Abstract
Most plastid gene products do not accumulate to high levels in meristem proplastids or in the specialized plastids of roots. To assess whether a modulation of plastid splicing activities might play a role in this tissue-dependent expression of the plastid genome, the ratio of spliced to unspliced transcripts from the atpF, petB, petD, and rpl16 genes was compared between several tissues of maize. Although these transcripts are predominantly spliced in green leaf tissue (both bundle sheath and mesophyll cells), spliced atpF, petB, and petD transcripts are underrepresented relative to their unspliced precursors in roots and leaf meristems. The ratio of spliced to unspliced rpl16 transcripts varies in a similar fashion, but the magnitude of the differences between tissues is not as great. The proportion of RNA that is spliced reflects the tissue of origin and not photosynthetic competency, chlorophyll content, or exposure to light since the leaves of photosynthetic mutants and of seedlings grown in the absence of light contain spliced and unspliced transcripts in normal ratios. These results raise the possibility that low RNA splicing activities are in part responsible for the limited expression of the plastid genome in meristematic and root tissue.
Full Text
The Full Text of this article is available as a PDF (3.4 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Baker N. R., Leech R. M. Development of Photosystem I and Photosystem II Activities in Leaves of Light-grown Maize (Zea mays). Plant Physiol. 1977 Oct;60(4):640–644. doi: 10.1104/pp.60.4.640. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Barkan A. Proteins encoded by a complex chloroplast transcription unit are each translated from both monocistronic and polycistronic mRNAs. EMBO J. 1988 Sep;7(9):2637–2644. doi: 10.1002/j.1460-2075.1988.tb03116.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bingham P. M., Chou T. B., Mims I., Zachar Z. On/off regulation of gene expression at the level of splicing. Trends Genet. 1988 May;4(5):134–138. doi: 10.1016/0168-9525(88)90136-9. [DOI] [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., Leech R. M. Genome Expression during Normal Leaf Development : I. CELLULAR AND CHLOROPLAST NUMBERS AND DNA, RNA, AND PROTEIN LEVELS IN TISSUES OF DIFFERENT AGES WITHIN A SEVEN-DAY-OLD WHEAT LEAF. Plant Physiol. 1982 Apr;69(4):904–910. doi: 10.1104/pp.69.4.904. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Deng X. W., Gruissem W. Constitutive transcription and regulation of gene expression in non-photosynthetic plastids of higher plants. EMBO J. 1988 Nov;7(11):3301–3308. doi: 10.1002/j.1460-2075.1988.tb03200.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Feinberg A. P., Vogelstein B. "A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity". Addendum. Anal Biochem. 1984 Feb;137(1):266–267. doi: 10.1016/0003-2697(84)90381-6. [DOI] [PubMed] [Google Scholar]
- Fromm H., Devic M., Fluhr R., Edelman M. Control of psbA gene expression: in mature Spirodela chloroplasts light regulation of 32-kd protein synthesis is independent of transcript level. EMBO J. 1985 Feb;4(2):291–295. doi: 10.1002/j.1460-2075.1985.tb03628.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hanley-Bowdoin L., Orozco E. M., Jr, Chua N. H. In vitro synthesis and processing of a maize chloroplast transcript encoded by the ribulose 1,5-bisphosphate carboxylase large subunit gene. Mol Cell Biol. 1985 Oct;5(10):2733–2745. doi: 10.1128/mcb.5.10.2733. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hollingsworth M. J., Johanningmeier U., Karabin G. D., Stiegler G. L., Hallick R. B. Detection of multiple, unspliced precursor mRNA transcripts for the Mr 32,000 thylakoid membrane protein from Euglena gracilis chloroplasts. Nucleic Acids Res. 1984 Feb 24;12(4):2001–2017. doi: 10.1093/nar/12.4.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hudson G. S., Mason J. G., Holton T. A., Koller B., Cox G. B., Whitfeld P. R., Bottomley W. A gene cluster in the spinach and pea chloroplast genomes encoding one CF1 and three CF0 subunits of the H+-ATP synthase complex and the ribosomal protein S2. J Mol Biol. 1987 Jul 20;196(2):283–298. doi: 10.1016/0022-2836(87)90690-5. [DOI] [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]
- Jolly S. O., McIntosh L., Link G., Bogorad L. Differential transcription in vivo and in vitro of two adjacent maize chloroplast genes: The large subunit of ribulosebisphosphate carboxylase and the 2.2-kilobase gene. Proc Natl Acad Sci U S A. 1981 Nov;78(11):6821–6825. doi: 10.1073/pnas.78.11.6821. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Klein R. R., Mullet J. E. Regulation of chloroplast-encoded chlorophyll-binding protein translation during higher plant chloroplast biogenesis. J Biol Chem. 1986 Aug 25;261(24):11138–11145. [PubMed] [Google Scholar]
- Koller B., Clarke J., Delius H. The structure of precursor mRNAs and of excised intron RNAs in chloroplasts of Euglena gracilis. EMBO J. 1985 Oct;4(10):2445–2450. doi: 10.1002/j.1460-2075.1985.tb03954.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Leech R. M., Rumsby M. G., Thomson W. W. Plastid differentiation, acyl lipid, and Fatty Acid changes in developing green maize leaves. Plant Physiol. 1973 Sep;52(3):240–245. doi: 10.1104/pp.52.3.240. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mullet J. E., Klein R. R. Transcription and RNA stability are important determinants of higher plant chloroplast RNA levels. EMBO J. 1987 Jun;6(6):1571–1579. doi: 10.1002/j.1460-2075.1987.tb02402.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rock C. D., Barkan A., Taylor W. C. The maize plastid psbB-psbF-petB-petD gene cluster: spliced and unspliced petB and petD RNAs encode alternative products. Curr Genet. 1987;12(1):69–77. doi: 10.1007/BF00420729. [DOI] [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]
- Rodermel S. R., Bogorad L. Molecular evolution and nucleotide sequences of the maize plastid genes for the alpha subunit of CF1 (atpA) and the proteolipid subunit of CF0 (atpH). Genetics. 1987 May;116(1):127–139. doi: 10.1093/genetics/116.1.127. [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 in Bundle Sheath and Mesophyll Cells of Maize of Genes for Photosystem II Components Encoded by the Plastid Genome. Plant Physiol. 1988 Apr;86(4):1020–1026. doi: 10.1104/pp.86.4.1020. [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]
- Tanaka M, Obokata J, Chunwongse J, Shinozaki K, Sugiura M. Rapid splicing and stepwise processing of a transcript from the psbB operon in tobacco chloroplasts: determination of the intron sites in petB and petD. Mol Gen Genet. 1987 Oct;209(3):427–431. doi: 10.1007/BF00331145. [DOI] [PubMed] [Google Scholar]
- Westhoff P., Farchaus J. W., Herrmann R. G. The gene for the Mr 10,000 phosphoprotein associated with photosystem II is part of the psbB operon of the spinach plastid chromosome. Curr Genet. 1986;11(3):165–169. doi: 10.1007/BF00420602. [DOI] [PubMed] [Google Scholar]
- Westhoff P., Herrmann R. G. Complex RNA maturation in chloroplasts. The psbB operon from spinach. Eur J Biochem. 1988 Feb 1;171(3):551–564. doi: 10.1111/j.1432-1033.1988.tb13824.x. [DOI] [PubMed] [Google Scholar]
- de Boer D., Cremers F., Teertstra R., Smits L., Hille J., Smeekens S., Weisbeek P. In vivo import of plastocyanin and a fusion protein into developmentally different plastids of transgenic plants. EMBO J. 1988 Sep;7(9):2631–2635. doi: 10.1002/j.1460-2075.1988.tb03115.x. [DOI] [PMC free article] [PubMed] [Google Scholar]