A pentatricopeptide repeat gene of rice is required for splicing of chloroplast transcripts and RNA editing of ndhA

Plant Biotechnology

Volumn 30, Issue 1, 2013, Pages 57-64

  Asano, Takayuki ^a   Miyao, Akio ^a   Hirochika, Hirohiko ^a   Kikuchi, Shoshi ^a   Kadowaki, Koh ichi ^a,b  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b NATIONAL INSTITUTE OF CROP SCIENCE   (Japan)

Author keywords

Albino; Chloroplast; Pentatricopeptide repeat; Rice; RNA editing; Splicing

Indexed keywords

EID: 84878060363     PISSN: 13424580     EISSN: 13476114     Source Type: Journal    
DOI: 10.5511/plantbiotechnology.12.1217a     Document Type: Article

References (59)

1. Adams M. D, Rudner DZ, Rio DC (1996) Biochemistry and regulation of pre-mRNA splicing. Curr Opin Cell Biol 8: 331-339
2. Asakura Y., Barkan A (2007) A CRM domain protein functions dually in group I and group II intron splicing in land plant chloroplasts. Plant Cell 19: 3864-3875
3. Asakura Y., Bayraktar OA, Barkan A (2008) Two CRM protein subfamilies cooperate in the splicing of group IIB introns in chloroplasts. RNA 14: 2319-2332
4. Asano T., Hakata M, Nakamura H, Aoki N, Komatsu S, Ichikawa H, Hirochika H, Ohsugi R (2011) Functional characterisation of OsCPK21, a calcium-dependent protein kinase that confers salt tolerance in rice. Plant Mol Biol 75: 179-191
5. Beick S., Schmitz-Linneweber C, Williams-Carrier R, Jensen B, Barkan A. (2008) The pentatricopeptide repeat protein PPR5 stabilizes a specific tRNA precursor in maize chloroplasts. Mol Cell Biol 28: 5337-5347
6. Bonen L., Vogel J (2001) The ins and outs of group II introns. Trends Genet 17: 322-331
7. Cai W., Ji D, Peng L, Guo J, Ma J, Zou M, Lu C, Zhang L (2009) LPA66 is required for editing psbF chloroplast transcripts in Arabidopsis. Plant Physiol 150: 1260-1271
8. Chateigner-Boutin AL, des Francs-Small CC, Delannoy E, Kahlau S, Tanz SK, de Longevialle AF, Fujii S, Small I (2011) OTP70 is a pentatricopeptide repeat protein of the E subgroup involved in splicing of the plastid transcript rpoC1. Plant J 65: 532-542
9. Chateigner-Boutin AL, Ramos-Vega M, Guevara-García A, Andrés C, de la Luz Gutiérrez-Nava M, Cantero A, Delannoy E, Jiménez LF, Lurin C, Small I, León P (2008) CLB19, a pentatricopeptide repeat protein required for editing of rpoA and clpP chloroplast transcripts. Plant J 56: 590-602
10. Del Campo EM, Sabater B, Martín M (2000) Transcripts of the ndhH-D operon of barley plastids: possible role of unedited site III in splicing of the ndhA intron. Nucleic Acids Res 28: 1092-1098
11. de Longevialle AF, Meyer EH, Andrés C, Taylor NL, Lurin C, Millar AH, Small ID (2007) The pentatricopeptide repeat gene OTP43 is required for trans-splicing of the mitochondrial nad1 Intron 1 in Arabidopsis thaliana. Plant Cell 19: 3256-3265
12. de Longevialle AF, Hendrickson L, Taylor NL, Delannoy E, Lurin C, Badger M, Millar AH, 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
13. de Longevialle AF, Small ID, Lurin C (2010) Nuclearly encoded splicing factors implicated in RNA splicing in higher plant organelles. Mol Plant 3: 691-705
14. Emanuelsson O., Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300: 1005-1016
15. Fujii S., Small I (2011) The evolution of RNA editing and pentatricopeptide repeat genes. New Phytol 191: 37-47
16. Goff S. A, Ricke D, Lan TH, Presting G, Wang R, Dunn M, Glazebrook J., Sessions A, Oeller P, Varma H, et al. (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296: 92-100
17. Hammani K., Okuda K, Tanz SK, Chateigner-Boutin AL, Shikanai T, 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
18. Hattori M., Miyake H, 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
19. Hood E. E, Gelvin SB, Melchers LS, Hoekema A (1993) New Agrobacterium helper plasmids for gene transfer to plants. Transgenic Res 2: 208-218
20. Ichinose M., Tasaki E, Sugita C, Sugita M (2012) A PPR-DYW protein is required for splicing of a group II intron of cox1 premRNA in Physcomitrella patens. Plant J 70: 271-278
21. Kazama T., Nakamura T, Watanabe M, Sugita M, Toriyama K (2008) Suppression mechanism of mitochondrial ORF79 accumulation by Rf1 protein in BT-type cytoplasmic male sterile rice. Plant J 55: 619-628
22. Kazama T., Toriyama K (2003) A pentatricopeptide repeatcontaining gene that promotes the processing of aberrant atp6 RNA of cytoplasmic male-sterile rice. FEBS Lett 544: 99-102
23. Kim S. R, Yang JI, Moon S, Ryu CH, An K, Kim KM, Yim J, An G (2009) Rice OGR1 encodes a pentatricopeptide repeat-DYW protein and is essential for RNA editing in mitochondria. Plant J 59: 738-749
24. Komori T., Ohta S, Murai N, Takakura Y, Kuraya Y, Suzuki S, Hiei Y, Imaseki H, Nitta N (2004) Map-based cloning of a fertility restorer gene, Rf-1, in rice (Oryza sativa L.). Plant J 37: 315-325
25. Kotera E., Tasaka M, Shikanai T (2005) A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts. Nature 433: 326-330
26. Lurin C., Andrés C, Aubourg S, Bellaoui M, Bitton F, Bruyère C, Caboche M., Debast C, Gualberto J, Hoffmann B, Lecharny A, Le Ret M, Martin-Magniette ML, Mireau H, Peeters N, Renou JP, Szurek B, Taconnat L, Small I (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16: 2089-2103
27. Meierhoff K., Felder S, Nakamura T, Bechtold N, 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
28. Miki D., Itoh R, Shimamoto K (2005) RNA silencing of single and multiple members in a gene family of rice. Plant Physiol 138: 1903-1913
29. Miyao A., Tanaka K, Murata K, Sawaki H, Takeda S, Abe K, Shinozuka Y., Onosato K, Hirochika H (2003) Target site specificity of the Tos17 retrotransposon shows a preference for insertion within genes and against insertion in retrotransposonrich regions of the genome. Plant Cell 15: 1771-1780
30. O'Toole N, Hattori M, Andres C, Iida K, Lurin C, Schmitz-Linneweber C., Sugita M, Small I (2008) On the expansion of the pentatricopeptide repeat gene family in plants. Mol Biol Evol 25: 1120-1128
31. Okuda K., Chateigner-Boutin AL, Nakamura T, Delannoy E, Sugita M, Myouga F, Motohashi R, Shinozaki K, Small I, Shikanai T (2009) Pentatricopeptide repeat proteins with the DYW motif have distinct molecular functions in RNA editing and RNA cleavage in Arabidopsis chloroplasts. Plant Cell 21: 146-156
32. Okuda K., Hammani K, Tanz SK, Peng L, Fukao Y, Myouga F, Motohashi R., Shinozaki K, Small I, Shikanai T (2010) The pentatricopeptide repeat protein OTP82 is required for RNA editing of plastid ndhB and ndhG transcripts. Plant J 61: 339-349
33. Okuda K., Myouga F, Motohashi R, Shinozaki K, Shikanai T (2007) Conserved domain structure of pentatricopeptide repeat proteins involved in chloroplast RNA editing. Proc Natl Acad Sci USA 104: 8178-8183
34. Ostheimer G. J, Williams-Carrier R, Belcher S, Osborne E, Gierke J, Barkan A (2003) Group II intron splicing factors derived by diversification of an ancient RNA-binding domain. EMBO J 22: 3919-3929
35. Ozawa K. (2009) Establishment of a high efficiency Agrobacteriummediated transformation system of rice (Oryza sativa L.). Plant Sci 176: 522-527
36. Reddy A. S (2007) Alternative splicing of pre-messenger RNAs in plants in the genomic era. Annu Rev Plant Biol 58: 267-294
37. Robbins J. C, Heller WP, Hanson MR (2009) A comparative genomics approach identifies a PPR-DYW protein that is essential for C-to-U editing of the Arabidopsis chloroplast accD transcript. RNA 15: 1142-1153
38. Rüdinger M., Szövényi P, Rensing SA, Knoop V (2011) Assigning DYW-type PPR proteins to RNA editing sites in the funariid mosses Physcomitrella patens and Funaria hygrometrica. Plant J 67: 370-380
39. Rüdinger M., Volkmar U, Lenz H, Groth-Malonek M, Knoop V (2012) Nuclear DYW-type PPR gene families diversify with increasing RNA editing frequencies in liverwort and moss mitochondria. J Mol Evol 74: 37-51
40. Schmitz-Linneweber C, Williams-Carrier R, 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
41. Schmitz-Linneweber C, Williams-Carrier RE, Williams-Voelker PM, Kroeger TS, Vichas A, Barkan A (2006) A pentatricopeptide repeat protein facilitates the trans-splicing of the maize chloroplast rps12 pre-mRNA. Plant Cell 18: 2650-2663
42. Schmitz-Linneweber C, Small I (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci 13: 663-670
43. Smith C. W, Valcárcel J (2000) Alternative pre-mRNA splicing: the logic of combinatorial control. Trends Biochem Sci 25: 381-388
44. Sosso D., Mbelo S, Vernoud V, Gendrot G, Dedieu A, Chambrier P, Dauzat M, Heurtevin L, Guyon V, Takenaka M, et al. (2012) PPR2263, a DYW-Subgroup Pentatricopeptide repeat protein, is required for mitochondrial nad5 and cob transcript editing, mitochondrion biogenesis, and maize growth. Plant Cell 24: 676-691
45. Takenaka M. (2010) MEF9, an E-subclass pentatricopeptide repeat protein, is required for an RNA editing event in the nad7 transcript in mitochondria of Arabidopsis. Plant Physiol 152: 939-947
46. Takenaka M., Verbitskiy D, Zehrmann A, Brennicke A (2010) Reverse genetic screening identifies five E-class PPR proteins involved in RNA editing in mitochondria of Arabidopsis thaliana. J Biol Chem 285: 27122-27129
47. Tang J., Kobayashi K, Suzuki M, Matsumoto S, Muranaka T (2010) The mitochondrial PPR protein LOVASTATIN INSENSITIVE 1 plays regulatory roles in cytosolic and plastidial isoprenoid biosynthesis through RNA editing. Plant J 61: 456-466
48. Tasaki E., Hattori M, 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
49. Tavares-Carreón F, Camacho-Villasana Y, Zamudio-Ochoa A, Shingú-Vázquez M, Torres-Larios A, Pérez-Martínez X (2008) The pentatricopeptide repeats present in Pet309 are necessary for translation but not for stability of the mitochondrial COX1 mRNA in yeast. J Biol Chem 283: 1472-1479
50. The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796-815
51. Till B., Schmitz-Linneweber C, Williams-Carrier R, 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
52. Toda T., Fujii S, Noguchi K, Kazama T, Toriyama K (2012) Rice MPR25 encodes a pentatricopeptide repeat protein and is essential for RNA editing of nad5 transcripts in mitochondria. Plant J 72: 450-460
53. Verbitskiy D., Zehrmann A, Brennicke A, Takenaka M (2010a) A truncated MEF11 protein shows site-specific effects on mitochondrial RNA editing. Plant Signal Behav 5: 5
54. Verbitskiy D., Zehrmann A, van der Merwe JA, Brennicke A, Takenaka M (2010b) The PPR protein encoded by the LOVASTATIN INSENSITIVE 1 gene is involved in RNA editing at three sites in mitochondria of Arabidopsis thaliana. Plant J 61: 446-455
55. Wang Z., Zou Y, Li X, Zhang Q, Chen L, Wu H, Su D, Chen Y, Guo J, Luo D, Long Y, Zhong Y, Liu YG (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
56. Watkins K. P, Kroeger TS, Cooke AM, Williams-Carrier RE, Friso G, Belcher SE, van Wijk KJ, Barkan A (2007) A ribonuclease III domain protein functions in group II intron splicing in maize chloroplasts. Plant Cell 19: 2606-2623
57. Yu J., Hu S, Wang J, Wong GK, Li S, Liu B, Deng Y, Dai L, Zhou Y, Zhang X, et al. (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296: 79-92
58. Zehrmann A., Verbitskiy D, van der Merwe JA, Brennicke A, Takenaka M (2009) A DYW domain-containing pentatricopeptide repeat protein is required for RNA editing at multiple sites in mitochondria of Arabidopsis thaliana. Plant Cell 21: 558-567
59. Zhou W., Cheng Y, Yap A, Chateigner-Boutin AL, Delannoy E, Hammani K., Small I, Huang J (2009) The Arabidopsis gene YS1 encoding a DYW protein is required for editing of rpoB transcripts and the rapid development of chloroplasts during early growth. Plant J 58: 82-96