Abstract
Transcripts of three distinct ribulose-1,5-bisphosphate carboxylase (RuBPC) small subunit (SS) genes account for ∼90% of the mRNA for this protein in maize leaves. Transcripts of two of them constitute >80% of the SS mRNA in 24-h greening maize leaves. The third gene contribute ∼10%. Transcripts of all three nuclear-encoded SS genes are detectable in bundle sheath (BSC) and mesophyll cells (MC) of etiolated maize leaves. The level of mRNA for each gene is different in etioplasts of MC but all drop during photoregulated development of chloroplasts in MC and follow a pattern of transitory rise and fall in BSC. The amounts of LS and SS proteins continue to increase steadily well after the mRNA levels reach their peaks in BSC. The molar ratio of mRNA for chloroplast-encoded RuBPC large subunit (LS) to the nuclear genome encoded SS is about 10:1 although LS and SS proteins are present in about equimolar amounts.
Keywords: bundle sheath cells, cell-specific expression, light induction, mesophyll cells, multigene family
Full text
PDF





Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Ames G. F., Nikaido K. Two-dimensional gel electrophoresis of membrane proteins. Biochemistry. 1976 Feb 10;15(3):616–623. doi: 10.1021/bi00648a026. [DOI] [PubMed] [Google Scholar]
- Aoyagi K., Bassham J. A. Appearance and accumulation of c(4) carbon pathway enzymes in developing maize leaves and differentiating maize a188 callus. Plant Physiol. 1986 Feb;80(2):322–333. doi: 10.1104/pp.80.2.322. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Aoyagi K., Nakamoto H. Pyruvate, pi dikinase in bundle sheath strands as well as in mesophyll cells in maize leaves. Plant Physiol. 1985 Jul;78(3):661–664. doi: 10.1104/pp.78.3.661. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bedbrook J. R., Link G., Coen D. M., Bogorad L. Maize plastid gene expressed during photoregulated development. Proc Natl Acad Sci U S A. 1978 Jul;75(7):3060–3064. doi: 10.1073/pnas.75.7.3060. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- 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]
- Crossland L. D., Rodermel S. R., Bogorad L. Single gene for the large subunit of ribulosebisphosphate carboxylase in maize yields two differentially regulated mRNAs. Proc Natl Acad Sci U S A. 1984 Jul;81(13):4060–4064. doi: 10.1073/pnas.81.13.4060. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Dean C., van den Elzen P., Tamaki S., Dunsmuir P., Bedbrook J. Linkage and homology analysis divides the eight genes for the small subunit of petunia ribulose 1,5-bisphosphate carboxylase into three gene families. Proc Natl Acad Sci U S A. 1985 Aug;82(15):4964–4968. doi: 10.1073/pnas.82.15.4964. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dunsmuir P., Smith S., Bedbrook J. A number of different nuclear genes for the small subunit of RuBPCase are transcribed in petunia. Nucleic Acids Res. 1983 Jun 25;11(12):4177–4183. doi: 10.1093/nar/11.12.4177. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Franssen H., Goldbach R., Broekhuijsen M., Moerman M., van Kammen A. Expression of Middle-Component RNA of Cowpea Mosaic Virus: In Vitro Generation of a Precursor to Both Capsid Proteins by a Bottom-Component RNA-Encoded Protease from Infected Cells. J Virol. 1982 Jan;41(1):8–17. doi: 10.1128/jvi.41.1.8-17.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gray J. C., Kung S. D., Wildman S. G. Polypeptide chains of the large and small subunits of fraction I protein from tobacco. Arch Biochem Biophys. 1978 Jan 15;185(1):272–281. doi: 10.1016/0003-9861(78)90167-4. [DOI] [PubMed] [Google Scholar]
- Gray L. A., Jr, Fulton R. L., Srivastava T. N., Flowers N. C. Surgical treatment of thrombosed Björk-Shiley aortic valve prosthesis. J Thorac Cardiovasc Surg. 1976 Mar;71(3):429–432. [PubMed] [Google Scholar]
- Gubler U., Hoffman B. J. A simple and very efficient method for generating cDNA libraries. Gene. 1983 Nov;25(2-3):263–269. doi: 10.1016/0378-1119(83)90230-5. [DOI] [PubMed] [Google Scholar]
- Hightower R. C., Meagher R. B. Divergence and differential expression of soybean actin genes. EMBO J. 1985 Jan;4(1):1–8. doi: 10.1002/j.1460-2075.1985.tb02309.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Huber S. C., Hall T. C., Edwards G. E. Differential Localization of Fraction I Protein between Chloroplast Types. Plant Physiol. 1976 May;57(5):730–733. doi: 10.1104/pp.57.5.730. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Inamine G., Nash B., Weissbach H., Brot N. 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 U S A. 1985 Sep;82(17):5690–5694. doi: 10.1073/pnas.82.17.5690. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
- Lamppa G. K., Bendich A. J. Changes in Chloroplast DNA Levels during Development of Pea (Pisum sativum). Plant Physiol. 1979 Jul;64(1):126–130. doi: 10.1104/pp.64.1.126. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Link G., Coen D. M., Bogorad L. Differential expression of the gene for the large subunit of ribulose bisphosphate carboxylase in maize leaf cell types. Cell. 1978 Nov;15(3):725–731. doi: 10.1016/0092-8674(78)90258-1. [DOI] [PubMed] [Google Scholar]
- Maas R. An improved colony hybridization method with significantly increased sensitivity for detection of single genes. Plasmid. 1983 Nov;10(3):296–298. doi: 10.1016/0147-619x(83)90045-8. [DOI] [PubMed] [Google Scholar]
- Nagy F., Morelli G., Fraley R. T., Rogers S. G., Chua N. H. Photoregulated expression of a pea rbcS gene in leaves of transgenic plants. EMBO J. 1985 Dec 1;4(12):3063–3068. doi: 10.1002/j.1460-2075.1985.tb04046.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nelson T., Harpster M. H., Mayfield S. P., Taylor W. C. Light-regulated gene expression during maize leaf development. J Cell Biol. 1984 Feb;98(2):558–564. doi: 10.1083/jcb.98.2.558. [DOI] [PMC free article] [PubMed] [Google Scholar]
- O'Farrell P. H. High resolution two-dimensional electrophoresis of proteins. J Biol Chem. 1975 May 25;250(10):4007–4021. [PMC free article] [PubMed] [Google Scholar]
- Parnes J. R., Velan B., Felsenfeld A., Ramanathan L., Ferrini U., Appella E., Seidman J. G. Mouse beta 2-microglobulin cDNA clones: a screening procedure for cDNA clones corresponding to rare mRNAs. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2253–2257. doi: 10.1073/pnas.78.4.2253. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Polans N. O., Weeden N. F., Thompson W. F. Inheritance, organization, and mapping of rbcS and cab multigene families in pea. Proc Natl Acad Sci U S A. 1985 Aug;82(15):5083–5087. doi: 10.1073/pnas.82.15.5083. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rodermel S. R., Bogorad L. Maize plastid photogenes: mapping and photoregulation of transcript levels during light-induced development. J Cell Biol. 1985 Feb;100(2):463–476. doi: 10.1083/jcb.100.2.463. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Roy H., Bloom M., Milos P., Monroe M. Studies on the assembly of large subunits of ribulose bisphosphate carboxylase in isolated pea chloroplasts. J Cell Biol. 1982 Jul;94(1):20–27. doi: 10.1083/jcb.94.1.20. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schuster G., Ohad I., Martineau B., Taylor W. C. Differentiation and development of bundle sheath and mesophyll thylakoids in maize. Thylakoid polypeptide composition, phosphorylation, and organization of photosystem II. J Biol Chem. 1985 Sep 25;260(21):11866–11873. [PubMed] [Google Scholar]
- Sheen J. Y., Bogorad L. Differential expression of six light-harvesting chlorophyll a/b binding protein genes in maize leaf cell types. Proc Natl Acad Sci U S A. 1986 Oct;83(20):7811–7815. doi: 10.1073/pnas.83.20.7811. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sheen J. Y., Bogorad L. Differential expression of the ribulose bisphosphate carboxylase large subunit gene in bundle sheath and mesophyll cells of developing maize leaves is influenced by light. Plant Physiol. 1985 Dec;79(4):1072–1076. doi: 10.1104/pp.79.4.1072. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Timko M. P., Kausch A. P., Castresana C., Fassler J., Herrera-Estrella L., Van den Broeck G., Van Montagu M., Schell J., Cashmore A. R. Light regulation of plant gene expression by an upstream enhancer-like element. Nature. 1985 Dec 12;318(6046):579–582. doi: 10.1038/318579a0. [DOI] [PubMed] [Google Scholar]
- Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhu Y. S., Kung S. D., Bogorad L. Phytochrome control of levels of mRNA complementary to plastid and nuclear genes of maize. Plant Physiol. 1985 Oct;79(2):371–376. doi: 10.1104/pp.79.2.371. [DOI] [PMC free article] [PubMed] [Google Scholar]