Abstract
The small subunit of ribulose 1,5-bisphosphate carboxylase/oxygenase (EC 4.1.1.39) in the French bean Phaseolus vulgaris L. is encoded by a small gene family consisting of a minimum of three members. Three small subunit genes (rbcS genes) represented in a light-grown primary leaf cDNA library were characterised by sequencing two cDNAs which were full-length and one which was deficient in part of the sequence encoding the transit peptide. The cDNA clones are identical in their coding sequences, for both the transit peptide and the mature polypeptide, but divergent in their untranslated sequences. The derived amino acid sequence is very similar to that reported for other species, although the first amino acid of the mature polypeptide is isoleucine, which differs from the methionine found in all other higher plant rbcS genes. Surprisingly, one of the cDNA clones contains two introns, which are at positions conserved in rbcS genes from other species. It is concluded that this cDNA resulted from the cloning of an unprocessed transcript. Alternative polyadenylation sites are found for two of the genes. Expression of the rbcS genes in the primary leaves is stimulated by light, although transcripts can readily be detected in dark-grown leaves. Expression is also organ-specific, as in other species. The frequency of cDNA clones in the library indicates that the different genes show quantitative differences in expression and S1 nuclease analysis suggests that individual rbcS genes are photoregulated.
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References
Batschauer A, Mösinger E, Kreuz K, Döre I, Apel K: 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 (1986).
Bedbrook JR, Smith SM, Ellis RJ: Molecular cloning and sequencing of cDNA encoding the precursor to the small subunit of chloroplast ribulose-1,5-bisphosphate carboxylase. Nature 287: 692–697 (1980).
Bennett J, Jenkins GI, Hartley MR: Differential regulation of the accumulation of the light-harvesting chlorophyll a/b complex and ribulose bisphosphate carboxylase/oxygenase in greening pea leaves. J Cell Biochem 25: 1–13 (1984).
Berry JO, Nikolau BJ, Carr JP, Klessig DF: Transcriptional and post-transcriptional regulation of ribulose 1,5-bisphosphate carboxylase gene expression in light- and dark-grown amaranth cotyledons. Mol Cell Biol 5: 2238–2246 (1985).
Berry-Lowe SL, McKnight TD, Shah DM, Meagher RB: The nucleotide sequence, expression, and evolution of one member of a multigene family encoding the small subunit of ribulose-1,5-bisphosphate carboxylase in soybean. J Mol Appl Genet 1: 483–498 (1982).
Birnboim H, Doly J: A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucl Acids Res 7: 1513–1523 (1979).
Birnstiel ML, Busslinger M, Strub K: Transcription termination and 3′ processing: the end is in site! Cell 41: 349–359 (1985).
Bradbeer JW, Ireland HMM, Smith JW, Rest J, Edge HJW: Plastid development in primary leaves of Phaseolus vulgaris. New Phytol 73: 263–270 (1974).
Brown JWS: A catalogue of splice junction and putative branch point sequences from plant introns. Nucl Acids Res 14: 9549–9559 (1986).
Burke JF: High sensitivity S1 mapping with single-stranded [32P]DNA probes synthesised from bacteriophage M13mp templates. Gene 30: 63–68 (1984).
Calzone FJ, Britten RJ, Davidson EH: Mapping of gene transcripts by nuclease protection assays and cDNA primer extension. In Berger SL, Kimmel AR (eds) Methods in Enzymology vol 152, pp. 611–632. Academic Press, London (1987).
Chory J, Peto C, Feinbaum R, Pratt L, Ausubel F: Arabidopsis thaliana mutant that develops as a light-grown plant in the absence of light. Cell 58: 991–999 (1989).
Coruzzi G, Broglie R, Cashmore AR, Chua N-H: Nucleotide sequences of two pea cDNA clones encoding the small subunit of ribulose-1,5-bisphosphate carboxylase and the major chlorophyll a/b-binding thylakoid polypeptide. J Biol Chem 258: 1399–1402 (1983).
Coruzzi G, Broglie R, Edwards C, Chua N-H: Tissue-specific and light-regulated expression of a pea nuclear gene encoding the small subunit of ribulose-1,5-bisphosphate carboxylase. EMBO J 3: 1671–1679 (1984).
Dean C, Pichersky E, Dunsmuir P: Structure, evolution and regulation of rbcS genes in higher plants. Annu Rev Plant Physiol Plant Mol Biol 40: 415–439 (1989).
Dean C, Tamaki S, Dunsmuir P, Favreau M, Katayama C, Dooner H, Bedbrook J: mRNA transcripts of several plant genes are polyadenylated at multiple sites in vivo. Nucl Acids Res 4: 2229–2240 (1986).
Dean C, van den Elzen P, Tamaki S, Dunsmuir P, Bedbrook J: Differential expression of the eight genes of the petunia ribulose bisphosphate carboxylase small subunit multi-gene family. EMBO J 4: 3055–3061 (1985).
Dellaporta SL, Wood J, Hicks JB: A plant DNA minipreparation: version II. Plant Mol Biol Rep 1: 19–21 (1983).
Dunsmuir P, Smith S, Bedbrook J: A number of different nuclear genes for the small subunit of RuBPCase are transcribed in petunia. Nucl Acids Res 11: 4177–4183 (1983).
Ellis RJ: Chloroplast proteins: synthesis, transport and assembly. Annu Rev Plant Physiol 32: 111–137 (1981).
Ellis RJ, Van der Vies SM: The Rubisco subunit binding protein. Photosynth Res 16: 101–115 (1988).
Fluhr R, Moses P, Morelli G, Coruzzi G, Chua N-H: Expression dynamics of the pea rbcS multigene family and organ distribution of the transcripts. EMBO J 5: 2063–2071 (1986).
Gallagher TF, Ellis RJ: Light-stimulated transcription of genes for two chloroplast polypeptides in isolated pea leaf nuclei. EMBO J 1: 1493–1498 (1982).
Gilmartin PM, Sarokin L, Memelink J, Chua N-H: Molecular light switches for plant genes. Plant Cell 2: 369–378 (1990).
Greenland AJ, Thomas MV, Walden RM: Expression of two nuclear genes encoding chloroplast proteins during early development of cucumber seedlings. Planta 170: 99–110 (1987).
Gutteridge S, Gatenby AA: The molecular analysis of the assembly, structure and function of Rubisco. In: BJ Miflin (ed), Oxford Surveys of Plant Molecular and Cell Biology vol 4, pp. 95–135. Oxford University Press, Oxford (1987).
Jenkins GI: Photoregulation of gene expression in plants. Photochem Photobiol 48: 821–832 (1988).
Jenkins GI: Photoregulation of plant gene expression. In: Grierson D (ed) Developmental Regulation of Plant Gene Expression, pp. 1–41. Blackie, Glasgow/London (1991).
Jenkins GI, Hartley MR, Bennett J: Photoregulation of chloroplast development: transcriptional, translational and post-translational controls? Phil Trans Royal Soc Lond B303: 409–431 (1983).
Jenkins GI, Smith H: Red: far-red ratio does not modulate the abundance of transcripts for two major chloroplast polypeptides in light-grown Pisum sativum terminal shoots. Photochem Photobiol 42: 679–684 (1985).
Keegstra K: Transport and routing of proteins into chloroplasts. Cell 56: 247–253 (1989).
Manzara T, Gruissem W: Organization and expression of the genes encoding ribulose-1,5-bisphosphate carboxylase in higher plants. Photosynth Res 16: 117–139 (1988).
Mount SM: A catalogue of splice junction sequences. Nucl Acids Res 10: 459–472 (1982).
Nagy F, Kay SA, Chua N-H: Analysis of gene expression in transgenic plants. In: Gelvin SB, Schilperoort RA (eds) Plant Molecular Biology Manual, pp. B4: 1–29. Kluwer Academic Publishers, Dordrecht (1988).
Polans NO, Weeden NF, Thompson WF: Inheritance, organisation and mapping of rbcS and cab multigene families in pea. Proc Natl Acad Sci USA 82: 5083–5087 (1985).
Robinson C, Ellis RJ: Transport of proteins into chloroplasts. Partial purification of a chloroplast protease involved in the processing of imported precursor polypeptides. Eur J Biochem 142: 337–342 (1984).
Sambrook J, Fritsch EF, Maniatis T: Molecular cloning: a laboratory manual, second edition. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).
Sanger F, Nicklen S, Coulson AR: DNA sequencing with chain termination inhibitors. Proc Natl Acad Sci USA 74: 5463–5467 (1977).
Shirley BW, Ham DP, Senecoff JF, Berry-Lowe SL, Zurfluh LL, Shah DM, Meagher RB: Comparison of the expression of two highly homologous members of the soybean ribulose-1,5-bisphosphate carboxylase small subunit gene family. Plant Mol Biol 14: 909–925 (1990).
Silverthorne J, Tobin EM: Post-transcriptional regulation of organ-specific expression of individual rbcS mRNAs in Lemna gibba. Plant Cell 2: 1181–1190 (1990).
Silverthorne J, Wimpee CF, Yamada T, Rolfe SA, Tobin EM: Differential expression of individual genes encoding the small subunit of ribulose-1,5-bisphosphate carboxylase in Lemna gibba. Plant Mol Biol 15: 49–58 (1990).
Simpson J, Van Montagu M, Herrera-Estrella L: Photosynthesis-associated gene families: differences in response to tissue-specific and environmental factors. Science 233: 34–38 (1986).
Sugita M, Gruissem W: Developmental, organ-specific and light-dependent expression of the tomato ribulose-1,5-bisphosphate carboxylase small subunit gene family. Proc Natl Acad Sci USA 84: 7104–7108 (1987).
Sugita M, Manzara T, Pichersky E, Cashmore A, Gruissem W: Genomic organisation, sequence analysis and expression of all five genes encoding the small subunit of ribulose-1.5-bisphosphate carboxylase/oxygenase from tomato. Mol Gen Genet 209: 247–256 (1987).
Taylor WC: Regulatory interactions between nuclear and plastid genomes. Annu Rev Plant Physiol Plant Mol Biol 40: 211–233 (1989).
Weeden NF: Expression of a single Rubisco small subunit gene in the bean: Plant Physiol 75, suppl. 159 (1984).
Whatley JM: Chloroplast development in primary leaves of Phaseolus vulgaris. New Phytol 73: 1097–1110 (1974).
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Knight, M.R., Jenkins, G.I. Genes encoding the small subunit of ribulose 1,5-bisphosphate carboxylase/oxygenase in Phaseolus vulgaris L.: nucleotide sequence of cDNA clones and initial studies of expression. Plant Mol Biol 18, 567–579 (1992). https://doi.org/10.1007/BF00040672
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DOI: https://doi.org/10.1007/BF00040672