RNA PROCESSING FACTOR 5 is required for efficient 5′ cleavage at a processing site conserved in RNAs of three different mitochondrial genes in Arabidopsis thaliana

Plant Journal

Volumn 74, Issue 4, 2013, Pages 593-604

  Hauler, Aron ^a   Jonietz, Christian ^a   Stoll, Birgit ^a   Stoll, Katrin ^a   Braun, Hans Peter ^b   Binder, Stefan ^a  

^a UNIVERSITY OF ULM   (Germany)

^b LEIBNIZ UNIVERSITY HANNOVER   (Germany)

Author keywords

5 RNA Processing; Arabidopsis thaliana; mitochondria; P class Pentatricopeptide Repeat Proteins; ribosomal RNA

Indexed keywords

ARABIDOPSIS THALIANA; CYTOPLASMIC MALE-STERILE; MITOCHONDRIAL GENES; MITOCHONDRIAL PROTEIN; PENTATRICOPEPTIDE REPEAT PROTEIN; PRECURSOR MOLECULES; RIBOSOMAL RNA; RNA PROCESSING;

MITOCHONDRIA; PLANTS (BOTANY); PROTEINS; SEED;

RNA;

ARABIDOPSIS PROTEIN; MESSENGER RNA; MITOCHONDRIAL MESSENGER RNA; MITOCHONDRIAL PROTEIN; PENTATRICOPEPTIDE REPEAT PROTEIN, ARABIDOPSIS; PLANT RNA; RIBOSOME RNA; RNA BINDING PROTEIN; RNA PROCESSING FACTOR 5, ARABIDOPSIS; RNA, RIBOSOMAL, 26S;

ARABIDOPSIS; ARTICLE; BINDING SITE; DNA SEQUENCE; GENE EXPRESSION; GENE INACTIVATION; GENETICS; GERMINATION; METABOLISM; MITOCHONDRION; MUTATION; NUCLEOTIDE SEQUENCE; PLANT SEED; RNA PROCESSING; RNA STABILITY; SEQUENCE ALIGNMENT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASE SEQUENCE; BINDING SITES; CONSERVED SEQUENCE; GENE EXPRESSION; GENE KNOCKOUT TECHNIQUES; GERMINATION; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MUTATION; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA STABILITY; RNA, MESSENGER; RNA, PLANT; RNA, RIBOSOMAL; RNA-BINDING PROTEINS; SEEDS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA;

ARABIDOPSIS THALIANA;

EID: 84877715374     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12143     Document Type: Article

References (52)

1. Alonso, J.M., Stepanova, A.N., Leisse, T.J., et al,. (2003) Genome-wide insertional mutagenesis of A. thaliana. Science 301, 653-657.
2. 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.
3. Bentolila, S., Alfonso, A.A., and, Hanson, M.R., (2002) A pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants. Proc. Natl Acad. Sci. USA 99, 10887-10892.
4. Binder, S., and, Brennicke, A., (1993) Transcription initiation sites in mitochondria of Oenothera berteriana. J. Biol. Chem. 268, 7849-7855.
5. Brown, G.G., Formanova, N., Jin, H., Wargachuk, R., Dendy, C., Patil, P., Laforest, M., Zhang, J., Cheung, W.Y., and, Landry, B.S., (2003) The radish Rfo restorer gene of Ogura cytoplasmic male sterility encodes a protein with multiple pentatricopeptide repeats. Plant J. 35, 262-272.
6. Budar, F., and, Pelletier, G., (2001) Male sterility in plants: occurrence, determinism, significance and use. C. R. Acad. Sci. III 324, 543-550.
7. Chang, S., Yang, T., Du, T., Huang, Y., Chen, J., Yan, J., He, J., and, Guan, R., (2011) Mitochondrial genome sequencing helps show the evolutionary mechanism of mitochondrial genome formation in Brassica. BMC genomics 12, 497.
8. Chase, C.D., (2007) Cytoplasmic male sterility: a window to the world of plant mitochondrial-nuclear interactions. Trends Genet. 23, 81-90.
9. Clough, S.J., and, Bent, A.F., (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of A. thaliana. Plant J. 16, 735-742.
10. Curtis, M.D., and, Grossniklaus, U., (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133, 462-469.
11. Czechowski, T., Stitt, M., Altmann, T., Udvardi, M.K., and, Scheible, W.R., (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 139, 5-17.
12. Delannoy, E., Stanley, W.A., Bond, C.S., and, Small, I.D., (2007) Pentatricopeptide repeat (PPR) proteins as sequence-specificity factors in post-transcriptional processes in organelles. Biochem. Soc. Trans. 35, 1643-1647.
13. Deng, Z., Zhang, X., Tang, W., et al,. (2007) A proteomics study of brassinosteroid response in Arabidopsis. Mol. Cell. Proteomics 6, 2058-2071.
14. Desloire, S., Gherbi, H., Laloui, W., et al,. (2003) Identification of the fertility restoration locus, Rfo, in radish, as a member of the pentatricopeptide-repeat protein family. EMBO Rep. 4, 588-594.
15. Dez, C., Houseley, J., and, Tollervey, D., (2006) Surveillance of nuclear-restricted pre-ribosomes within a subnucleolar region of Saccharomyces cerevisiae. EMBO J. 25, 1534-1546.
16. Forner, J., Weber, B., Thuss, S., Wildum, S., and, Binder, S., (2007) Mapping of mitochondrial mRNA termini in A. thaliana: t-elements contribute to 5′ and 3′ end formation. Nucleic Acids Res. 35, 3676-3692.
17. Francs-Small, C.C., Kroeger, T., Zmudjak, M., Ostersetzer-Biran, O., Rahimi, N., Small, I., and, Barkan, A., (2012) A PORR domain protein required for rpl2 and ccmF(C) intron splicing and for the biogenesis of c-type cytochromes in Arabidopsis mitochondria. Plant J. 69, 996-1005.
18. Fujii, S., and, Toriyama, K., (2008) Genome barriers between nuclei and mitochondria exemplified by cytoplasmic male sterility. Plant Cell Physiol. 49, 1484-1494.
19. Fujii, S., Bond, C.S., and, Small, I.D., (2011) Selection patterns on restorer-like genes reveal a conflict between nuclear and mitochondrial genomes throughout angiosperm evolution. Proc. Natl Acad. Sci. USA 108, 1723-1728.
20. Gagliardi, D., and, Leaver, C.J., (1999) Polyadenylation accelerates the degradation of the mitochondrial mRNA associated with cytoplasmic male sterility in sunflower. EMBO J. 18, 3757-3766.
21. Gutgsell, N.S., and, Jain, C., (2010) Coordinated regulation of 23S rRNA maturation in Escherichia coli. J. Bacteriol. 192, 1405-1409.
22. Henras, A.K., Soudet, J., Gerus, M., Lebaron, S., Caizergues-Ferrer, M., Mougin, A., and, Henry, Y., (2008) The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell. Mol. Life Sci. 65, 2334-2359.
23. Hölzle, A., Jonietz, C., Törjek, O., Altmann, T., Binder, S., and, Forner, J., (2011) A RESTORER OF FERTILITY-like PPR gene is required for 5′-end processing of the nad4 mRNA in mitochondria of A. thaliana. Plant J. 65, 737-744.
24. Hu, J., Wang, K., Huang, W., et al,. (2012) The rice pentatricopeptide repeat protein RF5 restores fertility in Hong-Lian cytoplasmic male-sterile lines via a complex with the glycine-rich protein GRP162. Plant Cell 24, 109-122.
25. 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.
26. Jonietz, C., Forner, J., Hölzle, A., Thuss, S., and, Binder, S., (2010) RNA PROCESSING FACTOR2 Is Required for 5 ′ End Processing of nad9 and cox3 mRNAs in Mitochondria of A. thaliana. Plant Cell 22, 443-453.
27. Jonietz, C., Forner, J., Hildebrandt, T., and, Binder, S., (2011) RNA PROCESSINGFACTOR 3 is crucial for the accumulation of mature ccmC transcripts in mitochondria of A. thaliana accession Columbia. Plant Physiol. 157, 1430-1439.
28. Kazama, T., and, Toriyama, K., (2003) A pentatricopeptide repeat-containing gene that promotes the processing of aberrant atp6 RNA of cytoplasmic male-sterile rice. FEBS Lett. 544, 99-102.
29. Kazama, T., Nakamura, T., Watanabe, M., Sugita, M., and, Toriyama, K., (2008) Suppression mechanism of mitochondrial ORF79 accumulation by Rf1 protein in BT-type cytoplasmic male sterile rice. Plant J. 55, 619-628.
30. Köhler, D., Schmidt-Gattung, S., and, Binder, S., (2010) The DEAD-box protein PMH2 is required for efficient group II intro splicing in mitochondria of A. thaliana. Plant Mol. Biol. 72, 459-467.
31. Koizuka, N., Imai, R., Fujimoto, H., Hayakawa, T., Kimura, Y., Kohno-Murase, J., Sakai, T., Kawasaki, S., and, Imamura, J., (2003) Genetic characterization of a pentatricopeptide repeat protein gene, orf687, that restores fertility in the cytoplasmic male-sterile Kosena radish. Plant J. 34, 407-415.
32. Koprivova, A., Colas des Francs-Small, C., Calder, G., Mugford, S.T., Tanz, S., Lee, B.-R., Zechmann, B., Small, I., and, Kopriva, S., (2010) Identification of a pentatricopeptide repeat protein implicated in splicing of intron 1 of mitochondrial nad7 transcripts. J. Biol. Chem. 285, 32192-32199.
33. Kuhn, J., Tengler, U., and, Binder, S., (2001) Transcript lifetime is balanced between stabilizing stem-loop structures and degradation-promoting polyadenylation in plant mitochondria. Mol. Cell. Biol. 21, 731-742.
34. Kühn, K., Weihe, A., and, Börner, T., (2005) Multiple promoters are a common feature of mitochondrial genes in Arabidopsis. Nucleic Acids Res. 33, 337-346.
35. Kühn, K., Richter, U., Meyer, E.H., Delannoy, E., Falcon de Longevialle, A., O'Toole, N., Börner, T., Millar, A.H., Small, I.D., and, Whelan, J., (2009) Phage-type RNA polymerase RPOTmp performs gene-specific transcription in mitochondria of A. thaliana. Plant Cell 21, 2762-2779.
36. 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.
37. 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.
38. Manavski, N., Guyon, V., Meurer, J., Wienand, U., and, Brettschneider, R., (2012) An essential pentatricopeptide repeat protein facilitates 5′ maturation and translation initiation of rps3 mRNA in maize mitochondria. Plant Cell 24, 3087-3105.
39. Marker, C., Zemann, A., Terhorst, T., Kiefmann, M., Kastenmayer, J.P., Green, P., Bachellerie, J.P., Brosius, J., and, Huttenhofer, A., (2002) Experimental RNomics: identification of 140 candidates for small non-messenger RNAs in the plant A. thaliana. Curr. Biol. 12, 2002-2013.
40. Matthes, A., Schmidt-Gattung, S., Köhler, D., Forner, J., Wildum, S., Raabe, M., Urlaub, H., and, Binder, S., (2007) Two DEAD-box proteins may be part of RNA-dependent high-molecular-mass protein complexes in Arabidopsis mitochondria. Plant Physiol. 145, 1637-1646.
41. McGinnis, S., and, Madden, T.L., (2004) BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucleic Acids Res. 32, W20-W25.
42. Meyer, E.H., Tomaz, T., Carroll, A.J., Estavillo, G., Delannoy, E., Tanz, S.K., Small, I.D., Pogson, B.J., and, Millar, A.H., (2009) Remodeled respiration in ndufs4 with low phosphorylation efficiency suppresses Arabidopsis germination and growth and alters control of metabolism at night. Plant Physiol. 151, 603-619.
43. 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.
44. Rene, O., and, Alix, J.H., (2011) Late steps of ribosome assembly in E. coli are sensitive to a severe heat stress but are assisted by the HSP70 chaperone machine. Nucleic Acids Res. 39, 1855-1867.
45. Roy-Chaudhuri, B., Kirthi, N., and, Culver, G.M., (2010) Appropriate maturation and folding of 16S rRNA during 30S subunit biogenesis are critical for translational fidelity. Proc. Natl Acad. Sci. USA 107, 4567-4572.
46. Sambrook, J., and, Russel, D.W., (2001) Molecular Cloning: A Laboratory Manual, Ed Ed 3. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
47. Schmitz-Linneweber, C., and, Small, I., (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci. 13, 663-670.
48. Schuster, J., Knill, T., Reichelt, H., Gershenzon, J., and, Binder, S., (2006) BRANCHED-CHAIN AMINOTRANSFERASE 4 is part of the chain elongation pathway in the biosynthesis of methionine-derived glucosinolates in Arabidopsis. Plant Cell 18, 1-16.
49. Sirdeshmukh, R., and, Schlessinger, D., (1985) Why is processing of 23 S ribosomal RNA in Escherichia coli not obligate for its function? J. Mol. Biol. 186, 669-672.
50. Small, I.D., and, Peeters, N., (2000) The PPR motif-a TPR-related motif prevalent in plant organellar proteins. Trends Biochem. Sci. 25, 46-47.
51. Wang, Z., Zou, Y., Li, X., et al,. (2006) Cytoplasmic male sterility of rice with boro II cytoplasm is caused by a cytotoxic peptide and is restored by two related PPR motif genes via distinct modes of mRNA silencing. Plant Cell 18, 676-687.
52. Wittig, I., Braun, H.P., and, Schagger, H., (2006) Blue native PAGE. Nat. Protoc. 1, 418-428.