Molecular identification and function of cis- and trans-acting determinants for petA transcript stability in Chlamydomonas reinhardtii chloroplasts

Molecular and Cellular Biology

Volumn 28, Issue 17, 2008, Pages 5529-5542

  Loiselay, Christelle ^a   Gumpel, Nicola J ^b   Girard Bascou, Jacqueline ^a   Watson, Adam T ^b,c   Purton, Saul ^b   Wollman, Francis André ^a   Choquet, Yves ^a  

^a INST DE BIOLOGIE PHYSICO CHIMIQUE   (France)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF SUSSEX   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MCA1 PROTEIN; MESSENGER RNA; PROTEIN; TCA1 PROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; CHLAMYDOMONAS REINHARDTII; CHLOROPLAST; CONTROLLED STUDY; DNA MODIFICATION; GENE; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC STABILITY; GENETIC TRANSCRIPTION; NONHUMAN; PETA GENE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION;

5' UNTRANSLATED REGIONS; ALGAL PROTEINS; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CHLAMYDOMONAS REINHARDTII; CHLOROPLASTS; CYTOCHROMES F; GENE EXPRESSION REGULATION; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEIC ACID CONFORMATION; PROTEIN BIOSYNTHESIS; RIBONUCLEASES; RNA STABILITY;

CHLAMYDOMONAS REINHARDTII; CHLOROPHYTA;

EID: 50249158627     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.02056-07     Document Type: Article

References (80)

1. Andres, C., C. Lurin, and I. D. Small. 2007. The multifarious roles of PPR proteins in plant mitochondrial gene expression. Physiol. Plant 129:14-22.
2. Anthonisen, I. L., M. L. Salvador, and U. Klein. 2001. Specific sequence elements in the untranslated regions of rbcL and atpB gene mRNAs stabilize transcripts in the chloroplast of Chlamydomonas reinhardtii. RNA 7:1024-1033.
3. Barkan, A., and M. Goldschmidt-Clermont. 2000. Participation of nuclear gene in chloroplast gene expression. Biochimie 82:559-572.
4. Barkan, A., M. Walker, M. Nolasco, and D. Johnson. 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.
5. Bollenbach, T. J., G. Schuster, and D. B. Stern. 2004. Cooperation of endo-and exoribonucleases in chloroplast mRNA turnover. Prog. Nucleic Acids Res. Mol. Biol. 78:305-337.
6. Boudreau, E., J. Nickelsen, S. D. Lemaire, F. Ossenbuhl, and J.-D. Rochaix. 2000. The Nac2 gene of Chlamydomonas encodes a chloroplast TPR-like protein involved in psbD mRNA stability. EMBO J. 19:3366-3376.
7. Boynton, J. E., and N. W. Gillham. 1993. Chloroplast transformation in Chlamydomonas. Methods Enzymol. 217:510-536.
8. Chen, X., K. Kindle, and D. B. Stern. 1993. Initiation codon mutations in the Chlamydomonas chloroplast petD gene result in temperature-sensitive photosynthetic growth. EMBO J. 12:3627-3635.
9. Choquet, Y., D. B. Stern, K. Wostrikoff, R. Kuras, J. Girard-Bascou, and F.-A. Wollman. 1998. Translation of cytochrome f is autoregulated through the 5′ untranslated region of petA mRNA in Chlamydomonas chloroplasts. Proc. Natl. Acad. Sci. USA 95:4380-4385.
10. Choquet, Y., and F.-A. Wollman. 2002. Translational regulations as specific traits of chloroplast gene expression. FEBS Lett. 529:39-42.
11. Choquet, Y., F. Zito, K. Wostrikoff, and F.-A. Wollman. 2003. Cytochrome f translation in Chlamydomonas chloroplast is autoregulated by its carboxyl-terminal domain. Plant Cell 15:1443-1454.
12. Dauvillee, D., O. Stampacchia, J. Girard-Bascou, and J.-D. Rochaix. 2003. Tab2 is a novel conserved RNA binding protein required for translation of the chloroplast psaB mRNA. EMBO J. 22:6378-6388.
13. Desloire, S., H. Gherbi, W. Laloui, S. Marhadour, V. Clouet, L. Cattolico, C. Falentin, S. Giancola, M. Renard, F. Budar, I. Small, M. Caboche, R. Delourme, and A. Bendahmane. 2003. Identification of the fertility restoration locus, Rfo, in radish, as a member of the pentatricopeptide-repeat protein family. EMBO Rep. 4:588-594.
14. Drager, R. G., J. Girard-Bascou, Y. Choquet, K. L. Kindle, and D. B. Stern. 1998. In vivo evidence for 5′→3′ exoribonuclease degradation of an unstable chloroplast mRNA. Plant J. 13:85-96.
15. Drager, R. G., D. C. Higgs, K. L. Kindle, and D. B. Stern. 1999. 5′ to 3′ exoribonucleolytic activity is a normal component of chloroplast mRNA decay pathways. Plant J. 19:521-531.
16. Drapier, D., J. Girard-Bascou, and F.-A. Wollman. 1992. Evidence for nuclear control of the expression of the atpA and atpB chloroplast genes in Chlamydomonas. Plant Cell 4:283-295.
17. Drapier, D., H. Suzuki, H. Levy, B. Rimbault, K. L. Kindle, D. B. Stern, and F.-A. Wollman. 1998. The chloroplast atpA gene cluster in Chlamydomonas reinhardtii: functional analysis of a polycistronic transcription unit. Plant Physiol. 117:629-641.
18. Eberhard, S., D. Drapier, and F.-A. Wollman. 2002. Searching limiting steps in the expression of chloroplast encoded proteins: relations between gene copy number, transcription, transcript abundance, and translation rate in the chloroplast of Chlamydomonas reinhardtii. Plant J. 31:1-14.
19. Edwards, T. A., J. Trincao, C. R. Escalante, R. P. Wharton, and A. K. Aggarwal. 2000. Crystallization and characterization of Pumilo: a novel RNA binding protein. J. Struct. Biol. 132:251-254.
20. Esposito, D., D. C. Higgs, R. G. Drager, D. B. Stern, and J. Girard-Bascou. 2001. A nucleus-encoded suppressor defines a new factor which can promote petD mRNA stability in the chloroplast of Chlamydomonas reinhardtii. Curr. Genet. 39:40-48.
21. Fischer, N., O. Stampacchia, K. Redding, and J.-D. Rochaix. 1996. Selectable marker recycling in the chloroplast. Mol. Gen. Genet. 251:373-380.
22. Fisk, D. G., M. B. Walker, and A. Barkan. 1999. Molecular cloning of the maize gene crp1 reveals similarity between regulators of mitochondrial and chloroplast gene expression. EMBO J. 18:2621-2630.
23. Fox, T. D. 1996. Genetics of mitochondrial translation. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
24. Girard-Bascou, J., Y. Choquet, N. J. Gumpel, D. Culler, S. Purton, S. Merchant, F. Laquerriere, and F.-A. Wollman. 1995. Nuclear control of the expression of the chloroplast pet genes in Chlamydomonas reinhardtii, p. 683-686. In P. Mathis (ed.), Photosynthesis: from light to biosphere, vol. III. Kluwer Academic Publishers, Dordrecht, The Netherlands.
25. Goldschmidt-Clermont, M. 1991. Transgenic expression of aminoglycoside adenine transferase in the chloroplast: a selectable marker of site-directed transformation of Chlamydomonas. Nucleic Acids Res. 19:4083-4089.
26. Grivell, L. A. 1995. Nucleo-mitochondrial interactions in mitochondrial gene expression. Crit. Rev. Biochem. Mol. Biol., 30:121-164.
27. Gudynaite-Savitch, L., M. Gretes, R. M. Morgan-Kiss, L. V. Savitch, J. Simmonds, S. E. Kohalmi, and N. P. Huner. 2006. Cytochrome f from the Antarctic psychrophile, Chlamydomonas raudensis UWO 241: structure, sequence, and complementation in the mesophile, Chlamydomonas reinhardtii. Mol. Genet. Genomics 275:387-398.
28. 6f complex. Plant Mol. Biol. 29:921-932.
29. Harris, E. H. 1989. The Chlamydomonas source book: a comprehensive guide to biology and laboratory use. Academic Press, Inc., San Diego, CA.
30. Higgs, D. C., R. Kuras, K. L. Kindle, F.-A. Wollman, and D. B. Stern. 1998. Inversions in the Chlamydomonas chloroplast genome suppress a petD 5′ untranslated region deletion by creating functional chimeric mRNAs. Plant J. 14:663-671.
31. Higuchi, R. 1990. Recombinant PCR, p. 177-183. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, and T. J. White (ed.), PCR protocols: a guide to methods and applications. Academic Press, Inc., New York, NY.
32. Islas-Osuna, M. A., T. P. Ellis, L. L. Marnell, T. M. Mittelmeier, and C. L. Dieckmann. 2002. Cbp1 is required for translation of the mitochondrial cytochrome b mRNA of Saccharomyces cerevisiae. J. Biol. Chem. 277:37987-37990.
33. Jensen, K. H., D. L. Herrin, F. G. Plumley, and G. W. Schmidt. 1986. Biogenesis of photosystem II complexes: transcriptional, translational, and posttranslational regulation. J. Cell Biol. 103:1315-1325.
34. Klinkert, B., I. Elles, and J. Nickelsen. 2006. Translation of chloroplast psbD mRNA in Chlamydomonas is controlled by a secondary RNA structure blocking the AUG start codon. Nucleic Acids Res. 34:386-394.
35. Kuchka, M., S. Mayfield, and J.-D. Rochaix. 1988. Nuclear mutations specifically affect the synthesis and/or degradation of the chloroplast-encoded D2 polypeptide of photosystem II in Chlamydomonas reinhardtii. EMBO J. 7:319-324.
36. Kuchka, M. R., M. Goldschmidt-Clermont, J. J. van Dillewijn, and J.-D. Rochaix. 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. 6f complexes: an approach using genetic transformation of the green alga Chlamydomonas reinhardtii. EMBO J. 13:1019-1027.
38. Lurin, C., C. Andres, S. Aubourg, M. Bellaoui, F. Bitton, C. Bruyere, M. Caboche, C. Debast, J. Gualberto, B. Hoffmann, A. Lecharny, M. Le Ret, M. L. Martin-Magniette, H. Mireau, N. Peeters, J. P. Renou, B. Szurek, L. Taconnat, and I. Small. 2004. Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16:2089-2103.
39. Majeran, W., J. Olive, D. Drapier, O. Vallon, and F.-A. Wollman. 2001. The light sensitivity of ATP synthase mutants of Chlamydomonas reinhardtii. Plant Physiol. 126:421-433.
40. Manthey, G. M., and J. E. McEwen. 1995. The product of the nuclear gene PET309 is required for translation of mature mRNA and stability or production of intron-containing RNAs derived from the mitochondrial COX1 locus of Saccharomyces cerevisiae. EMBO J. 14:4031-4043.
41. Matsumoto, T., M. Matsuo, and Y. Matsuda. 1991. Structural analysis and expression during dark-light transitions of a gene for cytochrome f in Chlamydomonas reinhardtii. Plant Cell Physiol. 32:863-872.
42. Meierhoff, K., S. Felder, T. Nakamura, N. Bechtold, and G. Schuster. 2003. HCF152, an Arabidopsis RNA binding pentatricopeptide repeat protein involved in the processing of chloroplast psbB-psbT-psbH-petB- petD RNAs. Plant Cell 15:1480-1495.
43. Minai, L., K. Wostrikoff, F.-A. Wollman, and Y. Choquet. 2006. Chloroplast biogenesis of photosystem II cores involves a series of assembly-controlled steps that regulate translation. Plant Cell 18:159-175.
44. Monde, R. A., G. Schuster, and D. B. Stern. 2000. Processing and degradation of chloroplast mRNA. Biochimie 82:573-582.
45. Monod, C., M. Goldschmidt-Clermont, and J.-D. Rochaix. 1992. Accumulation of chloroplast psbB RNA requires a nuclear factor in Chlamydomonas reinhardtii. Mol. Gen. Genet. 231:449-459.
46. Murakami, S., K. Kuehnle, and D. B. Stern. 2005. A spontaneous tRNA suppressor of a mutation in the Chlamydomonas reinhardtii nuclear MCD1 gene required for stability of the chloroplast petD mRNA. Nucleic Acids Res. 33:3372-3380.
47. Nakamura, T., K. Meierhoff, P. Westhoff, and G. Schuster. 2003. RNA-binding properties of HCF152, an Arabidopsis PPR protein involved in the processing of chloroplast RNA. Eur. J. Biochem. 270:4070-4081.
48. Nickelsen, J. 1998. Chloroplast RNA stability, p. 151-163. In J.-D. Rochaix, M. Goldschmidt-Clermont, and S. Merchant (ed.), The molecular biology of chloroplasts and mitochondria in Chlamydomonas. Kluwer Academic Publishers, Dordrecht, The Netherlands.
49. Nickelsen, J., M. Fleischmann, E. Boudreau, M. Rahire, and J.-D. Rochaix. 1999. Identification of cis-acting RNA leader elements required for chloroplast psbD gene expression in Chlamydomonas. Plant Cell 11:957-970.
50. Nickelsen, J., J. van Dillewyn, M. Rahire, and J.-D. Rochaix. 1994. Determinants for stability of the chloroplast psbD RNA arc located within its short leader region in Chlamydomonas reinhardtii. EMBO J. 13:3182-3191.
51. Okuda, K., F. Myouga, R. Motohashi, K. Shinozaki, and T. Shikanai. 2007. Conserved domain structure of pentatricopeptide repeat proteins involved in chloroplast RNA editing. Proc. Natl. Acad. Sci. USA 104:8178-8183.
52. Ossenbuhl, F., and J. Nickelsen. 2000. cis- and trans-acting determinants for translation of psbD mRNA in Chlamydomonas reinhardtii. Mol. Cell. Biol. 20:8134-8142.
53. Raynaud, C., C. Loiselay, K. Wostrikoff, R. Kuras, J. Girard-Bascou, F.-A. Wollman, and Y. Choquet. 2007. Evidence for regulatory function of nucleus-encoded factors on mRNA stabilization and translation in the chloroplast. Proc. Natl. Acad. Sci. USA 104:9093-9098.
54. Rochaix, J.-D., M. Kuchka, S. P. Mayfield, M. Schirmer-Rahire, J. Girard-Bascou, and P. Bennoun. 1989. Nuclear and chloroplast mutations affect the synthesis or stability of the chloroplast psbC gene product in Chlamydomonas reinhardtii. EMBO J. 8:1013-1021.
55. Rymarquis, L. A., D. C. Higgs, and D. B. Stern. 2006. Nuclear suppressors define three factors that participate in both 5′ and 3′ end processing of mRNAs in Chlamydomonas chloroplasts. Plant J. 46:448-461.
56. 6f complex. Plant J. 6:503-512.
57. Sakamoto, W., K. L. Kindle, and D. B. Stern. 1993. In vivo analysis of Chlamydomonas chloroplast petD gene expression using stable transformation of β-glucuronidase translational fusions. Proc. Natl. Acad. Sci. USA 90:497-501.
58. Sakamoto, W., N. R. Sturm, K. L. Kindle, and D. B. Stern. 1994. petD mRNA maturation in Chlamydomonas reinhardtii chloroplasts: role of 5′ endonucleolytic processing. Mol. Cell. Biol. 14:6180-6186.
59. Salone, V., M. Rudinger, M. Polsakiewicz, B. Hoffmann, M. Groth-Malonek, B. Szurek, I. Small, V. Knoop, and C. Lurin. 2007. A hypothesis on the identification of the editing enzyme in plant organelles. FEBS Lett. 581:4132-4138.
60. Schmitz-Linneweber, C., R. Williams-Carrier, and A. Barkan. 2005. RNA immunoprecipitation and microarray analysis show a chloroplast pentatricopeptide repeat protein to be associated with the 5′ region of mRNAs whose translation it activates. Plant Cell 17:2791-2804.
61. Schmitz-Linneweber, C., R. E. Williams-Carrier, P. M. Williams-Voelker, T. S. Kroeger, A. Vichas, and A. Barkan. 2006. A pentatricopeptide repeat protein facilitates the trans-splicing of the maize chloroplast rps12 pre-mRNA. Plant Cell 18:2650-2663.
62. Schwarz, C., I. Elles, J. Kortmann, M. Piotrowski, and J. Nickelsen. 2007. Synthesis of the D2 protein of photosystem II in Chlamydomonas is controlled by a high molecular mass complex containing the RNA stabilization factor Nac2 and the translational activator RBP40. Plant Cell 19:3627-3639.
63. Shikanai, T. 2006. RNA editing in plant organelles: machinery, physiological function, and evolution. Cell. Mol. Life Sci. 63:698-708.
64. Shimogawara, K., S. Fujiwara, A. Grossman, and H. Usuda. 1998. High-efficiency transformation of Chlamydomonas reinhardtii by electroporation. Genetics 148:1821-1828.
65. Sickmann, A., J. Reinders, Y. Wagner, C. Joppich, R. Zahedi, H. E. Meyer, B. Schonfisch, I. Perschil, A. Chacinska, B. Guiard, P. Rehling, N. Pfanner, and C. Meisinger. 2003. The proteome of Saccharomyces cerevisiae mitochondria. Proc. Natl. Acad. Sci. USA 100:13207-13212.
66. Sieburth, L. E., S. Berry-Lowe, and G. W. Schmidt. 1991. Chloroplast RNA stability in Chlamydomonas: rapid degradation of psbB and psbC transcripts in two nuclear mutants. Plant Cell 3:175-189.
67. Silflow, C. D. 1998. Organization of the nuclear genome, p. 25-40. In J.-D. Rochaix, M. Goldschmidt-Clermont, and S. Merchant (ed.), The molecular biology of chloroplasts and mitochondria in Chlamydomonas. Kluwer Academic Publishers, Dordrecht, The Netherlands.
68. Small, I. D., and N. Peeters. 2000. The PPR motif: a TPR-related motif prevalent in plant organellar proteins. Trends Biochem. Sci. 25:46-47.
69. Stampacchia, O. 1997. Photosystem I biogenesis in Chlamydomonas reinhardtii. Ph.D. thesis. University of Geneva, Geneva, Switzerland.
70. Sturm, N. R., R. Kuras, S. Buschlen, W. Sakamoto, K. L. Kindle, D. B. Stern, and F.-A. Wollman. 1994. The petD gene is transcribed by functionally redundant promoters in Chlamydomonas reinhardtii chloroplasts. Mol. Cell. Biol. 14:6171-6179.
71. Vaistij, F. E., E. Boudreau, S. D. Lemaire, M. Goldschmidt-Clermont, and J.-D. Rochaix. 2000. Characterization of mbb1, a nucleus-encoded tetratricopeptide-like repeat protein required for expression of the chloroplast psbB/psbT/psbH gene cluster in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 97:14813-14818.
72. Vaistij, F. E., M. Goldschmidt-Clermont, K. Wostrikoff, and J.-D. Rochaix. 2000. Stability determinants in the chloroplast psbB/T/H mRNAs of Chlamydomonas reinhardtii. Plant J. 21:469-482.
73. Wang, X., J. McLachlan, P. D. Zamore, and T. M. Hall. 2002. Modular recognition of RNA by a human pumilio-homology domain. Cell 110:501-512.
74. Wang, X., P. D. Zamore, and T. M. Hall. 2001. Crystal structure of a Pumilio homology domain. Mol. Cell 7:855-865.
75. Wang, Z., Y. Zou, X. Li, Q. Zhang, L. Chen, H. Wu, D. Su, Y. Chen, J. Guo, D. Luo, Y. Long, Y. Zhong, and Y. G. Liu. 2006. Cytoplasmic male sterility of rice with boro II cytoplasm is caused by a cytotoxic peptide and is restored by two related PPR motif genes via distinct modes of mRNA silencing. Plant Cell 18:676-687.
76. Wostrikoff, K., Y. Choquet, F.-A. Wollman, and J. Girard-Bascou. 2001. TCA1, a single nuclear-encoded translational activator specific for petA mRNA in Chlamydomonas reinhardtii chloroplast. Genetics 159:119-132.
77. Wostrikoff, K., J. Girard-Bascou, F.-A. Wollman, and Y. Choquet. 2004. Biogenesis of PSI involves a cascade of translational autoregulation in the chloroplast of Chlamydomonas. EMBO J. 22:2696-2705.
78. Zerges, W. 2000. Translation of mRNAs encoded by chloroplast genomes. Biochimie 82:583-601.
79. Zerges, W., and J.-D. Rochaix. 1994. The 5′ leader of a chloroplast mRNA mediates the translational requirements for two nucleus-encoded functions in Chlamydomonas reinhardtii. Mol. Cell. Biol. 14:5268-5277.
80. Zuker, M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31:3406-3415.