Small RNAs reveal two target sites of the RNA-maturation factor Mbb1 in the chloroplast of Chlamydomonas

Nucleic Acids Research

Volumn 42, Issue 5, 2014, Pages 3286-3297

  Loizeau, Karen ^a   Qu, Yujiao ^b   Depp, Sébastien ^a   Fiechter, Vincent ^a   Ruwe, Hannes ^b   Lefebvre Legendre, Linnka ^a   Schmitz Linneweber, Christian ^b   Goldschmidt Clermont, Michel ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b HUMBOLDT UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; PROTEIN MBB1; TETRATRICOPEPTIDE REPEAT PROTEIN; TRANSFER RNA; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ARTICLE; BINDING AFFINITY; BINDING ASSAY; CHLAMYDOMONAS; CHLAMYDOMONAS REINHARDTII; CHLOROPLAST; CHLOROPLAST GENOME; GENE MUTATION; IMMUNOPRECIPITATION; MICROBIAL GENE; NONHUMAN; PRIORITY JOURNAL; PSBB GENE; PSBH GENE; RNA BINDING; RNA PROCESSING; RNA SEQUENCE; RNA TRANSLATION; SITE DIRECTED MUTAGENESIS;

5' UNTRANSLATED REGIONS; BASE SEQUENCE; CHLAMYDOMONAS REINHARDTII; CHLOROPLAST PROTEINS; CHLOROPLASTS; MOLECULAR SEQUENCE DATA; MUTATION; PHOTOSYSTEM II PROTEIN COMPLEX; PROTEIN BIOSYNTHESIS; REGULATORY SEQUENCES, RIBONUCLEIC ACID; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA STABILITY; RNA, CHLOROPLAST; RNA, MESSENGER; RNA, SMALL UNTRANSLATED; RNA-BINDING PROTEINS;

EID: 84898933453     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt1272     Document Type: Article

References (69)

1. Herrin, D.L. and Nickelsen, J. (2004) Chloroplast RNA processing and stability. Photosynth. Res., 82, 301-314.
2. Barkan, A. (2011) Expression of plastid genes: Organelle-specific elaborations on a prokaryotic scaffold. Plant Physiol., 155, 1520-1532.
3. Stern, D.B., Goldschmidt-Clermont, M. and Hanson, M.R. (2010) Chloroplast RNA metabolism. Annu. Rev. Plant Biol., 61, 125-155.
4. Barkan, A. and Goldschmidt-Clermont, M. (2000) Participation of nuclear genes in chloroplast gene expression. Biochimie, 82, 559-572. (Pubitemid 30608452
5. Zerges, W. (2000) Translation in chloroplasts. Biochimie, 82, 583-601. (Pubitemid 30608454
6. Marin-Navarro, J., Manuell, A., Wu, J. and Mayfield, S. (2007) Chloroplast translation regulation. Photosynth. Res., 94, 359-774.
7. Lyska, D., Meierhoff, K. and Westhoff, P. (2013) How to build functional thylakoid membranes: From plastid transcription to protein complex assembly. Planta, 237, 413-428.
8. Raynaud, C., Loiselay, C., Wostrikoff, K., Kuras, R., Girard-Bascou, J., Wollman, F.A. and Choquet, Y. (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.
9. Stoppel, R., Lezhneva, L., Schwenkert, S., Torabi, S., Felder, S., Meierhoff, K., Westhoff, P. and Meurer, J. (2011) Recruitment of a ribosomal release factor for light-And stress-dependent regulation of petB transcript stability in Arabidopsis chloroplasts. Plant Cell, 23, 2680-2695.
10. Maier, U.G., Bozarth, A., Funk, H.T., Zauner, S., Rensing, S.A., Schmitz-Linneweber, C., Borner, T. and Tillich, M. (2008) Complex chloroplast RNA metabolism: Just debugging the genetic programme? BMC Biol., 6, 36.
11. Lurin, C., Andres, C., Aubourg, S., Bellaoui, M., Bitton, F., Bruyere, C., Caboche, M., Debast, C., Gualberto, J., Hoffmann, B. et al. (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell, 16, 2089-2103. (Pubitemid 39059730
12. Schmitz-Linneweber, C. and Small, I. (2008) Pentatricopeptide repeat proteins: A socket set for organelle gene expression. Trends Plant Sci., 13, 663-670.
13. Johnson, X., Wostrikoff, K., Finazzi, G., Kuras, R., Schwarz, C., Bujaldon, S., Nickelsen, J., Stern, D.B., Wollman, F.A. and Vallon, O. (2010) MRL1, a conserved Pentatricopeptide repeat protein, is required for stabilization of rbcL mRNA in Chlamydomonas and Arabidopsis. Plant Cell, 22, 234-248.
14. Rahire, M., Laroche, F., Cerutti, L. and Rochaix, J.D. (2012) Identification of an OPR protein involved in the translation initiation of the PsaB subunit of photosystem I. Plant J., 72, 652-661.
15. Preker, P.J. and Keller, W. (1998) The HAT helix, a repetitive motif implicated in RNA processing. Trends Biochem Sci., 23, 15-16. (Pubitemid 28093987
16. Shikanai, T. and Fujii, S. (2013) Function of PPR proteins in plastid gene expression. RNA Biol. (Epub ahead of print).
17. Wang, X., McLachlan, J., Zamore, P.D. and Hall, T.M. (2002) Modular recognition of RNA by a human pumilio-homology domain. Cell, 110, 501-512. (Pubitemid 35232293
18. Drager, R.G., Girard-Bascou, J., Choquet, Y., Kindle, K.L. and Stern, D.B. (1998) In vivo evidence for 50->30 exoribonuclease degradation of an unstable chloroplast mRNA. Plant J., 13, 85-96.
19. Vaistij, F.E., Goldschmidt-Clermont, M., Wostrikoff, K. and Rochaix, J.D. (2000) Stability determinants in the chloroplast psbB/T/H mRNAs of Chlamydomonas reinhardtii. Plant J., 21, 469-482. (Pubitemid 30181275
20. Nickelsen, J., Fleischmann, M., Boudreau, E., Rahire, M. and Rochaix, J.D. (1999) Identification of cis-Acting RNA leader elements required for chloroplast psbD gene expression in Chlamydomonas. Plant Cell, 11, 957-970.
21. Loiselay, C., Gumpel, N.J., Girard-Bascou, J., Watson, A.T., Purton, S., Wollman, F.A. and Choquet, Y. (2008) Molecular identification and function of cis-And trans-Acting determinants for petA transcript stability in Chlamydomonas reinhardtii chloroplasts. Mol. Cell. Biol., 28, 5529-5542.
22. Pfalz, J., Bayraktar, O.A., Prikryl, J. and Barkan, A. (2009) Sitespecific binding of a PPR protein defines and stabilizes 50 and 30 mRNA termini in chloroplasts. EMBO J., 28, 2042-2052.
23. Prikryl, J., Rojas, M., Schuster, G. and Barkan, A. (2011) Mechanism of RNA stabilization and translational activation by a pentatricopeptide repeat protein. Proc. Natl Acad. Sci. USA, 108, 415-420.
24. Hammani, K., Cook, W.B. and Barkan, A. (2012) RNA binding and RNA remodeling activities of the half-A-Tetratricopeptide (HAT) protein HCF107 underlie its effects on gene expression. Proc. Natl Acad. Sci. USA, 109, 5651-5656.
25. Ruwe, H. and Schmitz-Linneweber, C. (2012) Short non-coding RNA fragments accumulating in chloroplasts: Footprints of RNA binding proteins? Nucleic Acids Res., 40, 3106-3116.
26. Zhelyazkova, P., Sharma, C.M., Forstner, K.U., Liere, K., Vogel, J. and Borner, T. (2012) The primary transcriptome of barley chloroplasts: Numerous noncoding RNAs and the dominating role of the plastid-encoded RNA polymerase. Plant Cell, 24, 123-136.
27. Haili, N., Arnal, N., Quadrado, M., Amiar, S., Tcherkez, G., Dahan, J., Briozzo, P., Colas des Francs-Small, C., Vrielynck, N. and Mireau, H. (2013) The pentatricopeptide repeat MTSF1 protein stabilizes the nad4 mRNA in Arabidopsis mitochondria. Nucleic Acids Res., 41, 6650-6663.
28. Wang, L., Yu, X., Wang, H., Lu, Y.Z., de Ruiter, M., Prins, M. and He, Y.K. (2011) A novel class of heat-responsive small RNAs derived from the chloroplast genome of Chinese cabbage (Brassica rapa) BMC Genomics, 12, 289.
29. Monod, C., Goldschmidt-Clermont, M. and Rochaix, J.D. (1992) Accumulation of chloroplast psbB RNA requires a nuclear factor in Chlamydomonas reinhardtii. Mol. Gen. Genet., 231, 449-459.
30. Johnson, C.H. and Schmidt, G.W. (1993) The psbB gene cluster of the Chlamydomonas reinhardtii chloroplast: Sequence and transcriptional analyses of psbN and psbH. Plant Mol. Biol., 22, 645-658.
31. Vaistij, F.E., Boudreau, E., Lemaire, S.D., Goldschmidt-Clermont, M. and Rochaix, J.D. (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.
32. Felder, S., Meierhoff, K., Sane, A.P., Meurer, J., Driemel, C., Plucken, H., Klaff, P., Stein, B., Bechtold, N. and Westhoff, P. (2001) The nucleus-encoded HCF107 gene of Arabidopsis provides a link between intercistronic RNA processing and the accumulation of translation-competent psbH transcripts in chloroplasts. Plant Cell, 13, 2127-2141. (Pubitemid 32919022
33. Sane, A.P., Stein, B. and Westhoff, P. (2005) The nuclear gene HCF107 encodes a membrane-Associated R-TPR (RNA tetratricopeptide repeat)-containing protein involved in expression of the plastidial psbH gene in Arabidopsis. Plant J., 42, 720-730. (Pubitemid 40809889
34. Howard, M.J., Lim, W.H., Fierke, C.A. and Koutmos, M. (2012) Mitochondrial ribonuclease P structure provides insight into the evolution of catalytic strategies for precursor-TRNA 50 processing. Proc. Natl Acad. Sci. USA, 109, 16149-16154.
35. Harris, E.H. (1989) The Chlamydomonas Sourcebook. Academic Press, Inc, San Diego, CA.
36. Perron, K., Goldschmidt-Clermont, M. and Rochaix, J.D. (1999) A factor related to pseudouridine synthases is required for chloroplast group II intron trans-splicing in Chlamydomonas reinhardtii. EMBO J., 18, 6481-6490. (Pubitemid 29533252
37. Choquet, Y., Goldschmidt-Clermont, M., Girard-Bascou, J., Kuck, 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.
38. Ausubel, F.A., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A. and Struhl, K. (1998) Current Protocols in Molecular Biology. John Wiley & sons, New York, NY.
39. Ibrahim, F., Rymarquis, L.A., Kim, E.J., Becker, J., Balassa, E., Green, P.J. and Cerutti, H. (2010) Uridylation of mature miRNAs and siRNAs by the MUT68 nucleotidyltransferase promotes their degradation in Chlamydomonas. Proc. Natl Acad. Sci. USA, 107, 3906-3911.
40. Lu, C., Meyers, B.C. and Green, P.J. (2007) Construction of small RNA cDNA libraries for deep sequencing. Methods, 43, 110-117. (Pubitemid 47419364
41. Molnar, A., Schwach, F., Studholme, D.J., Thuenemann, E.C. and Baulcombe, D.C. (2007) miRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature, 447, 1126-1129. (Pubitemid 47014429
42. Pall, G.S. and Hamilton, A.J. (2008) Improved northern blot method for enhanced detection of small RNA. Nat. Protoc., 3, 1077-1084.
43. 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. (Pubitemid 21912776
44. Fischer, N., Stampacchia, O., Redding, K. and Rochaix, J.D. (1996) Selectable marker recycling in the chloroplast. Mol. Gen. Genet., 251, 373-380.
45. Bruick, R.K. and Mayfield, S.P. (1998) Processing of the psbA 50 untranslated region in Chlamydomonas reinhardtii depends upon factors mediating ribosome association. J. Cell. Biol., 143, 1145-1153.
46. Eberhard, S., Drapier, D. and Wollman, F.A. (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, 149-160. (Pubitemid 34829628
47. Summer, E.J., Schmid, V.H., Bruns, B.U. and Schmidt, G.W. (1997) Requirement for the H phosphoprotein in photosystem II of Chlamydomonas reinhardtii. Plant Physiol., 113, 1359-1368. (Pubitemid 27210631
48. Ossenbuhl, F., Hartmann, K. and Nickelsen, J. (2002) A chloroplast RNA binding protein from stromal thylakoid membranes specifically binds to the 50 untranslated region of the psbA mRNA. Eur. J. Biochem., 269, 3912-3919.
49. 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. (Pubitemid 24213470
50. Suay, L., Salvador, M.L., Abesha, E. and Klein, U. (2005) Specific roles of 50 RNA secondary structures in stabilizing transcripts in chloroplasts. Nucleic Acids Res., 33, 4754-4761. (Pubitemid 41418876
51. Higgs, D.C., Shapiro, R.S., Kindle, K.L. and Stern, D.B. (1999) Small cis-Acting sequences that specify secondary structures in a chloroplast mRNA are essential for RNA stability and translation. Mol. Cell. Biol., 19, 8479-8491.
52. Eberhard, S., Loiselay, C., Drapier, D., Bujaldon, S., Girard-Bascou, J., Kuras, R., Choquet, Y. and Wollman, F.A. (2011) Dual functions of the nucleus-encoded factor TDA1 in trapping and translation activation of atpA transcripts in Chlamydomonas reinhardtii chloroplasts. Plant J., 67, 1055-1066.
53. Barkan, A., Rojas, M., Fujii, S., Yap, A., Chong, Y.S., Bond, C.S. and Small, I. (2012) A combinatorial amino acid code for RNA recognition by pentatricopeptide repeat proteins. PLoS Genet., 8, e1002910.
54. Drager, R.G., Higgs, D.C., Kindle, K.L. and Stern, D.B. (1999) 50 to 30 exoribonucleolytic activity is a normal component of chloroplast mRNA decay pathways. Plant J., 19, 521-531.
55. Meierhoff, K., Felder, S., Nakamura, T., Bechtold, N. and Schuster, G. (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. (Pubitemid 36715187
56. 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.
57. Hotto, A.M., Schmitz, R.J., Fei, Z., Ecker, J.R. and Stern, D.B. (2011) Unexpected diversity of chloroplast noncoding RNAs as revealed by deep sequencing of the arabidopsis transcriptome. G3, 1, 559-570.
58. Luro, S., Germain, A., Sharwood, R.E. and Stern, D.B. (2013) RNase J participates in a pentatricopeptide repeat proteinmediated 50 end maturation of chloroplast mRNAs. Nucleic Acids Res., 41, 9141-9151.
59. Kuroda, H. and Maliga, P. (2003) The plastid clpP1 protease gene is essential for plant development. Nature, 425, 86-89. (Pubitemid 37101722
60. Chateigner-Boutin, A.L. and Hanson, M.R. (2002) Crosscompetition in transgenic chloroplasts expressing single editing sites reveals shared cis elements. Mol. Cell. Biol., 22, 8448-8456.
61. Chaudhuri, S., Carrer, H. and Maliga, P. (1995) Site-specific factor involved in the editing of the psbL mRNA in tobacco plastids. EMBO J., 14, 2951-2957.
62. Choquet, Y. and Vallon, O. (2000) Synthesis, assembly and degradation of thylakoid membrane proteins. Biochimie, 82, 615-634. (Pubitemid 30608456
63. Adam, Z. (2000) Chloroplast proteases: Possible regulators of gene expressioñBiochimie, 82, 647-654.
64. Baena-Gonzalez, E. and Aro, E.M. (2002) Biogenesis, assembly and turnover of photosystem II units. Philos. Trans. R. Soc. Lond. B Biol. Sci., 357, 1451-1459, discussion 1459-1460.
65. Erickson, J.D.R., Goldschmidt-Clermont, M. and Merchant, S. (1998) Assembly of Photosystem II. In Rochaix, J.-D., Goldschmidt-Clermont, M., Merchant S. (eds), The Molecular Biology of Chloroplast and Mitochondria in Chlamydomonas. Kluwer Academic Publishers, Dordrecht, pp. 255-285.
66. Markham, N.R. and Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res., 31, 3406-3415. (Pubitemid 37442169
67. Sturm, N.R., Kuras, R., Buschlen, 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.
68. Silk, G.W. and Wu, M. (1993) Posttranscriptional accumulation of chloroplast tufA (elongation factor gene) mRNA during chloroplast development in Chlamydomonas reinhardtii. Plant. Mol. Biol., 23, 87-96.
69. Drapier, D., Suzuki, H., Levy, H., Rimbault, B., Kindle, K.L., Stern, D.B. and Wollman, F.A. (1998) The chloroplast atpA gene cluster in Chlamydomonas reinhardtii. Functional analysis of a polycistronic transcription unit. Plant Physiol., 117, 629-641.