The pentatricopeptide repeat-SMR protein ATP4 promotes translation of the chloroplast atpB/E mRNA

Plant Journal

Volumn 72, Issue 4, 2012, Pages 547-558

  Zoschke, Reimo ^a,b   Kroeger, Tiffany ^b   Belcher, Susan ^b   Schöttler, Mark Aurel ^c   Barkan, Alice ^b   Schmitz Linneweber, Christian ^a  

^a HUMBOLDT UNIVERSITY   (Germany)

^b UNIVERSITY OF OREGON   (United States)

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

Author keywords

chloroplast; MutS related; pentatricopeptide repeat; RNA binding; translation; Zea mays

Indexed keywords

CHLOROPLAST; MUTS-RELATED; PENTATRICOPEPTIDE REPEATS; RNA BINDING; ZEA MAYS;

GENE EXPRESSION; GRAIN (AGRICULTURAL PRODUCT); PROTEINS; RNA; TRANSLATION (LANGUAGES);

CHLOROPHYLL;

CHLOROPLAST RNA; MESSENGER RNA; PLANT RNA; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; VEGETABLE PROTEIN;

5' UNTRANSLATED REGION; ALLELE; AMINO ACID SEQUENCE; ARTICLE; CHLOROPLAST; ENZYME ACTIVATION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOPRECIPITATION; MAIZE; METABOLISM; OPEN READING FRAME; PHOTOSYNTHESIS; PROTEIN SYNTHESIS; PROTEIN TERTIARY STRUCTURE; RIBOSOME;

5' UNTRANSLATED REGIONS; ALLELES; CHLOROPLAST PROTON-TRANSLOCATING ATPASES; CHLOROPLASTS; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, PLANT; IMMUNOPRECIPITATION; OPEN READING FRAMES; PHOTOSYNTHESIS; PLANT PROTEINS; PROTEIN BIOSYNTHESIS; PROTEIN STRUCTURE, TERTIARY; REPETITIVE SEQUENCES, AMINO ACID; RIBOSOMES; RNA, CHLOROPLAST; RNA, MESSENGER; RNA, PLANT; ZEA MAYS;

ARABIDOPSIS; ZEA MAYS;

EID: 84868471721     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2012.05081.x     Document Type: Article

References (56)

1. Baker, N.R., Harbinson, J., and, Kramer, D.M., (2007) Determining the limitations and regulation of photosynthetic energy transduction in leaves. Plant, Cell Environ. 30, 1107-1125.
2. Barkan, A., (1993) Nuclear mutants of maize with defects in chloroplast polysome assembly have altered chloroplast RNA metabolism. Plant Cell, 5, 389-402.
3. Barkan, A., (1998) Approaches to investigating nuclear genes that function in chloroplast biogenesis in land plants. Methods Enzymol. 297, 38-57.
4. Barkan, A., (2011) Expression of plastid genes: organelle-specific elaborations on a prokaryotic scaffold. Plant Physiol., 155, 1520-1532.
5. 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.
6. Barkan, A., Klipcan, L., Ostersetzer, O., Kawamura, T., Asakura, Y., and, Watkins, K.P., (2007) The CRM domain: an RNA binding module derived from an ancient ribosome-associated protein. RNA, 13, 55-64.
7. 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.
8. Bhandari, D., Guha, K., Bhaduri, N., and, Saha, P., (2011) Ubiquitination of mRNA cycling sequence binding protein from Leishmania donovani (LdCSBP) modulates the RNA endonuclease activity of its Smr domain. FEBS Lett. 585, 809-813.
9. Boulouis, A., Raynaud, C., Bujaldon, S., Aznar, A., Wollman, F.A., and, Choquet, Y., (2011) The nucleus-encoded trans-acting factor MCA1 plays a critical role in the regulation of cytochrome f synthesis in Chlamydomonas chloroplasts. Plant Cell, 23, 333-349.
10. Cai, W., Okuda, K., Peng, L., and, Shikanai, T., (2011) PROTON GRADIENT REGULATION 3 recognizes multiple targets with limited similarity and mediates translation and RNA stabilization in plastids. Plant J. 67, 318-327.
11. Diercks, T., Ab, E., Daniels, M.A., de Jong, R.N., Besseling, R., Kaptein, R., and, Folkers, G.E., (2008) Solution structure and characterization of the DNA-binding activity of the B3BP-Smr domain. J. Mol. Biol. 383, 1156-1170.
12. Drapier, D., Rimbault, B., Vallon, O., Wollman, F.A., and, Choquet, Y., (2007) Intertwined translational regulations set uneven stoichiometry of chloroplast ATP synthase subunits. EMBO J. 26, 3581-3591.
13. Fukui, K., and, Kuramitsu, S., (2011) Structure and function of the small MutS-related domain. Mol. Biol. Int. 2011, 691735.
14. Gillman, J.D., Bentolila, S., and, Hanson, M.R., (2007) The petunia restorer of fertility protein is part of a large mitochondrial complex that interacts with transcripts of the CMS-associated locus. Plant J. 49, 217-227.
15. Hammani, K., Okuda, K., Tanz, S.K., Chateigner-Boutin, A.L., Shikanai, T., and, Small, I., (2009) A study of new Arabidopsis chloroplast RNA editing mutants reveals general features of editing factors and their target sites. Plant Cell, 21, 3686-3699.
16. Hammani, K., des Francs-Small, C.C., Takenaka, M., Tanz, S.K., Okuda, K., Shikanai, T., Brennicke, A., and, Small, I., (2011) The pentatricopeptide repeat protein OTP87 is essential for RNA editing of nad7 and atp1 transcripts in Arabidopsis mitochondria. J. Biol. Chem. 286, 21361-21371.
17. Hattori, M., and, Sugita, M., (2009) A moss pentatricopeptide repeat protein binds to the 3' end of plastid clpP pre-mRNA and assists with mRNA maturation. FEBS J. 276, 5860-5869.
18. Hirose, T., and, Sugiura, M., (2004) Multiple elements required for translation of plastid atpB mRNA lacking the Shine-Dalgarno sequence. Nucleic Acids Res. 32, 3503-3510.
19. Keren, I., Klipcan, L., Bezawork-Geleta, A., Kolton, M., Shaya, F., and, Ostersetzer-Biran, O., (2008) Characterization of the molecular basis of group II intron RNA recognition by CRS1-CRM domains. J. Biol. Chem. 283, 23333-23342.
20. Kotera, E., Tasaka, M., and, Shikanai, T., (2005) A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts. Nature, 433, 326-330.
21. Koussevitzky, S., Nott, A., Mockler, T.C., Hong, F., Sachetto-Martins, G., Surpin, M., Lim, J., Mittler, R., and, Chory, J., (2007) Signals from chloroplasts converge to regulate nuclear gene expression. Science, 316, 715-719.
22. 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.
23. Lahmy, S., Barneche, F., Derancourt, J., Filipowicz, W., Delseny, M., and, Echeverria, M., (2000) A chloroplastic RNA-binding protein is a new member of the PPR family. FEBS Lett. 480, 255-260.
24. Liu, X., Yu, F., and, Rodermel, S., (2010) An Arabidopsis pentatricopeptide repeat protein, SUPPRESSOR OF VARIEGATION7, is required for FtsH-mediated chloroplast biogenesis. Plant Physiol. 154, 1588-1601.
25. 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.
26. Lurin, C., Andres, C., Aubourg, S., et al. (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell, 16, 2089-2103.
27. McCormac, D.J., and, Barkan, A., (1999) A nuclear gene in maize required for the translation of the chloroplast atpB/E mRNA. Plant Cell, 11, 1709-1716.
28. Moreira, D., and, Philippe, H., (1999) Smr: a bacterial and eukaryotic homologue of the C-terminal region of the MutS2 family. Trends Biochem. Sci. 24, 298-300.
29. Nishio, J.N., and, Whitmarsh, J., (1993) Dissipation of the proton electrochemical potential in intact chloroplasts. II. The pH gradient monitored by cytochrome f reduction kinetics. Plant Physiol. 101, 89-96.
30. Okuda, K., Nakamura, T., Sugita, M., Shimizu, T., and, Shikanai, T., (2006) A pentatricopeptide repeat protein is a site recognition factor in chloroplast RNA editing. J. Biol. Chem. 281, 37661-37667.
31. Ostheimer, G.J., Barkan, A., and, Matthews, B.W., (2002) Crystal structure of E. coli YhbY: a representative of a novel class of RNA binding proteins. Structure, 10, 1593-1601.
32. Ostheimer, G.J., 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 domain. EMBO J. 22, 3919-3929.
33. O'Toole, N., Hattori, M., Andres, C., Iida, K., Lurin, C., Schmitz-Linneweber, C., Sugita, M., and, Small, I., (2008) On the expansion of the pentatricopeptide repeat gene family in plants. Mol. Biol. Evol. 25, 1120-1128.
34. Pfalz, J., Liere, K., Kandlbinder, A., Dietz, K.J., and, Oelmuller, R., (2006) pTAC2, -6, and -12 are components of the transcriptionally active plastid chromosome that are required for plastid gene expression. Plant Cell, 18, 176-197.
35. Pfalz, J., Bayraktar, O.A., Prikryl, J., and, Barkan, A., (2009) Site-specific binding of a PPR protein defines and stabilizes 5' and 3' mRNA termini in chloroplasts. EMBO J. 28, 2042-2052.
36. 6f and ATP synthase complexes in tobacco: transformation with antisense RNA against nuclear-encoded transcripts for the Rieske FeS and ATPd polypeptides. Aust. J. Plant Physiol. 22, 285-297.
37. 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.
38. Rott, M., Martins, N.F., Thiele, W., Lein, W., Bock, R., Kramer, D.M., and, Schöttler, M.A., (2011) ATP synthase repression in tobacco restricts photosynthetic electron transport, CO2 assimilation, and plant growth by overacidification of the thylakoid lumen. Plant Cell, 23, 304-321.
39. 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.
40. Scharff, L.B., Childs, L., Walther, D., and, Bock, R., (2011) Local absence of secondary structure permits translation of mRNAs that lack ribosome-binding sites. PLoS Genet. 7, e1002155.
41. Schmitz-Linneweber, C., and, Small, I., (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci. 13, 663-670.
42. 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.
43. Schmitz-Linneweber, C., Williams-Carrier, R., Williams, P., Kroeger, T., Vichas, A., and, Barkan, A., (2006) A pentatricopeptide repeat protein binds to and facilitates the trans-splicing of the maize chloroplast rps12 pre-mRNA. Plant Cell, 18, 2650-2663.
44. 6f complex. J. Biol. Chem. 282, 976-985.
45. Schöttler, M.A., Flügel, C., Thiele, W., Stegemann, S., and, Bock, R., (2007) The plastome-encoded PsaJ subunit is required for efficient photosystem I excitation, but not for plastocyanin oxidation in tobacco. Biochem. J. 403, 251-260.
46. Small, I., and, Peeters, N., (2000) The PPR motif-a TPR-related motif prevalent in plant organellar proteins. Trends Biochem. Sci. 25, 46-47.
47. Stahl, D.J., Rodermel, S.R., Bogorad, L., and, Subramanian, A.R., (1993) Co-transcription pattern of an introgressed operon in the maize chloroplast genome comprising four ATP synthase subunit genes and the ribosomal rps2. Plant Mol. Biol. 21, 1069-1076.
48. Stern, D.B., Goldschmidt-Clermont, M., and, Hanson, M.R., (2010) Chloroplast RNA metabolism. Annu. Rev. Plant Biol. 61, 125-155.
49. Takahashi, Y., Goldschmidt-Clermont, M., Soen, S.-Y., Franzen, L.G., and, Rochaix, J.-D., (1991) Directed chloroplast transformation in Chlamydomonas reinhardtii: insertional inactivation of the psaC gene encoding the iron sulfur protein destabilizes photosystem I. EMBO J. 10, 2033-2040.
50. Takizawa, K., Cruz, J.A., Kanazawa, A., and, Kramer, D.M., (2007) The thylakoid proton motive force in vivo. Quantitative, non-invasive probes, energetics, and regulatory consequences of light-induced pmf. Biochim. Biophys. Acta, 1767, 1233-1244.
51. Tasaki, E., Hattori, M., and, Sugita, M., (2010) The moss pentatricopeptide repeat protein with a DYW domain is responsible for RNA editing of mitochondrial ccmFc transcript. Plant J. 62, 560-570.
52. 6f complex in maize. Mol. Gen. Genet. 249, 507-514.
53. Williams, P.M., and, Barkan, A., (2003) A chloroplast-localized PPR protein required for plastid ribosome accumulation. Plant J. 36, 675-686.
54. Williams-Carrier, R., Kroeger, T., and, Barkan, A., (2008) Sequence-specific binding of a chloroplast pentatricopeptide repeat protein to its native group II intron ligand. RNA, 14, 1930-1941.
55. Woodson, J.D., and, Chory, J., (2008) Coordination of gene expression between organellar and nuclear genomes. Nat. Rev. Genet. 9, 383-395.
56. Zoschke, R., Nakamura, M., Liere, K., Sugiura, M., Borner, T., and, Schmitz-Linneweber, C., (2010) An organellar maturase associates with multiple group II introns. Proc. Natl Acad. Sci. USA, 107, 3245-3250.