The RNA-binding protein RNP29 is an unusual Toc159 transport substrate

Frontiers in Plant Science

Volumn 5, Issue JUN, 2014, Pages

  Grimmer, Julia ^a   Rödiger, Anja ^a   Hoehenwarter, Wolfgang ^b   Helm, Stefan ^a   Baginsky, Sacha ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b LEIBNIZ INSTITUTE OF PLANT BIOCHEMISTRY   (Germany)

Author keywords

Import specificity; Mass spectrometry; Plastid protein import; Precursor accumulation; Protoplast; RNP29

Indexed keywords

EID: 84979591002     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00258     Document Type: Article

References (38)

1. Agne, B., and Kessler, F. (2009). Protein transport in organelles: the Toc complex way of preprotein import. FEBS J. 276, 1156-1165. doi: 10.1111/j.1742-4658.2009.06873.x
2. Bauer, J., Chen, K., Hiltbunner, A., Wehrli, E., Eugster, M., Schnell, D., et al. (2000). The major protein import receptor of plastids is essential for chloroplast biogenesis. Nature 403, 203-207. doi: 10.1038/35003214
3. Bienvenut, W. V., Espagne, C., Martinez, A., Majeran, W., Valot, B., Zivy, M., et al. (2011). Dynamics of post-translational modifications and protein stability in the stroma of Chlamydomonas reinhardtii chloroplasts. Proteomics 11, 1734-1750. doi: 10.1002/pmic.201000634
4. Bischof, S., Baerenfaller, K., Wildhaber, T., Troesch, R., Vidi, P. A., Roschitzki, B., et al. (2011). Plastid proteome assembly without Toc159, photosynthetic protein import and accumulation of N-acetylated plastid precursor proteins. Plant Cell 23, 3911-3928. doi: 10.1105/tpc.111.092882
5. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254. doi: 10.1016/0003-2697(76)90527-3
6. Chotewutmontri, P., Reddick, L. E., McWilliams, D. R., Campbell, I. M., and Bruce, B. D. (2012). Differential transit peptide recognition during preprotein binding and translocation into flowering plant plastids. Plant Cell 24, 3040-3059. doi: 10.1105/tpc.112.098327
7. Dutta, S., Teresinski, H. J., and Smith, M. D. (2014). A split-ubiquitin yeast two-hybrid screen to examine the substrate specificity of atToc159 and atToc132, two Arabidopsis chloroplast preprotein import receptors. PLoS ONE 9:e95026. doi: 10.1371/journal.pone.0095026
8. Ferrandez-Ayela, A., Micol-Ponce, R., Sanchez-Garcia, A. B., Alonso-Peral, M. M., Micol, J. L., and Ponce, M. R. (2013). Mutation of an Arabidopsis NatB N-alpha-terminal acetylation complex component causes pleiotropic developmental defects. PLoS ONE 8:e80697. doi: 10.1371/journal.pone.0080697
9. Helm, S., Dobritzsch, D., Rodiger, A., Agne, B., and Baginsky, S. (2014). Protein identification and quantification by data-independent acquisition and multi-parallel collision-induced dissociation mass spectrometry (MS(E)) in the chloroplast stroma proteome. J. Proteomics 98, 79-89. doi: 10.1016/j.jprot.2013.12.007
10. Hollebeke, J., Van Damme, P., and Gevaert, K. (2012). N-terminal acetylation and other functions of Nalpha-acetyltransferases. Biol. Chem. 393, 291-298. doi: 10.1515/hsz-2011-0228
11. Hwang, C. S., Shemorry, A., and Varshavsky, A. (2010). N-terminal acetylation of cellular proteins creates specific degradation signals. Science 327, 973-977. doi: 10.1126/science.1183147
12. Inoue, H., Rounds, C., and Schnell, D. J. (2010). The molecular basis for distinct pathways for protein import into Arabidopsis chloroplasts. Plant Cell 22, 1947-1960. doi: 10.1105/tpc.110.074328
13. Ivanova, Y., Smith, M. D., Chen, K., and Schnell, D. J. (2004). Members of the Toc159 import receptor family represent distinct pathways for protein targeting to plastids. Mol. Biol. Cell 15, 3379-3392. doi: 10.1091/mbc.E03-12-0923
14. Jarvis, P. (2008). Targeting of nucleus-encoded proteins to chloroplasts in plants. New Phytol. 179, 257-285. doi: 10.1111/j.1469-8137.2008.02452.x
15. Kubis, S., Patel, R., Combe, J., Bedard, J., Kovacheva, S., Lilley, K., et al. (2004). Functional specialization amongst the Arabidopsis Toc159 family of chloroplast protein import receptors. Plant Cell 16, 2059-2077. doi: 10.1105/tpc.104.023309
16. Kupsch, C., Ruwe, H., Gusewski, S., Tillich, M., Small, I., and Schmitz-Linneweber, C. (2012). 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 24, 4266-4280. doi: 10.1105/tpc.112.103002
17. Lee, D. W., Kim, J. K., Lee, S., Choi, S., Kim, S., and Hwang, I. (2008). Arabidopsis nuclear-encoded plastid transit peptides contain multiple sequence subgroups with distinctive chloroplast-targeting sequence motifs. Plant Cell 20, 1603-1622. doi: 10.1105/tpc.108.060541
18. Lee, S., Lee, D. W., Lee, Y., Mayer, U., Stierhof, Y. D., Jurgens, G., et al. (2009). Heat shock protein cognate 70-4 and an E3 ubiquitin ligase, CHIP, mediate plastid-destined precursor degradation through the ubiquitin-26S proteasome system in Arabidopsis. Plant Cell 21, 3984-4001. doi: 10.1105/tpc.109.071548
19. Li, H. M., and Teng, Y. S. (2013). Transit peptide design and plastid import regulation. Trends Plant Sci. 18, 360-366. doi: 10.1016/j.tplants.2013.04.003
20. Lorkovic, 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. doi: 10.1093/nar/30.3.623
21. Martinez, A., Traverso, J. A., Valot, B., Ferro, M., Espagne, C., Ephritikhine, G., et al. (2008). Extent of N-terminal modifications in cytosolic proteins from eukaryotes. Proteomics 8, 2809-2831. doi: 10.1002/pmic.200701191
22. Motohashi, R., Rodiger, A., Agne, B., Baerenfaller, K., and Baginsky, S. (2012). Common and specific protein accumulation patterns in different albino/pale-green mutants reveals regulon organization at the proteome level. Plant Physiol. 160, 2189-2201. doi: 10.1104/pp.112.204032
23. Pesaresi, P., Gardner, N. A., Masiero, S., Dietzmann, A., Eichacker, L., Wickner, R., et al. (2003). Cytoplasmic N-terminal protein acetylation is required for efficient photosynthesis in Arabidopsis. Plant Cell 15, 1817-1832. doi: 10.1105/tpc.012377
24. Polevoda, B., and Sherman, F. (2003). N-terminal acetyltransferases and sequence requirements for N-terminal acetylation of eukaryotic proteins. J. Mol. Biol. 325, 595-622. doi: 10.1016/S0022-2836(02)01269-X
25. Reiland, S., Messerli, G., Baerenfaller, K., Gerrits, B., Endler, A., Grossmann, J., et al. (2009). Large-scale Arabidopsis phosphoproteome profiling reveals novel chloroplast kinase substrates and phosphorylation networks. Plant Physiol. 150, 889-903. doi: 10.1104/pp.109.138677
26. Richter, S., and Lamppa, G. K. (1999). Stromal processing peptidase binds transit peptides and initiates their ATP-dependent turnover in chloroplasts. J. Cell Biol. 147, 33-44. doi: 10.1083/jcb.147.1.33
27. Rodiger, A., Agne, B., Baerenfaller, K., and Baginsky, S. (2014). Arabidopsis proteomics: a simple and standardizable workflow for quantitative proteome characterization. Methods Mol. Biol. 1072, 275-288. doi: 10.1007/978-1-62703-631-3_20
28. Schleiff, E., and Becker, T. (2011). Common ground for protein translocation: access control for mitochondria and chloroplasts. Nat. Rev. Mol. Cell Biol. 12, 48-59. doi: 10.1038/nrm3027
29. Sherman, F., Stewart, J. W., and Tsunasawa, S. (1985). Methionine or not methionine at the beginning of a protein. Bioessays 3, 27-31. doi: 10.1002/bies.950030108
30. Silva, J. C., Gorenstein, M. V., Li, G. Z., Vissers, J. P. C., and Geromanos, S. J. (2006). Absolute quantification of proteins by LCMSE: a virtue of parallel MS acquisition. Mol. Cell. Proteomics 5, 144-156. doi: 10.1074/mcp.M500230-MCP200
31. Smith, M. D., Rounds, C. M., Wang, F., Chen, K., Afitlhile, M., and Schnell, D. J. (2004). atToc159 is a selective transit peptide receptor for the import of nucleus-encoded chloroplast proteins. J. Cell Biol. 165, 323-334. doi: 10.1083/jcb.200311074
32. Strittmatter, P., Soll, J., and Bolter, B. (2010). The chloroplast protein import machinery: a review. Methods Mol. Biol. 619, 307-321. doi: 10.1007/978-1-60327-412-8_18
33. Teng, Y. S., Chan, P. T., and Li, H. M. (2012). Differential age-dependent import regulation by signal peptides. PLoS Biol. 10:e1001416. doi: 10.1371/journal.pbio.1001416
34. Uberlacker, B., and Werr, W. (1996). Vectors with rare-cutter restriction enzyme sites for expression of open reading frames in transgenic plants. Mol. Breed. 2, 293-295. doi: 10.1007/BF00564208
35. van Wijk, K. J., and Baginsky, S. (2011). Plastid proteomics in higher plants: current state and future goals. Plant Physiol. 155, 1578-1588. doi: 10.1104/pp.111.172932
36. 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. doi: 10.1002/pmic.200500657
37. Wessel, D. and Flugge, U. I. (1984). A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem. 138, 141-143. doi: 10.1016/0003-2697(84)90782-6
38. Zybailov, B., Rutschow, H., Friso, G., Rudella, A., Emanuelsson, O., Sun, Q., et al. (2008). Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. PLoS ONE 3:e1994. doi: 10.1371/journal.pone.0001994