Summary
We have cloned and sequenced all five members of the gene family for the small subunit (rbcS) of ribulose-1,5-bisphosphate carboxylase/oxygenase from tomato, Lycopersicon esculentum cv. VFNT LA 1221 cherry line. Two of the five genes, designated Rbcs-1 and Rbcs-2, are present as single genes at individual loci. Three genes, designated Rbcs-3A, Rbcs-3B and Rbcs-3C, are organized in a tandem array within 10 kb at a third independent locus. The Rbcs-2 gene contains three introns; all the other members of the tomato gene family contain two introns. The coding sequence of Rbcs-1 differs by 14.0% from that of Rbcs-2 and by 13.3% from that of Rbcs-3 genes. Rbcs-2 shows 10.4% divergence from Rbcs-3. The exon and intron sequences of Rbcs-3A are identical to those of Rbcs-3C, and differ by 1.9% from those of Rbcs-3B. Nucleotide sequence analysis suggests that the five rbcS genes encode four different precursors, and three different mature polypeptides. S1 nuclease mapping of the 5′ end of rbcS mRNAs revealed that the mRNA leader sequences vary in length from 8 to 75 nucleotides. Northern analysis using gene-specific oligonucleotide probes from the 3′ non-coding region of each gene reveals a four to five-fold difference among the five genes in maximal steady-state mRNA levels in leaves.
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Bedbrook, JR, Coen DM, Beaton AR, Bogorad L, Rich A (1979) Location of the single gene for the large subunit of ribulose bisphosphate carboxylase on the maize chloroplast chromosome. J Biol Chem 254:905–910
Bendich AJ, Anderson RS, Ward BL (1979) Plant DNA: long, pure and simple. In: Leaver CJ (ed) Genome organization and expression in plants. Plenum Press, New York London, pp 31–33
Bennett MD, Smith JM (1976) Nuclear DNA amounts in angiosperms. Philos Trans R Soc Lond 274:227–274
Bernatzky R, Tanksley SD (1986) Majority of random cDNA clones correspond to single loci in the tomato genome. Mol Gen Genet 203:8–14
Berry JO, Nikolau BJ, Carr JP, Klessig DF (1985) 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
Berry-Lowe SL, McKnight TD, Shah DM, Meagher RB (1982) 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
Biggin MD, Gibson TJ, Hong GF (1983) Buffer gradient gels and 35S label as an aid to rapid DNA sequence determination. Proc Natl Acad Sci USA 80:3963–3965
Blair GE, Ellis RJ (1973) Protein synthesis in chloroplasts. I. Lightdriven synthesis of large subunit of Fraction I protein by isolated pea chloroplasts. Biochim Biophys Acta 319:223–234
Breathnach R, Chambon P (1981) Organization and expression of eukaryotic split genes coding for proteins. Annu Rev Biochem 50:349–383
Broglie R, Coruzzi G, Lamppa G, Keith B, Chua N-H (1983) Structural analysis of nuclear genes coding for the precursor to the small subunit of wheat ribulose-1,5-bisphosphate carboxylase. Biotechnology 1:55–61
Dean C, Elzen PVD, Tamaki S, Dunsmuir P, Bedbrook J (1985) Differential expression of the eight genes of the petunia ribulose bisphosphate carboxylase small subunit multigene family. EMBO J 4:3055–3061
Dean C, Tamaki S, Dunsmuir P, Favreau M, Katayama C, Dooner H, Bedbrook J (1986) mRNA transcripts of several plant genes are polyadenylated at multiple sites in vivo. Nucleic Acids Res 14:2229–2240
Fluhr R, Kuhlemeier C, Nagy F, Chua N-H (1986a) Organ-specific and light-induced expression of plant genes. Science 232:1106–1112
Fluhr R, Moses P, Morelli G, Coruzzi G, Chua N-H (1986b) Expression dynamics of the pea rbcS multigene family and organ distribution of the transcripts. EMBO J 5:2063–2071
Frischauf A-M, Lehrach H, Poustka A, Murry N (1983) Lambda replacement vectors carrying polylinker sequences. J Mol Biol 170:827–842
Gillies SD, Morrison SL, Oi VT, Tonegawa S (1983) A tissuespecific transcription enhancer element is located in the major intron of a rearranged immunoglobulin heavy chain gene. Cell 33:115–123
Gruissem W, Callan K, Lynch J, Manzara T, Meighan M, Narita J, Piechulla B, Sugita M, Thelander M, Wanner L (1987) Plastid and nuclear gene expression during tomato fruit formation. In: Nevins D (ed) Tomato biotechnology. Liss, New York (in press)
Gruissem W, Zurawski G (1985) Identification and mutational analysis of the promoter for a spinach chloroplast transfer RNA gene. EMBO J 4:1637–1644
Inamine G, Nash B, Weissbach H, Brot N (1985) Light regulation of the synthesis of the large subunit of ribulose-1,5-bisphosphate carboxylase in peas: Evidence for translational control. Proc Natl Acad Sci USA 82:5690–5694
Loenen WAM, Blattner FR (1983) Lambda Charon vectors (Ch32, 33, 34 and 35) adapted for DNA cloning in recombinationdeficient hosts. Gene 26:171–179
Mazur BJ, Chui C-F (1985) Sequence of a genomic DNA clone for the small subunit of ribulose bis-phosphate carboxylase-oxygenase from tobacco. Nucleic Acids Res 13:2373–2386
Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: A laboratory manual, Cold Spring Harbor Laboratory, Cold Spring Harbor, New York
Maxam AM, Gilbert W (1977) A new method for sequencing DNA. Proc Natl Acad Sci USA 74:560–564
Messing J (1983) New M13 vectors for cloning. Methods Enzymol 101:20–78
Morelli G, Nagy F, Fraley RT, Rogers SG, Chua NH (1985) A short conserved sequence is involved in the light-inducibility of a gene encoding ribulose-1,5-bisphosphate carboxylase small subunit of pea. Nature 315:200–204
Miziorko HM, Lorimer GH (1983) Ribulose-1,5-bisphosphate carboxylase-oxygenase. Annu Rev Biochem 52:507–535
Muller K-D, Salnikow J, Vater J (1983) Amino acid sequence of the small subunit of D-ribulose-bisphosphate carboxylase/oxygenase from Nicotiana tabacum. Biochim Biophys Acta 742:78–83
Piechulla B, Imlay KRC, Gruissem W (1985) Plastid gene expression during fruit ripening in tomato. Plant Mol Biol 5:373–384
Piechulla B, Pichersky E, Cashmore AR, Gruissem W (1986) Expression of nuclear and plastid genes for photosynthesis-specific proteins during tomato fruit development and ripening. Plant Mol Biol 7:367–376
Pichersky E, Bernatzky R, Tanskley SD, Cashmore AR (1986) Evidence for selection as a mechanism in the concerted evolution of Lycopersicon esculentum (tomato) genes encoding the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase. Proc Natl Acad Sci USA 83:3880–3884
Polans NO, Weeden NF, Thomspon WF (1985) Inheritance, organization, and mapping of rbcS and cab multigene families in pea. Proc Natl Acad Sci USA 82:5083–5087
Proudfoot N, Brownlee GG (1976) 3′ Non-coding region sequences in eukaryotic messenger RNA. Nature 263:211–214
Sheen J-Y, Bogorad L (1986) Expression of the ribulose-1,5-bisphosphate carboxylase large subunit gene and three small subunit genes in two cell types of maize leaves. EMBO J 5:3417–3422
Shinozaki K, Sasaki Y, Sakihama T, Kamikubo T (1982) Coordinate light-induction of two mRNAs, encoded in nuclei and chloroplasts, of ribulose-1,5-bisphosphate carboxylase/oxygenase. FEBS Lett 144:73–76
Southern EM (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98:503–51
Stiekema WS, Wimpee CF, Tobin EM (1983) Nucleotide sequence encoding the precursor of the small subunit of ribulose-1,5-bisphosphate carboxylase from Lemna gibba L. G-3. Nucleic Acids Res 11:8051–8061
Sugita M, Gruissem W (1987) Developmental, organ-specific and light-dependent expression of the tomato ribulose-1,5-bisphosphate carboxylase small subunit gene family. Proc Natl Acad Sci USA (in press)
Sugita M, Sugiura M (1984) Nucleotide sequence and transcription of the gene for the 32,000 dalton thylakoid membrane protein from Nicotiana tabacum. Mol Gen Genet 195:308–313
Timko MP, Klausch AP, Hand JM, Cashmore AR, Herrera-Estrella L, Van den Broeck G, Montagu MV (1985) Structure and expression of nuclear genes encoding polypeptides of the photosynthetic apparatus. In: Steinback KE, Bonitz S, Arntzen CJ, Bogorad L (eds) Molecular biology of the photosynthetic apparatus. Cold Spring Harbor Laboratory. Cold Spring Harbor, NY, pp 381–396
Tobin EM, Silverthorne J (1985) Light regulation of gene expression in higher plants. Annu Rev Plant Physiol 36:569–593
Tumer NE, Clark WG, Tabor GJ, Hironaka CM, Fraley RT, Shah DM (1986) The genes encoding the small subunit of ribulose-1,5-bisphosphate carboxylase are expressed differentially in petunia leaves. Nucleic Acids Res 14:3325–3342
Vallejos CE, Tanksley SD, Bernatzky R (1986) Localization in the tomato genome of DNA restriction fragments containing sequences homologous to the rRNA (45S), the major chlorophyll a/b binding polypeptide and the ribulose bisphosphate carboxylase genes. Genetic 112:93–105
Vieira J, Messing J (1987) The production of single-stranded plasmid DNAs. Methods Enzymol (in press)
Weiher H, Koenig M, Gruss P (1983) Multiple point mutations affecting the simian virus 40 enhancer. Science 219:626–631
Wallace RB, Shaffer J, Murphy RF, Bonner J, Hirose T, Itakura K (1979) Hybridization of synthetic oligodeoxyribonucleotides to phi X 174 DNA: the effect of single base pair mismatch. Nucleic Acids Res 6:3543–3557
Zaug A, Kent JR, Cech T (1984) A labile phosphodiester bond at the ligation junction in a circular intervening sequence RNA. Science 224:574–578
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Communicated by R.B. Goldberg
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Sugita, M., Manzara, T., Pichersky, E. et al. Genomic organization, sequence analysis and expression of all five genes encoding the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase from tomato. Molec Gen Genet 209, 247–256 (1987). https://doi.org/10.1007/BF00329650
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DOI: https://doi.org/10.1007/BF00329650