In vivo evidence for 5'→ 3' exoribonuclease degradation of an unstable chloroplast mRNA

Plant Journal

Volumn 13, Issue 1, 1998, Pages 85-96

  Drager, Robert G ^a   Girard Bascou, Jacqueline ^b   Choquet, Yves ^b   Kindle, Karen L ^c   Stern, David B ^a  

^a United States Department of Agriculture Agricultural Research Service and Boyce Thompson Institute for Plant Research   (United States)

^b INST DE BIOLOGIE PHYSICO CHIMIQUE   (France)

^c Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5' EXORIBONUCLEASE; 5'-EXORIBONUCLEASE; CYTOCHROME B; CYTOCHROME B6F; EXORIBONUCLEASE; MESSENGER RNA; PLANT RNA; PRIMER DNA; PROTOZOAL RNA;

ALLELE; ANIMAL; ARTICLE; BIOLOGICAL MODEL; BIOSYNTHESIS; CHIMERA; CHLAMYDOMONAS REINHARDTII; CHLOROPLAST; CHROMOSOME MAP; GENE; GENE REARRANGEMENT; GENETICS; METABOLISM; MUTATION; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; RNA PROCESSING;

ALLELES; ANIMALS; BASE SEQUENCE; CHIMERA; CHLAMYDOMONAS REINHARDTII; CHLOROPLASTS; CHROMOSOME MAPPING; CYTOCHROME B GROUP; CYTOCHROME B6F COMPLEX; DNA PRIMERS; EXORIBONUCLEASES; GENE REARRANGEMENT; GENES, PLANT; GENES, PROTOZOAN; MODELS, BIOLOGICAL; MUTATION; POLYMERASE CHAIN REACTION; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER; RNA, PLANT; RNA, PROTOZOAN;

ANIMALIA; CHLAMYDOMONAS REINHARDTII; EMBRYOPHYTA;

EID: 0031910348     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.1998.00016.x     Document Type: Article

References (67)

1. Barkan, A. (1993) Nuclear mutants of maize with defects in chloroplast polysome assembly have altered chloroplast RNA metabolism. Plant Cell, 5, 389-402.
2. Barkan, A., Walker, M., Nolasco, M. and Johnson, D. (1994) A nuclear mutation in maize blocks the processing and translation of several chloroplast mRNAs and provides evidence for the differential translation of alternative mRNA forms. EMBO J. 13, 3170-3181.
3. Bennoun, P. and Delepelaire, P. (1982) Isolation of photosynthetic mutants in Chlamydomonas. In Methods in Chloroplast Molecular Biology (Edelman, M., Hallick, R. and Chua, N.-H., eds). Amsterdam: Elsevier, pp. 25-38.
4. Bennoun, P., Masson, A. and Delosme, M. (1980) A method for complementation analysis of nuclear and chloroplast mutants of photosynthesis in Chlamydomonas. Genet. 95, 39-47.
5. Cannistraro, V.J., Subbarao, M.N. and Kennel, D. (1986) Specific endonucleolytic cleavage sites for decay of Escherichia coll mRNA. J. Mol. Biol. 192, 257-274.
6. Carpousis, A.J., Van Houwe, G., Ehretsmann, C. and Krisch, H.M. (1994) Copurification of E. coli RNAase E and PNPase: Evidence for a specific association between two enzymes important in RNA processing and degradation. Cell. 76, 889-900.
7. Chen, X., Kindle, K. and Stern, D. (1993) Initiation codon mutations in the Chlamydomonas chloroplast petD gene result in temperature-sensitive photosynthetic growth. EMBO J. 12, 3627-3635.
8. Choquet, Y., Goldschmidt-Clermont, M., Girard-Bascou, J., Kück, U., Bennoun, P. and Rochaix, J.-D. (1988) Mutant phenotypes support a trans-splicing mechanism for the expression of the tripartite psaA gene in the C. reinhardtii chloroplast. Cell, 52, 903-913.
9. Church, G.M. and Gilbert, W. (1984) Genomic sequencing. Proc. Natl Acad. Sci. USA, 81, 1991-1995.
10. Cohen, S.N. (1995) Surprises at the 3′ end of prokaryotic RNA. Cell, 80, 829-832.
11. Danon, A. and Mayfield, S.P.Y. (1991) Light-regulated translational activators: Identification of chloroplast gene specific mRNA binding proteins. EMBO J. 10, 3993-4002.
12. Decker, C.J. and Parker, R. (1993) A turnover pathway for both stable and unstable mRNAs in yeast: Evidence for a requirement for deadenylation. Genes Dev. 7, 1632-1643.
13. Delepeiaire, P. (1983) Characterisation of additional thylakoid membrane polypeptides synthesized inside the chloroplast in Chlamydomonas reinhardtii. Photobiochem. Photobiophys. 6, 279-291.
14. Deutscher, M.P. (1993) Ribonuclease multiplicity, diversity and complexity. J. Biol. Chem. 268, 13011-13014.
15. Dieckmann, C.L., Koerner, T.J. and Tzagoloff, A. (1984) Assembly of the mitochondrial membrane system. CBP1, a yeast nuclear gene involved in 5′ end processing of cytochrome b pre-mRNA. J. Biol. Chem. 259, 4722-4731.
16. Dieckmann, C.L and Mittelmeier, T.M. (1987) Nuclearly encoded CBP1 interacts with the 5′ end of mitochondrial cytochrome b pre mRNA. Curr. Genet. 12, 391-397.
17. Dieckmann, C.L, Pape, L.K. and Tzagoloff, A. (1982) Identification and cloning of a yeast nuclear gene (CBP1) involved in expression of mitochondrial cytochrome b. Proc. Natl Acad. Act. USA, 79, 1805-1809.
18. Drager, R.G., Zeidler, M., Simpson, C.L. and Stern, D.B. (1996) A chloroplast transcript lacking the 3′ inverted repeat is degraded by 3′→5′ exoribonuclease activity. RNA, 2, 652-663.
19. Drapier, D., Girard-Bascou, J. and Wollman, F.-A, (1992) Evidence for nuclear control, of the expression of the atpA and atpB chloroplast genes in Chlamydomonas. Plant Cell, 4, 283-295.
20. Durant, I. (1990) Light-based detection of biomolecules. Nature, 346, 297-298.
21. Feinberg, A.P. and Vogelstein, B. (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high-specific activity. Anal. Biochem. 132, 6-13.
22. Gagne, G. and Guertin, M. (1992) The early genetic response to light in the green unicellular alga Chlamydornonas eugametos grown under light/dark cycles involves genes that represent direct responses to light and photosynthesis. Plant. Mol. Biol. 18, 429-445.
23. Gamble, P.E. and Mullet, U.E. (1989) Translation and stability of proteins encoded by the plastid psbA and psbB genes are regulated by a nuclear gene during light-induced chloroplast development in barley. J. Biol. Chem. 264, 7236-7243.
24. Girard, J., Chua, N.H., Bennoun, P., Schmidt, G. and Delosme, M. (1980) Studies on mutants deficient in the photosystem I reaction centers in Chlamydomonas reinhardtii. Curr. Genet. 2, 215-221.
25. Goldschmidt-Clermont, M., Girard-Bascou, J., Choquet, V. and Rochaix, J.-D. (1990) Trans-splicing mutants of Chlamydomonas reinhardtii. Mol. Gen. Genet. 223, 417-425.
26. Gray, M.W. (1993) Origin and evolution of organelle genomes. Curr. Opin. Genet. Dev. 3, 884-890.
27. Gumpel, N.J., Raltey, L., Girard-Bascou, J., Wollman, F.-A., Nugent, J.H.A. and Purton,S. (1995) Nuclear mutants of Chlamydomonas reinhardtii defective in the biogenesis of the cytochrome b6f complex. Plant. Mol. Biol. 29, 921-932.
28. Harris, E.H. (1989) The Chlamydomonas Sourcebook: a Comprehensive Guide to Biology and Laboratory Use. San Diego: Academic Press.
29. Hayes, R., Kudla, J., Schuster, G., Gabay, L., Maliga, P. and Gruissem, W. (1996) Chloroplast mRNA 3′-end processing by a high molecular weight protein complex is regulated by nuclear encoded RNA binding proteins. EMBO J. 15, 1132-1141.
30. Holten, T.A. and Graham, M.W. (1991) A simple and efficient method for direct cloning of PCR products using ddT-tailed vectors. Nucl Acids Res. 19, 1156.
31. Howe, G. and Merchant, S. (1992) The biosynthesis of membrane and soluble plastidic c-type cytochromes of Chlamydomonas reinhardtii is dependent on multiple common gene products. EMBOJ. 11, 2789-2801.
32. Huang, J. and Van der Ploeg, L.H. (1988) A 5′ exo-ribonuclease and RNA ligase of T. brucei. Nucl Acids Res. 16, 9737-9759.
33. Jefferson, R.A., Kavanagh, T.A. and Bevan, M.W. (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901-3908.
34. Jenkins, B.D., Kulhanek, D.J. and Barkan, A. (1997) Nuclear mutations that block group II RNA splicing in maize chloroplasts reveal several intron classes with distinct requirements for splicing factors. Plant Cell, 9, 283-296.
35. Jiang, W., Hou, Y. and Inouye, M. (1997) CspA, the major cold-shock protein of Escherichia coli, is an RNA chaperone. J. Biol. Chem. 272, 196-202.
36. Kuchka, M.R., Goldschmidt-Clermont, M., van Dillewijn, J. and Rochaix, J.-D. (1989) Mutation at the Chlamydomonas nuclear NAC2 locus specifically affects stability of the chloroplast psbD transcript encoding polypeptide D2 of PS II. Cell, 58, 869-876.
37. Kudla, J., Hayes, R. and Gruissem, W. (1996) Polyadenylation accelerates degradation of chloroplast mRNA. EMBO J. 15, 7137-7146.
38. Kuras, R. and Wollman, F.-A. (1994) The assembly of cytochrome b6/f complexes: an approach using genetic transformation of the green aiga Chlamydomonas reinhardtii. EMBO J. 13, 1019-1027.
39. Larimer, F.W., Hsu, C.L., Maupin, M.K. and Stevens, A. (1992) Characterization of the XRN1 gene encoding a 5′→3′ exoribonuclease: sequence data and analysis of disparate protein and mRNA levels of gene-disrupted yeast cells. Gene, 120, 51-57.
40. Levy, H., Kindle, K.L. and Stern, O.B. (1997) A nuclear mutation that affects 3' processing of several mRNAs in Chlamydomonas chioroplasts. Plant Cell, 9, 825-836.
41. Li, H.H., Quinn, J., Culler, D., Girard-Bascou, J. and Merchant, S. (1996) Molecular genetic analysis of plastocyanin biosynthesis in Chlamydomonas reinhardtii, J. Biol. Chem. 271, 31283-31289.
42. Lisitsky, L. Klaff, P. and Schuster, G. (1996) Addition of destabilizing poly (A) -rich sequences to endonuclease cleavage sites during the degradation of chloroplast mRNA. Proc. Natl Acad. Sci. USA, 93, 13398-13403.
43. Monod, C., Goldschmidt-Clermont, M. and Rochaix, J.-D. (1992) Accumulation of chloroptast psb BRNA requires a nuclear factor in Chlamydomonas reinhardtii. Mol. Gen. Genet. 231, 449-459.
44. Muhlrad, D., Decker, C.J. and Parker, R. (1994) Deadenylation of the unstable mRNA encoded by yeast MFA2 gene leads to decapping followed by 5′→3′ digestion of the transcript. Genes Dev. 8, 855-866.
45. Nickelsen, J., van Dillewijn, J., Rahire, M. and Rochaix, J.-D. (1994) Determinants for stability of the chloroplast psbD RNA are located within its short leader region in Chlamydomonas reinhardtii. EMBO J. 13, 3182-3191.
46. Rochaix, J.-D. (1980) Restriction fragments from Chlamydomonas chloroplast DNA. Meths. Enzymol. 65, 785-795.
47. Rochaix, J.-D., Kuchka, M., Mayfield, S., Schirmer, R.M., Girard, B.J. and Bennoun, P. (1989) Nuclear and chloroplast mutations affect the synthesis or stability of the chloroplast psbC gene product in Chlamydomonas reinhardtii. EMBO J. 8, 1013-1021.
48. Rott, R., Drager, R.G., Stern, D.B. and Schuster, G. (1996) The 3′ untranslated regions of chloroplast genes in Chiamydomonas reinhardtii do not serve as efficient transcriptional terminators. Mol. Gen. Genet. 252, 676-683.
49. Sakamoto, W., Chen, X., Kindle, K.L. and Stern, D.B. (1994a) Function of the Chlamydomonas reinhardtii pefD5′ untranslated region in regulating the accumulation of subunit IV of the cytochrome b6/f complex. Plant J. 6, 503-512.
50. Sakamoto, W., Kindle, K.L. and Stern, D.B. (1993) In vivo analysis of Chlamydomonas chloroplast petD gene expression using stable transformation of β-glucuronidase translationai fusions. Proc. Natl Acad. Sci. USA, 90, 497-501.
51. Sakamoto, W., Sturm, N.R., Kindle, K.L. and Stern, D.B. (1994b) petD mRNA maturation in Chlamydomonas reinhardtii chioroplasts: Role of 5′ endonucleolytic processing. Mol. Cell. Biol. 14, 6180-6186.
52. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
53. Schuster, G. and Gruissem, W. (1991) Chloroplast mRNA 3′ end processing requires a nuclear-encoded RNA binding protein. EMBO J. 10, 1493-1502.
54. Shepherd, H.S., Boynton, J.E. and Gillham, N.W. (1979) Mutations in nine chloroplast loci of Chlamydomonas affecting photosynthetic functions. Proc. Natl Acad. Sci. USA, 76, 1353-1357.
55. Sieburth, L.E., Berry-Lowe, S. and Schmidt, G.W. (1991) Chloroplast RNA stability in Chlamydomonas: Rapid degradation of psbB and psbC transcripts in two nuclear mutants. Plant Cell, 3, 175-189.
56. Stampacchia, O., Girard-Bascou, J., Zanasco, J.-L., Zerges, W., Bennoun, P. and Rochaix, J.-D. (1997) A nuclear-encoded function essential for translation of the chloroplast psaB mRNA in Chlamydomonas reinhardtii. Plant Cell, 9, 773-782.
57. Staples, R.R. and Dieckmann, C.L. (1994) Suppressor analyses of temperature-sensitive cpb1 strains of Saccharomyces cerevisiae: the product of the nuclear gene SOC1 affects mitochondrial cytochrome b mRNA post-transcriptionally. Genet. 138, 565-575.
58. Stern, D.B. and Gruissem, W. (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.
59. Stern, D.B. and Gruissem, W. (1989) Chloroplast messenger RNA 3′ end maturation is biochemically distinct from prokaryotic messenger RNA processing. Plant Mol. Biol. 13, 615-625.
60. Stern, D.B., Higgs, D.C. and Yang, J. (1997) Transcriptional and translational activities of chloroplasts. Trends Plant Sci. 2, 308-315.
61. Stern, D.B. and Kindle, K.L (1993) 3′ end maturation of the Chlamydomonas reinhardtii chioroplast atpB mRNA is a twostep process. Mol. Cell. Biol. 13, 2277-2285.
62. Stern, D.B., Radwanski, E.R. and Kindle, K.L. (1991) A 3′ stem/ loop structure of the Chlamydomonas chioroplast atpB gene regulates mRNA accumulation in vivo. Plant Cell, 3, 285-297.
63. Stevens, A. and Maupin, M.K. (1987) A 5′→3′ exoribonuclease of human placental nuclei: purification and substrate specificity. Nucl Acids Res. 15, 695-708.
64. Sturm, N.R., Kuras, R., Büschlen, S., Sakamoto, W., Kindle, K.L., Stern, D.B. and Wollman, F.-A. (1994) The petD gene is transcribed by functionally redundant promoters in Chlamydomonas reinhardtii chloroplasts. Mol. Cell. Biol. 14, 6171-6179.
65. Vreken, P. and Raué, H.A. (1992) The rate limiting step in yeast PGK1 mRNA degradation is an endonucleolytic cleavage in the 3'-terminal part of the coding region. Mol. Cell. Biol. 12, 2986-2996.
66. Westhoff, P. and Herrmann, R.G. (1988) Complex RNA maturation in chloroplasts. The psbBoperon from spinach. Eur. J. Biochem. 171, 551-564.
67. Xu, F. and Cohen, S.N. (1995) RNA degradation in Escherichia coli regulated by 3′ adenylation and 5′ phosphorylation. Nature, 374, 180-183.