3'-processed mRNA is preferentially translated in Chlamydomonas reinhardtii chloroplasts

Molecular and Cellular Biology

Volumn 18, Issue 8, 1998, Pages 4605-4611

  Rott, Ruth ^a   Levy, Haim ^b,c   Drager, Robert G ^b   Stern, David B ^b   Schuster, Gadi ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^b Boyce Thompson Institute for Plant Research   (United States)

^c ISRAEL INSTITUTE FOR BIOLOGICAL RESEARCH   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; MESSENGER RNA;

ARTICLE; CHLAMYDOMONAS REINHARDTII; CHLOROPLAST; CONTROLLED STUDY; NONHUMAN; POLYMERASE CHAIN REACTION; POLYSOME; PRIORITY JOURNAL; TRANSLATION INITIATION;

CHLAMYDOMONAS REINHARDTII;

EID: 0031830328     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.18.8.4605     Document Type: Article

References (53)

1. Audren, H., C. Bisanz-Seyer, J. F. Briat, and R. Mache. 1987. Structure and transcription of the 5S ribosomal RNA gene from spinach chloroplasts. Curr. Genet. 12:263-270.
2. Barkan, A. 1993. Nuclear mutants of maize with defects in chloroplast polysome assembly have altered chloroplast RNA metabolism. Plant Cell 5:389-402.
3. Barkan, A. 1988. Proteins encoded by a complex chloroplast transcription unit are each translated from both monocistronic and polycistronic RNAs. EMBO J. 7:2637-2644.
4. Barkan, A. 1989. Tissue-dependent plastid RNA splicing in maize: transcripts from four plastid genes are predominantly unspliced in leaf meristems and roots. Plant Cell 1:437-446.
5. Blowers, A. D., U. Klein, G. S. Ellmore, and L. Bogorad. 1993. Functional in vivo analyses of the 3′ flanking sequences of the Chlamydomonas chloroplast rbcL and psaB genes. Mol. Gen. Genet. 238:339-349.
6. Breidenbach, E., E. Jenni, and A. Boschetti. 1988. Synthesis of two proteins in chloroplasts and mRNA distribution between thylakoids and stroma during the cell cycle of Chlamydomonas reinhardtii. Eur. J. Biochem. 177:225-232.
7. Choquet, Y., M. Goldschmidt-Clermont, J. Girard-Bascou, U. Kueck, P. Bennoun, and J. D. Rochaix. 1988. Mutant phenotypes support a trans-splicing mechanism for the expression of the tripartite psaA gene in the Chlamydomonas reinhardtii chloroplast. Cell 52:903-914.
8. Christensen, A. K., L. E. Kahn, and C. M. Bourne. 1987. Circular polysomes predominate on the rough endoplasmic reticulum of somatotropes and mammotropes in the rat anterior pituitary. Am. J. Anat. 178:1-10.
9. Copertino, D. W., and R. B. Hallick. 1991. Group II twintron: an intron within an intron in a chloroplast cytochrome b-559 gene. EMBO J. 10:433-442.
10. Craig, A., A. Haghighat, A. Yu, and N. Sonenberg. 1998. Interaction of polyadenylate-binding protein with eIF4G homologue PAIP enhances translation. Nature 392:520-523.
11. Deng, X., and W. Gruissem. 1988. Constitutive transcription and regulation of gene expression in non-photosynthetic plastids of higher plants. EMBO J. 7:3301-3308.
12. Drager, R. G., and D. B. Stern. Chloroplast RNA synthesis and processing. In J.-D. Rochaix, M. Goldschmidt-Clermont, and S. Merchant (ed.). Molecular biology of chlamydomonas: chloroplasts and mitochondria, in press. Kluwer Academic Publishers, Dordrecht, The Netherlands.
13. Drager, R. G., M. Zeidler, C. L. Simpson, and D. B. Stern. 1996. A chloroplast transcript lacking the 3′ inverted repeat is degraded by 3′→5́ exoribonuclease activity. RNA 2:652-663.
14. Dron, M., M. Rahire, and J.-D. Rochaix. 1982. Sequence of the chloroplast DNA region of Chlamydomonas reinhardtii containing the large subunit of riboluse bisphosphate carboxylase and part of its flanking genes. J. Mol. Biol. 162:775-793.
15. Franch, T., and K. Gerdes. 1996. Programmed cell death in bacteria: translational repression by mRNA end-pairing. Mol. Microbiol. 21:1049-1060.
16. Gallie, D. R. 1996. Translation control of cellular and viral mRNAs. Plant Mol. Biol. 32:145-158.
17. Hayes, R., J. Kudla, G. Schuster, L. Gabay, P. Maliga, and W. Gruissem. 1996. Chloroplast mRNA 3́-end processing by a high molecular weight protein complex is regulated by nuclear encoded RNA binding proteins. EMBO J. 15:1132-1141.
18. Hentze, M. W. 1997. eIF4G: a multipurpose ribosome adapter? Science 275:500-501.
19. Hirose, T., and M. Sugiura. 1997. Both RNA editing and RNA cleavage are required for translation of tobacco ndhD mRNA: a possible regulatory mechanism for the expression of chloroplast operon consisting of functionally unrelated genes. EMBO J. 16:6804-6811.
20. Hirose, T., and M. Sugiura. 1996. cis-acting elements and trans-acting factors for accurate translation of chloroplast psbA mRNAs: development of an in vitro translation system from tobacco chloroplasts. EMBO J. 15:1687-1695.
21. Jackson, R. J., and N. Standart. 1990. Do the poly(A) tail and 3′ untranslated region control mRNA translation? Cell 62:15-24.
22. Keus, R. J. A., A. F. Dekker, K. C. J. Kreuk, and G. S. P. Groot. 1986. Transcription of ribosomal DNA in chloroplasts of Spirodela oligorhiza. Curr. Genet. 9:91-98.
23. Kindle, K. L., H. Suzuki, and D. B. Stern. 1994. Gene amplification can correct a photosynthetic growth defect caused by mRNA instability in Chlamydomonas chloroplasts. Plant Cell 6:187-200.
24. Klaff, P., and W. Gruissem. 1991. Changes in chloroplast mRNA stability during leaf development. Plant Cell 3:517-530.
25. Klein, R. R., H. S. Mason, and J. E. Mullet. 1988. Light-regulated translation of chloroplast proteins. I. Transcripts of psaA-psaB, psbA, and rbcL are associated with polysomes in dark-grown and illuminated barley seedlings. J. Cell Biol. 106:289-301.
26. Kuck, U., Y. Choquet, M. Schneider, M. Dron, and P. Bennoun. 1987. Structural and transcription analysis of two homologous genes for the p700 chlorophyll a-apoproteins in Chlamydomonas reinhardtii: evidence for in vivo trans-splicing. EMBO J. 6:2185-2196.
27. Kudla, J., R. Hayes, and W. Gruissem. 1996. Polyadenylation accelerates degradation of chloroplast mRNA. EMBO J. 15:7137-7146.
28. Leaver, C. J. 1973. Molecular integrity of chloroplast ribosomal ribonucleic acid. Biochem. J. 135:237-240.
29. Levy, H., K. L. Kindle, and D. B. Stern. 1997. A nuclear mutation that affects the 3′ processing of several mRNAs in Chlamydomonas reinhardtii chloroplasts. Plant Cell 9:825-836.
30. Lisitsky, I., P. Klaff, and G. Schuster. 1996. Addition of poly(A)-rich sequences to endonucleolytic cleavage sites in the degradation of spinach chloroplast mRNA. Proc. Natl. Acad. Sci. USA 93:13398-13403.
31. Lisitsky, I., P. Klaff, and G. Schuster. 1997. Blocking polyadenytation of mRNA in the chloroplast inhibits its degradation. Plant J. 12:1173-1178.
32. Lisitsky, I., A. Kotler, and G. Schuster. 1997. The mechanism of preferential degradation of polyadenylated RNA in the chloroplast: the exoribonuclease 100RNP/PNPase displays high binding affinity for poly(A) sequence. J. Biol. Chem. 272:17648-17653.
33. Lisitsky, I., V. Liveanu, and G. Schuster. 1995. RNA-binding characteristics of a ribonucleoprotein from spinach chloroplast. Plant Physiol. 107:933-941.
34. McGarvey, P., and R. B. Helling. 1989. Processing of chloroplast ribosomal RNA transcripts in Euglena gracilis bacillaris. Curr. Genet. 15:363-370.
35. Rochaix, J.-D. 1996. Post-transcriptional regulation of chloroplast gene expression in Chlamydomonas reinhardtii. Plant Mol. Biol. 32:327-341.
36. Rott, R., R. G. Drager, D. B. Stern, and G. Schuster. 1996. The 3′ untranslated regions of chloroplast genes in Chlamydomonas reinhardtii do not serve as efficient transcriptional terminators. Mol. Gen. Genet. 252:676-683.
37. Rott, R., V. Liveanu, R. G. Drager, D. B. Stern, and G. Schuster. 1998. The sequence and structure of the 3′ untranslated regions of chloroplast transcripts are important determinants of mRNA accumulation and stability. Plant. Mol. Biol. 36:307-314.
38. Rott, R., and N. Nelson. 1981. Purification and immunological properties of proton-ATPase complexes from yeast and rat liver mitochondria. J. Biol. Chem. 256:9224-9228.
39. Sachs, A. B., and R. W. Davis. 1989. The polyadenylic acid binding protein is required for polyadenylic acid shortening and 60S ribosomal subunit-dependent translation initiation. Cell 58:857-868.
40. Sachs, A. B., P. Sarnow, and M. W. Hentze. 1997. Starting at the beginning, middle, and end: translation initiation in eukaryotes. Cell 89:831-838.
41. Sarkar, N. 1997. Polyadenylation of mRNA in prokaryotes. Annu. Rev. Biochem. 66:173-197.
42. Schuster, G., R. Timberg, and I. Ohad. 1988. Turnover of photosystem II proteins during photoinhibition of Chlamydomonas reinhardtii. Eur. J. Biochem. 177:403-410.
43. Standart, N., and R. J. Jackson. 1994. Regulation of translation by specific protein/mRNA interactions. Biochimie 76:867-879.
44. Stern, D. B., and W. Gruissem. 1987. Control of plastid gene expression: 3′ inverted repeats act as mRNA processing and stabilizing elements, but do not terminate transcription. Cell 51:1145-1157.
45. Stern, D. B., D. C. Higgs, and J. Yang. 1997. Transcription and translation in chloroplasts. Trends Plant Sci. 2:308-315.
46. Stern, D. B., H. Jones, and W. Gruissem. 1989. Function of plastid mRNA 3′ inverted repeats: RNA stabilization and gene-specific protein binding. J. Biol. Chem. 264:18742-18750.
47. Stern, D. B., and K. L. Kindle. 1993. 3′ end maturation of the Chlamydomonas reinhardtii chloroplast atpB mRNA is a two-step process. Mol. Cell. Biol. 13:2277-2285.
48. Stern, D. B., E. R. Radwanski, and K. L. Kindle. 1991. A 3′ stem/loop structure of the Chlamydomonas chloroplast atpB gene regulates mRNA accumulation in vivo. Plant Cell 3:285-297.
49. Sugita, M., and M. Sugiura. 1996. Regulation of gene expression in chloroplasts of higher plants. Plant Mol. Biol. 32:315-326.
50. Tarum, S. Z., and A. B. Sachs. 1996. Association of yeast poly(A) tail binding protein with translation initiation factor eIF-4G. EMBO J. 15:7168-7177.
51. Thisted, T., A. K. Nielsen, and K. Gerdes. 1994. Mechanism of postsegregational killing: translation of hok, srnB, and pnd mRNAs of plasmids R1, F and R483 is activated by 3′ end processing. EMBO J. 13:1950-1959.
52. Vera, A., F. Yokoi, and M. Sugiura. 1993. The existence of pre-mature 16S rRNA species in plastid ribosomes. FEBS Lett. 327:29-31.
53. Westhoff, P., and R. G. Herrmann. 1988. Complex RNA maturation in chloroplasts: the psbB operon from spinach. Eur. J. Biochem. 171:551-564.