Arabidopsis chloroplast RNA binding proteins CP31A and CP29A associate with large transcript pools and confer cold stress tolerance by influencing multiple chloroplast RNA processing steps

Plant Cell

Volumn 24, Issue 10, 2012, Pages 4266-4280

  Kupsch, Christiane ^a   Ruwe, Hannes ^a   Gusewski, Sandra ^a   Tillich, Michael ^a,c   Small, Ian ^b   Schmitz Linneweber, Christian ^a  

^a HUMBOLDT UNIVERSITY   (Germany)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84870679344     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.112.103002     Document Type: Article

References (55)

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. (2011). Expression of plastid genes: Organelle-specific elaborations on a prokaryotic scaffold. Plant Physiol. 155: 1520-1532.
3. Beick, S., Schmitz-Linneweber, C., Williams-Carrier, R., Jensen, B., and Barkan, A. (2008). The pentatricopeptide repeat protein PPR5 stabilizes a specific tRNA precursor in maize chloroplasts. Mol. Cell. Biol. 28: 5337-5347.
4. Cho, W.K., Geimer, S., and Meurer, J. (2009). Cluster analysis and comparison of various chloroplast transcriptomes and genes in Arabidopsis thaliana. DNA Res. 16: 31-44.
5. Churin, Y., Hess, W.R., and Börner, T. (1999). Cloning and characterization of three cDNAs encoding chloroplast RNA-binding proteins from barley (Hordeum vulgare L.): Differential regulation of expression by light and plastid development. Curr. Genet. 36: 173-181.
6. Cléry, A., Blatter, M., and Allain, F.H. (2008). RNA recognition motifs: Boring? Not quite. Curr. Opin. Struct. Biol. 18: 290-298.
7. de Longevialle, A.F., Hendrickson, L., Taylor, N.L., Delannoy, E., Lurin, C., Badger, M., Millar, A.H., and Small, I. (2008). The pentatricopeptide repeat gene OTP51 with two LAGLIDADG motifs is required for the cis-splicing of plastid ycf3 intron 2 in Arabidopsis thaliana. Plant J. 56: 157-168.
8. Dreyfuss, G., Kim, V.N., and Kataoka, N. (2002). Messenger-RNAbinding proteins and the messages they carry. Nat. Rev. Mol. Cell Biol. 3: 195-205.
9. Fleischmann, T.T., Scharff, L.B., Alkatib, S., Hasdorf, S., Schöttler, M.A., and Bock, R. (2011). Nonessential plastid-encoded ribosomal proteins in tobacco: A developmental role for plastid translation and implications for reductive genome evolution. Plant Cell 23: 3137-3155.
10. Grennan, A.K., and Ort, D.R. (2007). Cool temperatures interfere with D1 synthesis in tomato by causing ribosomal pausing. Photosynth. Res. 94: 375-385.
11. Hajdukiewicz, P.T., Allison, L.A., and Maliga, P. (1997). The two RNA polymerases encoded by the nuclear and the plastid compartments transcribe distinct groups of genes in tobacco plastids. EMBO J. 16: 4041-4048.
12. Hayes, R., Kudla, J., Schuster, G., Gabay, L., Maliga, P., and Gruissem, W. (1996). Chloroplast mRNA 39-end processing by a high molecular weight protein complex is regulated by nuclear encoded RNA binding proteins. EMBO J. 15: 1132-1141.
13. Hirose, T., and Sugiura, M. (2001). Involvement of a site-specific trans-acting factor and a common RNA-binding protein in the editing of chloroplast mRNAs: Development of a chloroplast in vitro RNA editing system. EMBO J. 20: 1144-1152.
14. Hopkins, W.G., and Elfman, B. (1984). Temperature-induced chloroplast ribosome deficiency in virescent maize. J. Hered. 75: 207-211.
15. 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.
16. Jacobs, J., and Kück, U. (2011). Function of chloroplast RNA-binding proteins. Cell. Mol. Life Sci. 68: 735-748.
17. Keene, J.D. (2007). RNA regulons: Coordination of post-transcriptional events. Nat. Rev. Genet. 8: 533-543.
18. Kenan, D.J., Query, C.C., and Keene, J.D. (1991). RNA recognition: Towards identifying determinants of specificity. Trends Biochem. Sci. 16: 214-220.
19. Kleffmann, T., von Zychlinski, A., Russenberger, D., Hirsch-Hoffmann, M., Gehrig, P., Gruissem, W., and Baginsky, S. (2007). Proteome dynamics during plastid differentiation in rice. Plant Physiol. 143: 912-923.
20. Krecic, A.M., and Swanson, M.S. (1999). hnRNP complexes: Composition, structure, and function. Curr. Opin. Cell Biol. 11: 363-371.
21. Kroeger, T.S., Watkins, K.P., Friso, G., van Wijk, K.J., and Barkan, A. (2009). A plant-specific RNA-binding domain revealed through analysis of chloroplast group II intron splicing. Proc. Natl. Acad. Sci. USA 106: 4537-4542.
22. Kunst, L. (1998). Preparation of physiologically active chloroplasts from Arabidopsis. Methods Mol Biol. 82: 43-48.
23. Kusumi, K., Sakata, C., Nakamura, T., Kawasaki, S., Yoshimura, A., and Iba, K. (2011). A plastid protein NUS1 is essential for buildup of the genetic system for early chloroplast development under cold stress conditions. Plant J. 68: 1039-1050.
24. Li, Y.Q., and Sugiura, M. (1990). Three distinct ribonucleoproteins from tobacco chloroplasts: Each contains a unique amino terminal acidic domain and two ribonucleoprotein consensus motifs. EMBO J. 9: 3059-3066.
25. Li, Y.Q., and Sugiura, M. (1991). Nucleic acid-binding specificities of tobacco chloroplast ribonucleoproteins. Nucleic Acids Res. 19: 2893-2896.
26. Liu, X., Rodermel, S.R., and Yu, F. (2010). A var2 leaf variegation suppressor locus, SUPPRESSOR OF VARIEGATION3, encodes a putative chloroplast translation elongation factor that is important for chloroplast development in the cold. BMC Plant Biol. 10: 287.
27. Lorković, Z.J., and Barta, A. (2002). Genome analysis: RNA recognition motif (RRM) and K homology (KH) domain RNA-binding proteins from the flowering plant Arabidopsis thaliana. Nucleic Acids Res. 30: 623-635.
28. Maris, C., Dominguez, C., and Allain, F.H. (2005). The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J. 272: 2118-2131.
29. Maruyama, K., Sato, N., and Ohta, N. (1999). Conservation of structure and cold-regulation of RNA-binding proteins in cyanobacteria: probable convergent evolution with eukaryotic glycinerich RNA-binding proteins. Nucleic Acids Res. 27: 2029-2036.
30. Mentzen, W.I., and Wurtele, E.S. (2008). Regulon organization of Arabidopsis. BMC Plant Biol. 8: 99.
31. Millerd, A., Goodchild, D.J., and Spencer, D. (1969). Studies on a maize mutant sensitive to low temperature II. Chloroplast structure, development, and physiology. Plant Physiol. 44: 567-583.
32. Mochizuki, N., Brusslan, J.A., Larkin, R., Nagatani, A., and Chory, J. (2001). Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proc. Natl. Acad. Sci. USA 98: 2053-2058.
33. Nakamura, T., Ohta, M., Sugiura, M., and Sugita, M. (1999). Chloroplast ribonucleoproteins are associated with both mRNAs and intron-containing precursor tRNAs. FEBS Lett. 460: 437-441.
34. Nakamura, T., Ohta, M., Sugiura, M., and Sugita, M. (2001). Chloroplast ribonucleoproteins function as a stabilizing factor of ribosome-free mRNAs in the stroma. J. Biol. Chem. 276: 147-152.
35. Nishimura, K., Ashida, H., Ogawa, T., and Yokota, A. (2010). A DEAD box protein is required for formation of a hidden break in Arabidopsis chloroplast 23S rRNA. Plant J. 63: 766-777.
36. Ohta, M., Sugita, M., and Sugiura, M. (1995). Three types of nuclear genes encoding chloroplast RNA-binding proteins (cp29, cp31 and cp33) are present in Arabidopsis thaliana: Presence of cp31 in chloroplasts and its homologue in nuclei/cytoplasms. Plant Mol. Biol. 27: 529-539.
37. Petersen, K., Schöttler, M.A., Karcher, D., Thiele, W., and Bock, R. (2011). Elimination of a group II intron from a plastid gene causes a mutant phenotype. Nucleic Acids Res. 39: 5181-5192.
38. Pfalz, J., Bayraktar, O.A., Prikryl, J., and Barkan, A. (2009). Sitespecific binding of a PPR protein defines and stabilizes 59 and 39 mRNA termini in chloroplasts. EMBO J. 28: 2042-2052.
39. Raab, S., Toth, Z., de Groot, C., Stamminger, T., and Hoth, S. (2006). ABA-responsive RNA-binding proteins are involved in chloroplast and stromule function in Arabidopsis seedlings. Planta 224: 900-914.
40. Rogalski, M., Ruf, S., and Bock, R. (2006). Tobacco plastid ribosomal protein S18 is essential for cell survival. Nucleic Acids Res. 34: 4537-4545.
41. Rogalski, M., Schöttler, M.A., Thiele, W., Schulze, W.X., and Bock, R. (2008). Rpl33, a nonessential plastid-encoded ribosomal protein in tobacco, is required under cold stress conditions. Plant Cell 20: 2221-2237.
42. Ruwe, H., Kupsch, C., Teubner, M., and Schmitz-Linneweber, C. (2011). The RNA-recognition motif in chloroplasts. J. Plant Physiol. 168: 1361-1371.
43. 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.
44. Schmitz-Linneweber, C., Williams-Carrier, R., and Barkan, A. (2005). RNA immunoprecipitation and microarray analysis show a chloroplast pentatricopeptide repeat protein to be associated with the 59 region of mRNAs whose translation it activates. Plant Cell 17: 2791-2804.
45. Schmitz-Linneweber, C., Williams-Carrier, R.E., Williams-Voelker, P.M., Kroeger, T.S., Vichas, A., and Barkan, A. (2006). A pentatricopeptide repeat protein facilitates the trans-splicing of the maize chloroplast rps12 pre-mRNA. Plant Cell 18: 2650-2663.
46. Schuster, G., and Gruissem, W. (1991). Chloroplast mRNA 39 end processing requires a nuclear-encoded RNA-binding protein. EMBO J. 10: 1493-1502.
47. Stern, D.B., Goldschmidt-Clermont, M., and Hanson, M.R. (2010). Chloroplast RNA metabolism. Annu. Rev. Plant Biol. 61: 125-155.
48. Tillich, M., Beick, S., and Schmitz-Linneweber, C. (2010). Chloroplast RNA-binding proteins: repair and regulation of chloroplast transcripts. RNA Biol. 7: 172-178.
49. Tillich, M., Hardel, S.L., Kupsch, C., Armbruster, U., Delannoy, E., Gualberto, J.M., Lehwark, P., Leister, D., Small, I.D., and Schmitz-Linneweber, C. (2009). Chloroplast ribonucleoprotein CP31A is required for editing and stability of specific chloroplast mRNAs. Proc. Natl. Acad. Sci. USA 106: 6002-6007.
50. Tokuhisa, J.G., Vijayan, P., Feldmann, K.A., and Browse, J.A. (1998). Chloroplast development at low temperatures requires a homolog of DIM1, a yeast gene encoding the 18S rRNA dimethylase. Plant Cell 10: 699-711.
51. Wang, B.C., Wang, H.X., Feng, J.X., Meng, D.Z., Qu, L.J., and Zhu, Y.X. (2006). Post-translational modifications, but not transcriptional regulation, of major chloroplast RNA-binding proteins are related to Arabidopsis seedling development. Proteomics 6: 2555-2563.
52. Yamori, W., Noguchi, K., Hikosaka, K., and Terashima, I. (2010). Phenotypic plasticity in photosynthetic temperature acclimation among crop species with different cold tolerances. Plant Physiol. 152: 388-399.
53. Zhelyazkova, P., Hammani, K., Rojas, M., Voelker, R., Vargas-Suárez, M., Börner, T., and Barkan, A. (2012). Protein-mediated protection as the predominant mechanism for defining processed mRNA termini in land plant chloroplasts. Nucleic Acids Res. 40: 3092-3105.
54. Zoschke, R., Nakamura, M., Liere, K., Sugiura, M., Börner, T., and Schmitz-Linneweber, C. (2010). An organellar maturase associates with multiple group II introns. Proc. Natl. Acad. Sci. USA 107: 3245-3250.
55. Zubo, Y. O., et al. (2008). Cytokinin stimulates chloroplast transcription in detached barley leaves. Plant Physiol 148: 1082-1093.