A CRM domain protein functions dually in group I and group II intron splicing in land plant chloroplasts

Plant Cell

Volumn 19, Issue 12, 2007, Pages 3864-3875

  Asakura, Yukari ^a   Barkan, Alice ^a  

^a UNIVERSITY OF OREGON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BIOASSAY; PIGMENTS; PROTEINS; RNA; SEED;

CHLOROPLASTS; CRM DOMAIN; INTRONS;

PLANTS (BOTANY);

ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); EMBRYOPHYTA; ZEA MAYS;

EID: 39149118562     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.107.055160     Document Type: Article

References (35)

1. Alonso, J.M., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
2. Asakura, Y., and Barkan, A. (2006). Arabidopsis orthologs of maize chloroplast splicing factors promote splicing of orthologous and species-specific group II introns. Plant Physiol. 142: 1656-1663.
3. Ban, N., Nissen, P., Hansen, J., Moore, P., and Steitz, T. (2000). The complete atomic structure of the large ribosomal subunit at 2.4 A resolution. Science 289: 905-920.
4. Barkan, A. (1998). Approaches to investigating nuclear genes that function in chloroplast biogenesis in land plants. Methods Enzymol. 297: 38-57.
5. Barkan, A., Klipcan, L., Ostersetzer, O., Kawamura, T., Asakura, Y., and Watkins, K. (2007). The CRM domain: An RNA binding module derived from an ancient ribosome-associated protein. RNA 13: 55-64.
6. Bonen, L., and Vogel, J. (2001). The ins and outs of group II introns. Trends Genet. 17: 322-331.
7. Boudreau, E., Takahashi, Y., Lemieux, C., Turmel, M., and Rochaix, J. (1997). The chloroplast ycf3 and ycf4 open reading frames of Chlamydomonas reinhardtii are required for the accumulation of the photosystem I complex. EMBO J. 16: 6095-6104.
8. Emanuelsson, O., and von Heijne, G. (2001). Prediction of organellar targeting signals. Biochim. Biophys. Acta 1541: 114-119.
9. Halls, C., Mohr, S., Del Campo, M., Yang, Q., Jankowsky, E., and Lambowitz, A.M. (2007). Involvement of DEAD-box proteins in group I and group II intron splicing. Biochemical characterization of Mss116p, ATP hydrolysis-dependent and -independent mechanisms, and general RNA chaperone activity. J. Mol. Biol. 365: 835-855.
10. Hattori, M., Miyake, H., and Sugita, M. (2007). A pentatricopeptide repeat protein is required for RNA processing of clpP pre-mRNA in moss chloroplasts. J. Biol. Chem. 282: 10773-10782.
11. Hsieh, J., Andrews, A.J., and Fierke, C.A. (2004). Roles of protein subunits in RNA-protein complexes: lessons from ribonuclease P. Biopolymers 73: 79-89.
12. Huang, H.R., Rowe, C.E., Mohr, S., Jiang, Y., Lambowitz, A.M., and Perlman, P.S. (2005). The splicing of yeast mitochondrial group I and group II introns requires a DEAD-box protein with RNA chaperone function. Proc. Natl. Acad. Sci. USA 102: 163-168.
13. Jenkins, B., Kulhanek, D., 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.
14. Kuroda, H., and Maliga, P. (2003). The plastid clpP1 protease gene is essential for plant development. Nature 425: 86-89.
15. 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.
16. Michel, F., Umesono, K., and Ozeki, H. (1989). Comparative and functional anatomy of group II catalytic introns - A review. Gene 82: 5-30.
17. 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.
18. Ostersetzer, O., Watkins, K., Cooke, A., and Barkan, A. (2005). CRS1, a chloroplast group II intron splicing factor, promotes intron folding through specific interactions with two intron domains. Plant Cell 17: 241-255.
19. Ostheimer, G., Barkan, A., and Matthews, B. (2002). Crystal structure of E. coli YhbY: A representative of a novel class of RNA binding proteins. Structure 10: 1593-1601.
20. Ostheimer, G., Williams-Carrier, R., Belcher, S., Osborne, E., Gierke, J., and Barkan, A. (2003). Group II intron splicing factors derived by diversification of an ancient RNA binding module. EMBO J. 22: 3919-3929.
21. Ostheimer, G.J., Rojas, M., Hadjivassiliou, H., and Barkan, A. (2006). Formation of the CRS2-CAF2 group ll intron splicing complex is mediated by a 22 amino acid motif in the C-terminal region of CAF2. J. Biol. Chem. 281: 4732-4738.
22. Pyle, A., and Lambowitz, A. (2006). Group II introns: Ribozymes that splice RNA and invade DNA. In The RNA World, R. Gesteland, T. Cech, and J. Atkins, eds (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press), pp. 469-506.
23. Roy, L.M., and Barkan, A. (1998). A secY homologue is required for the elaboration of the chloroplast thylakoid membrane and for normal chloroplast gene expression. J. Cell Biol. 141: 385-395.
24. Ruf, S., Kossel, H., and Bock, R. (1997). Targeted inactivation of a tobacco intron-containing open reading frame reveals a novel chloroplast-encoded photosystem I-related gene. J. Cell Biol. 139: 95-102.
25. 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 5′-region of mRNAs whose translation it activates. Plant Cell 17: 2791-2804.
26. 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.
27. Sessions, A., et al. (2002). A high-throughput Arabidopsis reverse genetics system. Plant Cell 14: 2985-2994.
28. Simon, D., Fewer, D., Friedl, T., and Bhattacharya, D. (2003). Phylogeny and self-splicing ability of the plastid tRNA-Leu group I Intron. J. Mol. Evol. 57: 710-720.
29. Solem, A., Zingler, N., and Pyle, A.M. (2006). A DEAD protein that activates intron self-splicing without unwinding RNA. Mol. Cell 24: 611-617.
30. Till, B., Schmitz-Linneweber, C., Williams-Carrier, R., and Barkan, A. (2001). CRS1 is a novel group II intron splicing factor that was derived from a domain of ancient origin. RNA 7: 1227-1238.
31. Vogel, J., Boerner, T., and Hess, W. (1999). Comparative analysis of splicing of the complete set of chloroplast group II introns in three higher plant mutants. Nucleic Acids Res. 27: 3866-3874.
32. Watkins, K., Kroeger, T., Cooke, A., Williams-Carrier, R., Friso, G., Belcher, S., van Wijk, K.J., and Barkan, A. (2007). A ribonuclease III domain protein functions in group II intron splicing in maize chloroplasts. Plant Cell 19: 2606-2623.
33. Weeks, K.M. (1997). Protein-facilitated RNA folding. Curr. Opin. Struct. Biol. 7: 336-342.
34. Williams, P., and Barkan, A. (2003). A chloroplast-localized PPR protein required for plastid ribosome accumulation. Plant J. 36: 675-686.
35. Xu, M.-Q., Kaathe, S., Goodrich-Blair, H., Nierzwicki-Bauer, S., and Shub, D. (1990). Bacterial origin of a chloroplast intron: Conserved self-splicing group I introns in cyanobacteria. Science 250: 1566-1569.