrylate-imbedded tissue and 3H-antisense- and -sense-strand RNA probes were used to determine the qualitative and quantitative distribution of Cab RNAs in cotyledonary cells. Cab RNAs were most abundant in the palisade cells. These results indicate an interaction of both developmental and environmental cues in modulating the expression of the Cab gene family in soybean cotyledons.

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Abbreviations

Cab :

genes for chlorophyll-a/b-binding protein

bp:

base pair(s)

poly(A)+ RNA:

polyadenylated RNA

rbcS:

ribulose-1,5-bisphosphate-carboxylase small-subunit gene

References

  • Angerer, L.M., Cox, K.H., Angerer, R.C. (1987) Demonstration of tissue-specific gene expression by in-situ hybridization. Methods Enzymol. 152, 649–661

    Google Scholar 

  • Bartholomew, D.M., Bartley, G.E., Scolnik, P.A. (1991) Abscisic acid control of rbcS and cab transcription in tomato leaves. Plant Physiol. 96, 291–296

    Google Scholar 

  • Batschauer, A., Mosinger, F., Kreuz, K., Dorr, L, Apel, K. (1986) The implication of a plastid-derived factor in the transcriptional control of nuclear genes encoding the light-harvesting chlorophyll a/b protein. Eur. J. Biochem. 154, 625–634

    Google Scholar 

  • Beach, L.R., Spencer, D., Randal, P.J., Higgins, T.J. (1985) Transcriptional and post-transcriptional regulation of storage protein gene expression in sulfur-deficient pea seeds. Nucleic Acids Res. 13, 999–1013

    Google Scholar 

  • Beck, N.G., Lord, E.M. (1988) Breeding system in Ficus carica, the common fig. I. Floral diversity. Am. J. Bot. 75, 1904–1912

    Google Scholar 

  • Bedbrook, J.R., Smith, S.M., Ellis, J. (1980) Molecular cloning and sequencing of cDNA encoding the precursor to the small subunit of chloroplast ribulose-1,5-bisphosphate carboxylase. Nature 287, 692–697

    Google Scholar 

  • Berk, A.J., Sharp, P.A. (1977) Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell 12, 721–732

    Google Scholar 

  • Berry, J.O., Carr, J.P., Klessig, D.F. (1986) mRNAs encoding ribulose-1,5-bisphosphate carboxylase remain bound to polysomes but are not translated in amaranth seedlings transferred to darkness. Proc. Natl. Acad. Sci. USA 85, 4190–4194

    Google Scholar 

  • Bewley, J.D., Black, M. (1983) Physiology and biochemistry of seeds in relation to germination, vol. 1: Development, germination, and growth. Springer, New York

    Google Scholar 

  • Carlson, J.B., Lersten, N.R. (1987) Reproductive morphology. In: Soybean: Improvement, production, and uses, 2nd edn., pp. 95–134, Wilcox, J.R., ed. American Society of Agronomy, Madison, Wis

    Google Scholar 

  • Chang, Y.C., Walling, L.L. (1991) Abscisic acid negatively regulates expression of chlorophyll a/b binding protein genes during soybean embryogeny. Plant Physiol., in press

  • Clewell, D.B., Helinski, D.R. (1969) Supercoiled circular DNA-protein complex in Escherichia coli: Purification and induced conversion to an open circular DNA. Proc. Natl. Acad. Sci. USA 62, 1159–1166

    Google Scholar 

  • Cox, K.H., DeLeon, D.V., Angerer, L.M., Angerer, R.C. (1984) Detection of mRNAs in sea urchin embryos in-situ hybridization using asymmetric RNA probes. Devel. Biol. 101, 485–502

    Google Scholar 

  • Demmin, D.S., Stockinger, J.S., Chang, Y.C., Walling, L.L. (1989) Phylogenetic relationships between the chlorophyll a/b binding protein (Cab) multigene family: an intra- and inter-species study. J. Mol. Evol. 29, 266–279

    Google Scholar 

  • Feinberg, A.P., Vogelstein, B. (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132, 6–13

    Google Scholar 

  • Flores, S., Tobin, E.M. (1986) Benzyadenine modulation of the expression of two genes for nuclear-encoded chloroplast proteins in Lemna gibba: Apparent post-transcriptional regulation. Planta 168, 340–349

    Google Scholar 

  • Gallagher T.F., Ellis R.J. (1982) Light-stimulated transcription of genes for two chloroplast polypeptides in isolated pea nuclei. EMBO J. 2, 1493–1498

    Google Scholar 

  • Giuliano, G., Hiffman, N.E., Ko, K., Scolnik, P.A., Cashmore, A.R. (1988) A light-entrained circadian clock controls transcription of several plant genes. EMBO J. 7, 3635–3642

    Google Scholar 

  • Goldberg, R.B., Hoschek, G., Tam, S.H., Ditta, G.S., Breidenbach, R.W. (1981) Abundance, diversity, and regulation of mRNA sequence sets in soybean embryogenesis. Dev. Biol. 83, 201–217

    Google Scholar 

  • Greenland, A.J., Thomas, M.V., Waiden, R.M. (1987) Expression of two nuclear genes encoding chloroplast proteins during early development of cucumber seedlings. Planta 170, 99–110

    Google Scholar 

  • Harada, J.J., Baden, C.S., Comai, L. (1988) Spatially regulated genes expressed during seed germination and post-germinative development are activated during embryogeny. Mol. Gen. Genet. 212, 466–473

    Google Scholar 

  • Harris, M., Mackender, R.O., Smith, D.L. (1986) Photosynthesis of cotyledons of soybean seedlings. New Phytol. 104, 319–329

    Google Scholar 

  • Horwitz, B.A., Thompson, W.F., Briggs, W.R. (1988) Phytochrome regulation of greening Pisum: Chlorophyll accumulation and abundance of mRNA for the light-harvesting chlorophyll a/b binding proteins. Plant Physiol. 86, 299–305

    Google Scholar 

  • Jamrich, M., Mahon, K.A., Gavis, E.R., Gall, J.G. (1984) Histone RNA in amphibian oocytes visualized by in-situ hybridization to methacrylate-embedded tissue sections. EMBO J. 3, 1939–1943

    Google Scholar 

  • Kamalay, J.C., Goldberg, R.B. (1984) Organ-specific nuclear RNAs in tobacco. Proc. Natl. Acad. Sci. USA 81, 2801–2805

    Google Scholar 

  • Kaufman, L.S., Thompson, W.F., Briggs, W.R. (1984) Different red light requirements for phytochrome-induced accumulation of Cab RNA and rbcS RNA. Science 226, 1447–1449

    Google Scholar 

  • Kloppstech, K. (1985) Diurnal and circadian rhythmicity in the expression of light-induced plant nuclear gene expression. Planta 165, 502–506

    Google Scholar 

  • Langdale, J.A., Zelitch, I., Miller, E., Nelson, T. (1988) Cell position and light influence C4 versus C3 patterns of photosynthetic gene expression. EMBO J. 7, 3643–3651

    Google Scholar 

  • Langeridge, J., Langeridge, P., Bergquist, P.L. (1980) Extraction of nucleic acid from agarose gels. Anal. Biochem. 103, 264–271

    Google Scholar 

  • Lersten, N.R., Carlson, J.B. (1987) Vegetative morphology. In: Soybean: Improvement, production, and uses, 2nd edn., pp. 49–94, Wilcox, J.R., ed. American Society of Agronomy, Madison, Wis

    Google Scholar 

  • Lovell, P., Moore K. (1971) A comparative study of the role of the cotyledon in seeding development. J. Exp. Bot. 22, 153–162

    Google Scholar 

  • Maniatis, T., Fritsch, E.F., Sambrook, J. (1982) DNA cloning. A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y., USA

    Google Scholar 

  • Marrs, K.A., Kaufmann, L.S. (1989) Blue-light regulation of transcription for nuclear genes in pea. Proc. Natl. Acad. Sci. USA 86, 4492–4495

    Google Scholar 

  • Meyerowitz, E.M. (1987) In-situ hybridization to RNA in plant tissue. Plant Mol. Biol. Rep. 5, 242–250

    Google Scholar 

  • Miziorko, H.M., Lorimer, G.H. (1983) Ribulose-1,5-bisphosphate carboxylase-oxgenase. Annu. Rev. Biochem. 52, 507–535

    Google Scholar 

  • Mullet, J.E. (1988) Chloroplast development and gene expression. Annu. Rev. Plant Physiol. Plant Mol. Biol. 39, 475–502

    Google Scholar 

  • Nagy, F., Kay, S.A., Chua, N.-H. (1988) A circadian clock regulates transcription of the wheat Cab-1 gene. Genes Devel. 2, 376–382

    Google Scholar 

  • Piechulla, B., Gruissem, W. (1987) Diurnal mRNA fluctuations of nuclear and plastid genes in developing tomato fruits. EMBO J. 6, 3593–3599

    Google Scholar 

  • Piechulla, B., Pichersky, E., Cashmore, A.R., Gruissem, W. (1986). Expression of nuclear and plastid genes for photosynthetic specific proteins during tomato fruit development and ripening. Plant Mol. Biol. 7, 367–376

    Google Scholar 

  • Richter, G., Wessel, L. (1985) Red light inhibits blue light-induced chloroplast development in cultured plant cells at the mRNA level. Plant Mol. Biol. 5, 175–182

    Google Scholar 

  • Saito, G.Y., Chang, Y.C., Walling, L.L., Thomson, W.W. (1989) A correlation in plastid development and cytoplasmic ultrastructure with nuclear gene expression during seed ripening in soybean. New Phytol. 113, 459–469

    Google Scholar 

  • Saito, G.Y., Chang, Y.C., Walling, L.L., Thomson, W.W. (1990) Chloroplast development and nuclear gene expression in cotyledons of soybean seedlings. New Phytol. 114, 547–554

    Google Scholar 

  • Schmidt, G.W., Bartlett, S.G., Grossman, A.R., Cashmore, A.R., Chua, N.-H. (1981) Biosynthetic pathways of two polypeptides subunits of light-harvesting chlorophyll a/b protein complex. J. Cell Biol. 91, 468–478

    Google Scholar 

  • Silverthorne, J., Tobin, E.M. (1984) Demonstration of transcriptional regulation of specific genes by phytochrome action. Proc. Natl. Acad. Sci. USA 81, 1112–1116

    Google Scholar 

  • Simpson, J., Van Montagu, M., Herrera-Estrella, L. (1986) Photosynthesis-associated gene families: differences in response to tissue-specific and environmental factors. Science 233, 34–38

    Google Scholar 

  • Smith, A., Hinchee, M., Horsch, R. (1987) Cell and tissue specific expression localized by in-situ RNA hybridization in floral tissues. Plant Mol. Biol. Rep. 5, 237–241

    Google Scholar 

  • Smith, D.L. (1983) Cotyledon anatomy in the leguminosae. J. Linnean Soc. Bot. 86, 325–355

    Google Scholar 

  • Taylor, W.C. (1989) Regulatory interactions between nuclear and plastid genomes. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 211–233

    Google Scholar 

  • Thornber, J.P. (1986) Biochemical characterization and structure of pigment-proteins of photosynthetic organisms. In: Encyclopedia of Plant Physiology. N.S., vol. 43, Photosynthetic membranes, pp. 98–114, Staehelin, L.A., Arnzten, C.J., eds. Springer-Verlag, Berlin

    Google Scholar 

  • Treffry, T., Klein, S. Abrahamsen, M. (1967) Studies of fine structural and biochemical changes in cotyledons of germinating soybeans. Aust. J. Biol. Sci. 20, 859–868

    Google Scholar 

  • Tuquet, C., Newman, D.W. (1980) Aging and regreening in soybean cotyledons 1. Ultrastructural changes in plastids and plastoglobuli. Cytobios 29, 43–59

    Google Scholar 

  • Walling, L.L., Drews, G.N., Goldberg, R.B. (1986) Transcriptional and post-transcriptional regulation of soybean seed protein mRNA levels. Proc. Natl. Acad. Sci. USA 83, 2123–2127

    Google Scholar 

  • Walling, L.L., Chang, Y.C., Demmin, D.S., Holzer, F.M. (1988) Isolation, characterization, and evolutionary relatedness of three members from the soybean multigene family encoding chlorophyll a/b binding proteins. Nucleic Acids Res. 16, 10477–10492

    Google Scholar 

  • Wilson, R.F. (1987) Seed metabolism. In: Soybean: Improvement, production, and uses, 2nd edn., pp. 643–686, Wilcox, J.R., ed. American Society of Agronomy, Madison, Wis

    Google Scholar 

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The authors wish to thank Drs. Flizabeth Bray, Bradley Hyman and Laurie Rosenberg for their helpful comments on this manuscript, and to Dr. Elizabeth Lord and members her laboratory who trained Y.C.C. in tissue sectioning. We would like to thank Dr. B. Hyman for use of his laser densitometer. Y.C.C. was a student in the Univeristy of California Riverside Genetics Graduate Group program; this paper is in partial fulfillment of the dissertation requirements for a Ph.D. degree in Genetics for Y.C.C. This work was supported by a U.S. Department of Agriculture Grant 86-CRCR-1-2238 and a McKnight Foundation Grant awarded to L.L.W.

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Chang, Y.C., Walling, L.L. Spatial and temporal expression of Cab mRNAs in cotyledons of the developing soybean seedling. Planta 186, 262–272 (1992). https://doi.org/10.1007/BF00196256

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