Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1987 Oct;84(20):7104–7108. doi: 10.1073/pnas.84.20.7104

Developmental, organ-specific, and light-dependent expression of the tomato ribulose-1,5-bisphosphate carboxylase small subunit gene family.

M Sugita 1, W Gruissem 1
PMCID: PMC299238  PMID: 3478683

Abstract

The tomato gene family for the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase [3-phospho-D-glycerate carboxy-lyase (dimerizing); EC 4.1.1.39] has five genes, designated Rbcs-1, -2, -3A, -3B, and -3C. We have measured the steady-state mRNA levels for each of the five genes in various tomato organs using gene-specific oligonucleotides. All five genes are highly expressed in leaves, and transcripts of two genes, Rbcs-3B and Rbcs-3C, account for approximately equal to 60% of the total leaf transcripts. The relative transcript levels in the stem, in nature fruits, and etiolated seedlings (plants germinated and grown in the dark) correspond to 3.2%, 6.5%, and 4.6%, respectively, of the ribulose-1,5-bisphosphate carboxylase/oxygenase small subunit mRNA level in leaves, and no transcripts have been detected in roots and ripe tomato fruits. Only Rbcs-1 and Rbcs-2 are expressed during the photosynthetically active phase of fruit development. Transcripts from these genes and from the Rbcs-3A locus are also present in etiolated seedlings. Rbcs-3B and Rbcs-3C transcripts, which are the most abundant mRNAs of the ribulose-1,5-bisphosphate carboxylase/oxygenase small subunit gene family in the leaf, are undetectable in dark-grown seedlings and immature fruit. The selective expression of Rbcs-1 and Rbcs-2 in the dark and in the pericarp of green fruit and the induction and rapid mRNA accumulation for Rbcs-3B and Rbcs-3C after illumination may reflect different regulatory mechanism(s) that control the expression of individual members in the tomato ribulose-1,5-bisphosphate carboxylase/oxygenase small subunit gene family.

Full text

PDF
7104

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Berry-Lowe S. L., Mc Knight T. D., Shah D. M., Meagher R. B. 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. 1982;1(6):483–498. [PubMed] [Google Scholar]
  2. Berry-Lowe S. L., Meagher R. B. Transcriptional regulation of a gene encoding the small subunit of ribulose-1,5-bisphosphate carboxylase in soybean tissue is linked to the phytochrome response. Mol Cell Biol. 1985 Aug;5(8):1910–1917. doi: 10.1128/mcb.5.8.1910. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Berry J. O., Nikolau B. J., Carr J. P., Klessig D. F. Transcriptional and post-transcriptional regulation of ribulose 1,5-bisphosphate carboxylase gene expression in light- and dark-grown amaranth cotyledons. Mol Cell Biol. 1985 Sep;5(9):2238–2246. doi: 10.1128/mcb.5.9.2238. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Berry J. O., Nikolau B. J., Carr J. P., Klessig D. F. Translational regulation of light-induced ribulose 1,5-bisphosphate carboxylase gene expression in amaranth. Mol Cell Biol. 1986 Jul;6(7):2347–2353. doi: 10.1128/mcb.6.7.2347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Coen D. M., Bedbrook J. R., Bogorad L., Rich A. Maize chloroplast DNA fragment encoding the large subunit of ribulosebisphosphate carboxylase. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5487–5491. doi: 10.1073/pnas.74.12.5487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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. 1984 Aug;3(8):1671–1679. doi: 10.1002/j.1460-2075.1984.tb02031.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dean C., 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. 1985 Dec 1;4(12):3055–3061. doi: 10.1002/j.1460-2075.1985.tb04045.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Deng X. W., Gruissem W. Control of plastid gene expression during development: the limited role of transcriptional regulation. Cell. 1987 May 8;49(3):379–387. doi: 10.1016/0092-8674(87)90290-x. [DOI] [PubMed] [Google Scholar]
  9. Fluhr R., Kuhlemeier C., Nagy F., Chua N. H. Organ-specific and light-induced expression of plant genes. Science. 1986 May 30;232(4754):1106–1112. doi: 10.1126/science.232.4754.1106. [DOI] [PubMed] [Google Scholar]
  10. Fluhr Robert, Moses Phyllis, Morelli Giorgio, Coruzzi Gloria, Chua Nam-Hai. Expression dynamics of the pea rbcS multigene family and organ distribution of the transcripts. EMBO J. 1986 Sep;5(9):2063–2071. doi: 10.1002/j.1460-2075.1986.tb04467.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gallagher T. F., Ellis R. J. Light-stimulated transcription of genes for two chloroplast polypeptides in isolated pea leaf nuclei. EMBO J. 1982;1(12):1493–1498. doi: 10.1002/j.1460-2075.1982.tb01345.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gruissem W., Zurawski G. Identification and mutational analysis of the promoter for a spinach chloroplast transfer RNA gene. EMBO J. 1985 Jul;4(7):1637–1644. doi: 10.1002/j.1460-2075.1985.tb03831.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Pichersky E., Bernatzky R., Tanksley S. D., Cashmore A. R. 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 U S A. 1986 Jun;83(11):3880–3884. doi: 10.1073/pnas.83.11.3880. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Piechulla B., Glick R. E., Bahl H., Melis A., Gruissem W. Changes in Photosynthetic Capacity and Photosynthetic Protein Pattern during Tomato Fruit Ripening. Plant Physiol. 1987 Jul;84(3):911–917. doi: 10.1104/pp.84.3.911. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Sasaki Y., Sakihama T., Kamikubo T., Shinozaki K. Phytochrome-mediated regulation of two mRNAs, encoded by nuclei and chloroplasts of ribulose-1,5-bisphosphate carboxylase/oxygenase. Eur J Biochem. 1983 Jul 1;133(3):617–620. doi: 10.1111/j.1432-1033.1983.tb07507.x. [DOI] [PubMed] [Google Scholar]
  16. Sheen J. Y., Bogorad L. 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. 1986 Dec 20;5(13):3417–3422. doi: 10.1002/j.1460-2075.1986.tb04663.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Shinozaki K., Sugiura M. The nucleotide sequence of the tobacco chloroplast gene for the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase. Gene. 1982 Nov;20(1):91–102. doi: 10.1016/0378-1119(82)90090-7. [DOI] [PubMed] [Google Scholar]
  18. Silverthorne J., Tobin E. M. Demonstration of transcriptional regulation of specific genes by phytochrome action. Proc Natl Acad Sci U S A. 1984 Feb;81(4):1112–1116. doi: 10.1073/pnas.81.4.1112. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Vallejos C. E., Tanksley S. D., Bernatzky R. 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. Genetics. 1986 Jan;112(1):93–105. doi: 10.1093/genetics/112.1.93. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Wallace R. B., Shaffer J., Murphy R. F., Bonner J., Hirose T., Itakura K. Hybridization of synthetic oligodeoxyribonucleotides to phi chi 174 DNA: the effect of single base pair mismatch. Nucleic Acids Res. 1979 Aug 10;6(11):3543–3557. doi: 10.1093/nar/6.11.3543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Zurawski G., Perrot B., Bottomley W., Whitfeld P. R. The structure of the gene for the large subunit of ribulose 1,5-bisphosphate carboxylase from spinach chloroplast DNA. Nucleic Acids Res. 1981 Jul 24;9(14):3251–3270. doi: 10.1093/nar/9.14.3251. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES