Abstract
An Arabidopsis cDNA (Atrbp33) encoding a nuclear-encoded chloroplast RNA-binding protein (RBP) has been isolated (A.J. DeLisle [1993] Plant Physiol 102: 313-314). ATRBP33 shares global structural homology with all known chloroplast RBPs: a chloroplast transit peptide in the amino terminus, followed by a unique acidic domain and a tandem pair of ribonucleoprotein consensus sequence-type RNA-binding domains in the carboxyl end. In vitro translation products of Atrbp33 were found to be imported into chloroplasts, suggesting that ATRBP33 is localized in chloroplasts. The expression of Atrbp33 was higher in chloroplast-containing organs than in nonchloroplast-containing organs. Furthermore, Atrbp33 was expressed in a light-dependent manner. These features are consistent with its postulated role in posttranscriptional control of chloroplast genes. Northern analyses and RNase protection assays showed that as many as nine messages are encoded by the single Atrbp33 gene. Sequence analysis of the cDNAs indicated that some of the transcripts have truncated 5' ends. Most interestingly, the multiple mRNAs potentially encode different polypeptides, one of which lacks a chloroplast transit peptide and acidic domain and contains only one intact RNA-binding domain. Unlike the chloroplast-localized ATRBP33, the truncated polypeptide may function in other cellular compartments.
Full Text
The Full Text of this article is available as a PDF (3.3 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Adams C. C., Stern D. B. Control of mRNA stability in chloroplasts by 3' inverted repeats: effects of stem and loop mutations on degradation of psbA mRNA in vitro. Nucleic Acids Res. 1990 Oct 25;18(20):6003–6010. doi: 10.1093/nar/18.20.6003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bandziulis R. J., Swanson M. S., Dreyfuss G. RNA-binding proteins as developmental regulators. Genes Dev. 1989 Apr;3(4):431–437. doi: 10.1101/gad.3.4.431. [DOI] [PubMed] [Google Scholar]
- Bar-Zvi D., Shagan T., Schindler U., Cashmore A. R. RNP-T, a ribonucleoprotein from Arabidopsis thaliana, contains two RNP-80 motifs and a novel acidic repeat arranged in an alpha-helix conformation. Plant Mol Biol. 1992 Dec;20(5):833–838. doi: 10.1007/BF00027154. [DOI] [PubMed] [Google Scholar]
- Barkan A. Nuclear Mutants of Maize with Defects in Chloroplast Polysome Assembly Have Altered Chloroplast RNA Metabolism. Plant Cell. 1993 Apr;5(4):389–402. doi: 10.1105/tpc.5.4.389. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cline K., Fulsom D. R., Viitanen P. V. An imported thylakoid protein accumulates in the stroma when insertion into thylakoids is inhibited. J Biol Chem. 1989 Aug 25;264(24):14225–14232. [PubMed] [Google Scholar]
- Cline K. Import of proteins into chloroplasts. Membrane integration of a thylakoid precursor protein reconstituted in chloroplast lysates. J Biol Chem. 1986 Nov 5;261(31):14804–14810. [PubMed] [Google Scholar]
- Cook W. B., Walker J. C. Identification of a maize nucleic acid-binding protein (NBP) belonging to a family of nuclear-encoded chloroplast proteins. Nucleic Acids Res. 1992 Jan 25;20(2):359–364. doi: 10.1093/nar/20.2.359. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Danon A., Mayfield S. P. Light regulated translational activators: identification of chloroplast gene specific mRNA binding proteins. EMBO J. 1991 Dec;10(13):3993–4001. doi: 10.1002/j.1460-2075.1991.tb04974.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Deng X. W., Stern D. B., Tonkyn J. C., Gruissem W. Plastid run-on transcription. Application to determine the transcriptional regulation of spinach plastid genes. J Biol Chem. 1987 Jul 15;262(20):9641–9648. [PubMed] [Google Scholar]
- Didier D. K., Klee H. J. Identification of an Arabidopsis DNA-binding protein with homology to nucleolin. Plant Mol Biol. 1992 Mar;18(5):977–979. doi: 10.1007/BF00019212. [DOI] [PubMed] [Google Scholar]
- Gruissem W. Chloroplast gene expression: how plants turn their plastids on. Cell. 1989 Jan 27;56(2):161–170. doi: 10.1016/0092-8674(89)90889-1. [DOI] [PubMed] [Google Scholar]
- Hirose T., Sugita M., Sugiura M. cDNA structure, expression and nucleic acid-binding properties of three RNA-binding proteins in tobacco: occurrence of tissue-specific alternative splicing. Nucleic Acids Res. 1993 Aug 25;21(17):3981–3987. doi: 10.1093/nar/21.17.3981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kuchka M. R., Goldschmidt-Clermont M., van Dillewijn J., Rochaix J. D. Mutation at the Chlamydomonas nuclear NAC2 locus specifically affects stability of the chloroplast psbD transcript encoding polypeptide D2 of PS II. Cell. 1989 Sep 8;58(5):869–876. doi: 10.1016/0092-8674(89)90939-2. [DOI] [PubMed] [Google Scholar]
- Leutwiler L. S., Meyerowitz E. M., Tobin E. M. Structure and expression of three light-harvesting chlorophyll a/b-binding protein genes in Arabidopsis thaliana. Nucleic Acids Res. 1986 May 27;14(10):4051–4064. doi: 10.1093/nar/14.10.4051. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Li Y. Q., Sugiura M. Three distinct ribonucleoproteins from tobacco chloroplasts: each contains a unique amino terminal acidic domain and two ribonucleoprotein consensus motifs. EMBO J. 1990 Oct;9(10):3059–3066. doi: 10.1002/j.1460-2075.1990.tb07502.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Li Y., Nagayoshi S., Sugita M., Sugiura M. Structure and expression of the tobacco nuclear gene encoding the 33 kDa chloroplast ribonucleoprotein. Mol Gen Genet. 1993 May;239(1-2):304–309. doi: 10.1007/BF00281632. [DOI] [PubMed] [Google Scholar]
- Ludevid M. D., Freire M. A., Gómez J., Burd C. G., Albericio F., Giralt E., Dreyfuss G., Pagès M. RNA binding characteristics of a 16 kDa glycine-rich protein from maize. Plant J. 1992 Nov;2(6):999–1003. [PubMed] [Google Scholar]
- Mattaj I. W. A binding consensus: RNA-protein interactions in splicing, snRNPs, and sex. Cell. 1989 Apr 7;57(1):1–3. doi: 10.1016/0092-8674(89)90164-5. [DOI] [PubMed] [Google Scholar]
- Mieszczak M., Klahre U., Levy J. H., Goodall G. J., Filipowicz W. Multiple plant RNA binding proteins identified by PCR: expression of cDNAs encoding RNA binding proteins targeted to chloroplasts in Nicotiana plumbaginifolia. Mol Gen Genet. 1992 Sep;234(3):390–400. doi: 10.1007/BF00538698. [DOI] [PubMed] [Google Scholar]
- Monod C., Goldschmidt-Clermont M., Rochaix J. D. Accumulation of chloroplast psbB RNA requires a nuclear factor in Chlamydomonas reinhardtii. Mol Gen Genet. 1992 Feb;231(3):449–459. doi: 10.1007/BF00292715. [DOI] [PubMed] [Google Scholar]
- Murray M. G., Thompson W. F. Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res. 1980 Oct 10;8(19):4321–4325. doi: 10.1093/nar/8.19.4321. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nairn C. J., Winesett L., Ferl R. J. Nucleotide sequence of an actin gene from Arabidopsis thaliana. Gene. 1988 May 30;65(2):247–257. doi: 10.1016/0378-1119(88)90461-1. [DOI] [PubMed] [Google Scholar]
- Nietfeld W., Mentzel H., Pieler T. The Xenopus laevis poly(A) binding protein is composed of multiple functionally independent RNA binding domains. EMBO J. 1990 Nov;9(11):3699–3705. doi: 10.1002/j.1460-2075.1990.tb07582.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Preugschat F., Wold B. Isolation and characterization of a Xenopus laevis C protein cDNA: structure and expression of a heterogeneous nuclear ribonucleoprotein core protein. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9669–9673. doi: 10.1073/pnas.85.24.9669. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rochaix J. D. Post-transcriptional steps in the expression of chloroplast genes. Annu Rev Cell Biol. 1992;8:1–28. doi: 10.1146/annurev.cb.08.110192.000245. [DOI] [PubMed] [Google Scholar]
- Sachs A. B., Davis R. W., Kornberg R. D. A single domain of yeast poly(A)-binding protein is necessary and sufficient for RNA binding and cell viability. Mol Cell Biol. 1987 Sep;7(9):3268–3276. doi: 10.1128/mcb.7.9.3268. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Salvador M. L., Klein U., Bogorad L. Light-regulated and endogenous fluctuations of chloroplast transcript levels in Chlamydomonas. Regulation by transcription and RNA degradation. Plant J. 1993 Feb;3(2):213–219. doi: 10.1046/j.1365-313x.1993.t01-13-00999.x. [DOI] [PubMed] [Google Scholar]
- Scherly D., Boelens W., Dathan N. A., van Venrooij W. J., Mattaj I. W. Major determinants of the specificity of interaction between small nuclear ribonucleoproteins U1A and U2B'' and their cognate RNAs. Nature. 1990 Jun 7;345(6275):502–506. doi: 10.1038/345502a0. [DOI] [PubMed] [Google Scholar]
- Sieburth L. E., Berry-Lowe S., Schmidt G. W. Chloroplast RNA Stability in Chlamydomonas: Rapid Degradation of psbB and psbC Transcripts in Two Nuclear Mutants. Plant Cell. 1991 Feb;3(2):175–189. doi: 10.1105/tpc.3.2.175. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Smith C. W., Patton J. G., Nadal-Ginard B. Alternative splicing in the control of gene expression. Annu Rev Genet. 1989;23:527–577. doi: 10.1146/annurev.ge.23.120189.002523. [DOI] [PubMed] [Google Scholar]
- Stern D. B., Gruissem W. Chloroplast mRNA 3' end maturation is biochemically distinct from prokaryotic mRNA processing. Plant Mol Biol. 1989 Dec;13(6):615–625. doi: 10.1007/BF00016017. [DOI] [PubMed] [Google Scholar]
- Stern D. B., Gruissem W. Control of plastid gene expression: 3' inverted repeats act as mRNA processing and stabilizing elements, but do not terminate transcription. Cell. 1987 Dec 24;51(6):1145–1157. doi: 10.1016/0092-8674(87)90600-3. [DOI] [PubMed] [Google Scholar]
- Stern D. B., Jones H., Gruissem W. Function of plastid mRNA 3' inverted repeats. RNA stabilization and gene-specific protein binding. J Biol Chem. 1989 Nov 5;264(31):18742–18750. [PubMed] [Google Scholar]
- Stern D. B., Radwanski E. R., Kindle K. L. A 3' stem/loop structure of the Chlamydomonas chloroplast atpB gene regulates mRNA accumulation in vivo. Plant Cell. 1991 Mar;3(3):285–297. doi: 10.1105/tpc.3.3.285. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ye L. H., Li Y. Q., Fukami-Kobayashi K., Go M., Konishi T., Watanabe A., Sugiura M. Diversity of a ribonucleoprotein family in tobacco chloroplasts: two new chloroplast ribonucleoproteins and a phylogenetic tree of ten chloroplast RNA-binding domains. Nucleic Acids Res. 1991 Dec 11;19(23):6485–6490. doi: 10.1093/nar/19.23.6485. [DOI] [PMC free article] [PubMed] [Google Scholar]