Abstract
The rbcS1, 2 and 3 genes of Phaseolus vulgaris are identical in coding sequence and we have studied their expression using gene-specific probes derived from their 3′ non-coding regions. The genes differ in their relative levels of expression but show only minor qualitative differences in their regulation. Transcripts of the three genes are undetectable in primary leaves in the imbibed seed, accumulate early in leaf expansion reaching a maximum 7–10 d after sowing and decrease to low levels by the time expansion is complete. Both dark-grown and light-grown primary leaves exhibit this ontogenetic pattern of expression, although the light-grown leaves have two to three times more rbcS transcripts. Light can over-ride the ontogenetic control of rbcS expression; for example, when 7-d-old dark-grown primary leaves are illuminated there is a 6- to 12-fold increase in the transcript levels of the rbcS genes. Transfer of illuminated leaves to darkness results in the loss of transcripts of all three genes, but rbcS2 transcripts persist in the dark-adapted leaves. Possible physiological mechanisms of the ontogenetic regulation of expression are discussed.
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Abbreviations
- rbcS :
-
gene encoding the small subunit of Rubisco
- Rubisco:
-
ribulose 1,5-bisphosphate carboxylase/oxygenase
References
Aoyagi K, Kuhlemeier C, Chua N-H (1988) The pea rbcS-3A promoter directs cell specific expression in transgenic tobacco. Mol Gen Genet 213: 179–185
Barnett LK, Clugston CK, Jenkins GI (1990) Two phytochromemediated effects of light on transcription of genes encoding the small subunit of ribulose 1,5-bisphosphate carboxylase-oxygenase in dark-grown pea (Pisum sativum) plants. FEBS Lett 224: 287–290
Bate NJ, Rothstein SJ, Thompson JE (1991) Expression of nuclear and chloroplast photosynthesis-specific genes during leaf senescence. J Exp Bot 42: 801–811
Binnie C (1990) The use of synthetic oligonucleotides as hybridisation probes. Adv Gen Tech 1: 135–154
Clugston CK, Barnett LK, Urwin NAR, Jenkins GI (1990) Photoreceptors controlling transcription of rbcS genes in green leaf tissue of Pisum sativum. Photochem Photobiol 52: 23–28
Dean C, Pichersky E, Dunsmuir P (1989) Structure, evolution and regulation of rbcS genes in higher plants. Annu Rev Plant Phys Plant Mol Biol 40: 415–439
Dean C, van denElzen P, Tamaki S, Dunsmuir P, Bedbrook J (1995) Differential expression of the eight genes of the petunia ribulose bisphosphate carboxylase small subunit multi-gene family. EMBO J 4: 3055–3061
Dedonder A, Rethy R, Fredericq H, VanMontagu M, Krebbers E (1993) Arabidopsis rbcS genes are differentially regulated by light. Plant Physiol 101: 801–808
Flores S, Tobin EM (1986) Benzyladenine modulation of the expression of two genes for nuclear-encoded chloroplast proteins in Lemna gibba: apparent post-transcriptional regulation. Planta 168: 340–349
Fluhr R, Chua N-H (1986) Developmental regulation of two genes encoding ribulose-bisphosphate carboxylase small subunit in pea and transgenic petunia plants: phytochrome response and blue light induction. Proc Natl Acad Sci USA 83: 2358–2362
Fluhr R, Moses P, Morelli G, Coruzzi G, Chua N-H (1986) Expression dynamics of the pea rbcS multigene family and organ distribution of the transcripts. EMBO J 5: 2063–2071
Gallagher TF, Jenkins GI, Ellis RJ (1985) Rapid modulation of transcription of nuclear genes encoding chloroplast proteins by light. FEBS Lett 186: 241–245
Gerlach WL, Bedbrook JR (1979) Cloning and characterisation of ribosomal RNA genes from wheat and barley. Nucl Acids Res 7: 1869–1885
Gilmartin PM, Sarokin L, Memelink J, Chua N-H (1990) Molecular light switches for plant genes. Plant Cell 2: 369–378
Greenland AJ, Thomas MV, Walden RM (1987) Expression of two nuclear genes encoding chloroplast proteins during early development of cucumber seedlings. Planta 170: 99–110
Jenkins GI (1986) Photoregulation of expression of genes encoding ribulose-1,5-bisphosphate carboxylase/oxygenase. Biochem Soc Trans 14: 22–25
Knight MR (1989) The structure and expression of genes encoding the small subunit of ribulose 1,5-bisphosphate carboxylase/ oxygenase in Phaseolus vulgaris L. Ph.D. thesis, University of Glasgow, UK
Knight MR, Jenkins GI (1992) 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
Krapp A, Hofmann B, Schäfer C, Stitt M (1993) Regulation of the expression of rbcS and other photosynthetic genes by carbohydrates: a mechanism for the ‘sink regulation’ of photosynthesis? Plant J 3: 817–828
Kuhlemeier C, Cuozzo M, Green PJ, Goyvaerts E, Ward K, Chua N-H (1988) Localization and conditional redundancy of regulatory elements in rbcS-3A, a pea gene encoding the small subunit of ribulose-bisphosphate carboxylase. Proc Natl Acad Sci USA 85: 4662–4666
Loza-Tavera H, Martinez-Barajas E, Sánchez-de-Jiménez E (1990) Regulation of ribulose-1,5-bisphosphate carboxylase expression in second leaves of maize seedlings from low and high yield populations. Plant Physiol 93: 541–548
Manzara T, Carrasco P, Gruissem W (1991) Developmental and organ-specific changes in promoter DNA-protein interactions in the tomato rbcS gene family. Plant Cell 3: 1305–1316
Manzara T, Gruissem W (1988) Organisation and expression of the genes encoding ribulose-1,5-bisphosphate carboxylase/oxygenase in higher plants. Photosynth Res 16: 117–139
Maxam AM, Gilbert W (1980) Sequencing end-labelled DNA with base-specific chemical cleavages. In: Grossman L, Moldave K, (eds) Methods in enzymology, vol. 65. Academic Press, New York, pp 499–560
Naito K, Tsuji H, Hatakeyama I (1979) Benzyladenine-induced increase in DNA content per cell, chloroplast size, and chloroplast number per cell in intact bean leaves. J Exp Bot 30: 1145–1151
Nelson T, Harpster MH, Mayfield SP, Taylor WC (1984) Light-regulated gene expression during maize leaf development. J Cell Biol 98: 558–564
Sawbridge TI, López-Juez E, Knight MR, Jenkins GI (1994) A blue-light photoreceptor mediates the fluence-rate-dependent expression of genes encoding the small subunit of ribulose 1,5 bisphosphate carboxylase/oxygenase in light-grown Phaseolus vulgaris primary leaves. Planta 192: 1–8
Sheen J (1990) Metabolic repression of transcription in higher plants. Plant Cell 2: 1027–1038
Shirley BW, Ham DP, Senecoff JF, Berry-Lowe SL, Zurfluh LL, Shah DM, Meagher RB (1990) 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
Silverthorne J, Tobin EM (1990) Post-transcriptional regulation of organ-specific expression of individual rbcS mRNAs in Lemna gibba. Plant Cell 2: 1181–1190
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 84: 7104–7108
Sugita M, Manzara T, Pichersky E, Cashmore AR, Gruissem W (1987) 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
Taylor WC (1989) Regulatory interactions between nuclear and plastid genomes. Annu Rev Plant Physiol Plant Mol Biol 40: 211–233
Tobin EM, Silverthorne J (1985) Light regulation of gene expression in higher plants. Annu Rev Plant Physiol 36: 569–593
Ueda T, Pichersky E, Malik VS, Cashmore AR (1989) Level of expression of the tomato rbcS3-A gene is modulated by a far upstream promoter element in a developmentally regulated manner. Plant Cell 1: 217–227
Wanner LA, Gruissem W (1991) Expression dynamics of the tomato rbcS gene family during development. Plant Cell 3: 1289–1303
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T.I.S. and M.R.K. gratefully acknowledge the award of Ph.D. studentships from the UK Science and Engineering Research Council S.E.R.C. G.I.J. thanks the S.E.R.C. and the UK Agricultural and Food Research Council for the support of his research.
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Sawbridge, T.I., Knight, M.R. & Jenkins, G.I. Ontogenetic regulation and photoregulation of members of the Phaseolus vulgaris L. rbcS gene family. Planta 198, 31–38 (1996). https://doi.org/10.1007/BF00197583
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DOI: https://doi.org/10.1007/BF00197583