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 Journal

Volumn 58, Issue 1, 2009, Pages 82-96

  Zhou, Wenbin ^a   Cheng, Yuxiang ^a   Yap, Aaron ^b   Chateigner Boutin, Anne Laure ^b   Delannoy, Etienne ^b   Hammani, Kamel ^b   Small, Ian ^b   Huang, Jirong ^a  

^a INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Arabidopsis; Chloroplast development; Pentatricopeptide repeat protein; Plastid gene expression; RNA polymerase

Indexed keywords

AMINOLEVULINIC ACID; ARABIDOPSIS PROTEIN; CHLOROPHYLL; CHLOROPLAST PROTEIN; CHLOROPLAST RNA; PEPPER PROTEIN, ARABIDOPSIS; PLANT RNA; RNA BINDING PROTEIN;

ALLELE; ARABIDOPSIS; ARTICLE; CHLOROPLAST; DARKNESS; ENZYME ACTIVATION; FLUORESCENCE; GENE INACTIVATION; GENETIC COMPLEMENTATION; GENETICS; GERMINATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; OXIDATION REDUCTION REACTION; PHOTOSYNTHESIS; PLANT LEAF; PLASMID; PROTEIN MOTIF; RNA EDITING; THYLAKOID; TIME; TRANSGENIC PLANT; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ALLELES; AMINO ACID MOTIFS; AMINOLEVULINIC ACID; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHLOROPHYLL; CHLOROPLAST PROTEINS; CHLOROPLASTS; DARKNESS; ENZYME ACTIVATION; FLUORESCENCE; GENE KNOCKOUT TECHNIQUES; GENETIC COMPLEMENTATION TEST; GERMINATION; MICROSCOPY, ELECTRON, TRANSMISSION; MUTATION; OXIDATION-REDUCTION; PHOTOSYNTHESIS; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; PLASMIDS; RNA EDITING; RNA, CHLOROPLAST; RNA, PLANT; RNA-BINDING PROTEINS; THYLAKOIDS; TIME FACTORS;

ARABIDOPSIS;

EID: 63349084758     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2008.03766.x     Document Type: Article

References (68)

1. Allison, L.A. (2000) The role of sigma factors in plastid transcription. Biochimie, 82, 537 548.
2. Allison, L.A., Simon, L.D. Maliga, P. (1996) Deletion of rpoB reveals a second distinct transcription system in plastids of higher plants. EMBO J. 15, 2802 2809.
3. Alonso, J.M., Stepanova, A.N., Leisse, T.J. et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science, 301, 653 657.
4. Archer, E.K. Bonnett, H.T. (1987) Characterization of a virescent chloroplast mutant of tobacco. Plant Physiol. 83, 920 925.
5. Aubourg, S., Boudet, N., Kreis, M. Lecharny, A. (2000) In Arabidopsis thaliana, 1% of the genome codes for a novel protein family unique to plants. Plant Mol. Biol. 42, 603 613.
6. Barkan, A. (1993) Nuclear mutants of maize with defects in chloroplast polysome assembly have altered chloroplast RNA metabolism. Plant Cell, 5, 389 402.
7. Barkan, A. Goldschmidt-Clermont, M. (2000) Participation of nuclear genes in chloroplast gene expression. Biochimie, 82, 559 572.
8. 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.
9. Benedict, C.R. Ketring, D.L. (1972) Nuclear gene affecting greening in virescent peanut leaves. Plant Physiol. 49, 972 976.
10. Bentolila, S., Chateigner-Boutin, A.L. Hanson, M.R. (2005) Ecotype allelic variation in C-to-U editing extent of a mitochondrial transcript identifies RNA-editing quantitative trait loci in Arabidopsis. Plant Physiol. 139, 2006 2016.
11. Chateigner-Boutin, A.L. Small, I. (2007) A rapid high-throughput method for the detection and quantification of RNA editing based on high-resolution melting of amplicons. Nucleic Acids Res. 35, e114.
12. Chateigner-Boutin, A.L., Ramos-Vega, M., Guevara-Garcia, A. et al. (2008) CLB19, a pentatricopeptide repeat protein required for editing of rpoA and clpP chloroplast transcripts. Plant J. 56, 590 602.
13. Chaudhuri, S., Carrer, H. Maliga, P. (1995) Site-specific factor involved in the editing of the psbL mRNA in tobacco plastids. EMBO J. 14, 2951 2957.
14. Cline, K. Mori, H. (2001) Thylakoid delta pH-dependent precursor proteins bind to a cpTatC-Hcf106 complex before Tha4-dependent transport. J. Cell Biol. 154, 719 730.
15. Clough, S.J. Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735 743.
16. da Costa e Silva, O., Lorbiecke, R., Garg, P. et al. (2004) The Etched1 gene of Zea mays (L.) encodes a zinc ribbon protein that belongs to the transcriptionally active chromosome (TAC) of plastids and is similar to the transcription factor TFIIS. Plant J. 38, 923 939.
17. De Santis-MacIossek, G., Kofer, W., Bock, A., Schoch, S., Maier, R.M., Wanner, G., Rudiger, W., Koop, H.U. Herrmann, R.G. (1999) Targeted disruption of the plastid RNA polymerase genes rpoA, B and C1: molecular biology, biochemistry and ultrastructure. Plant J. 18, 477 489.
18. Delannoy, E., Stanley, W.A., Bond, C.S. Small, I.D. (2007) Pentatricopeptide repeat (PPR) proteins as sequence-specificity factors in post-transcriptional processes in organelles. Biochem. Soc. Trans. 35, 1643 1647.
19. Demarsy, E., Courtois, F., Azevedo, J., Buhot, L. Lerbs-Mache, S. (2006) Building up of the plastid transcriptional machinery during germination and early plant development. Plant Physiol. 142, 993 1003.
20. Dhingra, A. Daniell, H. (2006) Chloroplast genetic engineering via organogenesis or somatic embryogenesis. Methods Mol. Biol. 323, 245 262.
21. Dyall, S.D., Brown, M.T. Johnson, P.J. (2004) Ancient invasions: from endosymbionts to organelles. Science, 304, 253 257.
22. Emanuelsson, O., Nielsen, H. von Heijne, G. (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci. 8, 978 984.
23. Falcon de Longevialle, A.F., Meyer, E.H., Andrés, C., Taylor, N.L., Lurin, C., Millar, A.H. Small, I.D. (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.
24. Falcon de Longevialle, A., Hendrickson, L., Taylor, N.L., Delannoy, E., Lurin, C., Badger, M., Millar, A.H. 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.
25. Hajdukiewicz, P.T., Allison, L.A. Maliga, P. (1997) The two RNA polymerases encoded by the nuclear and the plastid compartments transcribe distinct groups of genes in tobacco plastids. EMBO J. 16, 4041 4048.
26. Hanaoka, M., Kanamaru, K., Fujiwara, M., Takahashi, H. Tanaka, K. (2005) Glutamyl-tRNA mediates a switch in RNA polymerase use during chloroplast biogenesis. EMBO Rep. 6, 545 550.
27. 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.
28. Hedtke, B., Börner, T. Weihe, A. (1997) Mitochondrial and chloroplast phage type RNA polymerases in Arabidopsis. Science, 277, 809 811.
29. Hess, W.R. Börner, T. (1999) Organellar RNA polymerases of higher plants. Int. Rev. Cytol. 190, 1 59.
30. Hricová, A., Quesada, V. Micol, J.L. (2006) The SCABRA3 nuclear gene encodes the plastid RpoTp RNA polymerase, which is required for chloroplast biogenesis and mesophyll cell proliferation in Arabidopsis. Plant Physiol. 141, 942 956.
31. Huang, J., Takano, T. Akita, S. (2000) Expression of α-expansin genes in young seedlings of rice (oryza sativa L.). Planta, 211, 467 473.
32. Ichikawa, T., Nakazawa, M., Kawashima, M. et al. (2003) Sequence database of 1172 T-DNA insertion sites in Arabidopsis activation-tagging lines that showed phenotypes in T1 generation. Plant J. 36, 421 429.
33. Ikeda, T.M. Gray, M.W. (1999) Characterization of a DNA-binding protein implicated in transcription in wheat mitochondria. Mol. Cell. Biol. 19, 8113 8122.
34. Ishizaki, Y., Tsunoyama, Y., Hatano, K., Ando, K., Kato, K., Shinmyo, A., Kobori, M., Takeba, G., Nakahira, Y. Shiina, T. (2005) A nuclear-encoded sigma factor, Arabidopsis SIG6, recognizes sigma-70 type chloroplast promoters and regulates early chloroplast development in cotyledons. Plant J. 42, 133 144.
35. Kanamaru, K., Nagashima, A., Fujiwara, M., Shimada, H., Shirano, Y., Nakabayashi, K., Shibata, D., Tanaka, K. Takahashi, H. (2001) An Arabidopsis sigma factor (SIG2)-dependent expression of plastid-encoded tRNAs in chloroplasts. Plant Cell Physiol. 42, 1034 1043.
36. Kasai, K., Kawagishi-Kobayashi, M., Teraishi, M., Ito, Y., Ochi, K., Wakasa, K. Tozawa, Y. (2004) Differential expression of three plastidial sigma factors, OsSIG1, OsSIG2A, and OsSIG2B, during leaf development in rice. Biosci. Biotechnol. Biochem. 68, 973 977.
37. Kleffmann, T., von Zychlinski, A., Russenberger, D., Hirsch-Hoffmann, M., Gehrig, P., Gruissem, W. Baginsky, S. (2007) Proteome dynamics during plastid differentiation in rice. Plant Physiol. 143, 912 923.
38. Kotera, E., Tasaka, M. Shikanai, T. (2005) A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts. Nature, 433, 326 330.
39. Koussevitzky, S., Stanne, T.M., Peto, C.A., Giap, T., Sjögren, L.L., Zhao, Y., Clarke, A.K. Chory, J. (2007) An Arabidopsis thaliana virescent mutant reveals a role for ClpR1 in plastid development. Plant Mol. Biol. 63, 85 96.
40. Kruse, E., Grimm, B., Beator, J. Kloppstech, K. (1997) Developmental and circadian control of the capacity for δ-aminolevulinic acid synthesis in green barley. Planta, 202, 235 241.
41. Kusumi, K., Mizutani, A., Nishimura, M. Iba, K. (1997) A virescent gene V1 determines the expression timing of plastid genes for transcription/ translation apparatus during early leaf development in rice. Plant J. 12, 1241 1250.
42. Lichtenthaler, H.K. (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol. 148, 350 382.
43. Liere, K. Maliga, P. (1999) In vitro characterization of the tobacco rpoB promoter reveals a core sequence motif conserved between phage-type plastid and plant mitochondrial promoters. EMBO J. 18, 249 257.
44. Loschelder, H., Schweer, J., Link, B. Link, G. (2006) Dual temporal role of plastid sigma factor 6 in Arabidopsis development. Plant Physiol. 142, 642 650.
45. Lurin, C., Andrés, 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.
46. 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.
47. Meurer, J., Berger, A. Westhoff, P. (1996a) A nuclear mutant of Arabidopsis with impaired stability on distinct transcripts of the plastid psbB, psbD/C, ndhH, and ndhC operons. Plant Cell, 8, 1193 1207.
48. Meurer, J., Meierhoff, K. Westhoff, P. (1996b) Isolation of high chlorophyll-fluorescence mutants of Arabidopsis thaliana and their characterisation by spectroscopy, immunoblotting and northern hybridisation. Planta, 198, 385 396.
49. Mullet, J.E. (1988) Chloroplast development and gene expression. Annu. Rev. Plant Physiol. Plant Mol. Biol. 39, 475 502.
50. 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.
51. 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.
52. Pfalz, J., Liere, K., Kandlbinder, A., Dietz, K.J. Oelmüller, 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.
53. Porra, R.J., Thompson, W.A. Kriedemann, P.E. (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectrometry. Biochim. Biophys. Acta 975, 384 394.
54. Rhyne, C.L. (1955) The inheritance of Yellow-Green, a possible mutation in cotton. Genetics, 40, 235 245.
55. Rivals, E., Bruyère, C., Toffano-Nioche, C. Lecharny, A. (2006) Formation of the Arabidopsis pentatricopeptide repeat family. Plant Physiol. 141, 825 839.
56. Salone, V., Rüdinger, M., Polsakiewicz, M., Hoffmann, B., Groth-Malonek, M., Szurek, B., Small, I., Knoop, V. Lurin, C. (2007) A hypothesis on the identification of the editing enzyme in plant organelles. FEBS Lett. 581, 4132 4138.
57. Sato, S., Nakamura, Y., Kaneko, T., Asamizu, E. Tabata, S. (1999) Complete structure of the chloroplast genome of Arabidopsis thaliana. DNA Res. 6, 283 290.
58. Schägger, H., Cramer, W.A. von Jagow, G. (1994) Analysis of molecular masses and oligomeric states of protein complexes by blue native electrophoresis and isolation of membrane protein complexes by two-dimensional native electrophoresis. Anal. Biochem. 217, 220 230.
59. 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.
60. Schmitz-Linneweber, C., Williams-Carrier, R.E., Williams-Voelker, P.M., Kroeger, T.S., 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.
61. Schweer, J., Loschelder, H. Link, G. (2006) A promoter switch that can rescue a plant sigma factor mutant. FEBS Lett. 580, 6617 6622.
62. Severinov, K., Soushko, M., Goldfarb, A. Nikiforov, V. (1993) Rifampicin region revisited. New rifampicin-resistant and streptolydigin-resistant mutants in the beta subunit of Escherichia coli RNA polymerase. J. Biol. Chem. 268, 14820 14825.
63. Small, I.D. Peeters, N. (2000) The PPR motif - A TPR-related motif prevalent in plant organellar proteins. Trends Biochem. Sci. 25, 46 47.
64. Sugimoto, H., Kusumi, K., Noguchi, K., Yano, M., Yoshimura, A. Iba, K. (2007) The rice nuclear gene, VIRESCENT 2, is essential for chloroplast development and encodes a novel type of guanylate kinase targeted to plastids and mitochondria. Plant J. 52, 512 527.
65. Swiatecka-Hagenbruch, M., Emanuel, C., Hedtke, B., Liere, K. Börner, T. (2008) Impaired function of the phage-type RNA polymerase RpoTp in transcription of chloroplast genes is compensated by a second phage-type RNA polymerase. Nucleic Acids Res. 36, 785 792.
66. Swiatek, M., Regel, R.E., Meurer, J., Wanner, G., Pakarasi, H.B., Ohad, I. Herrmann, R.G. (2003) Effects of selective inactivation of individual genes for low-molecular-mass subunits on the assembly of photosystem II, as revealed by chloroplast transformation: the psbEFLJ operon in Nicotiana tabacum. Mol. Genet. Genomics, 268, 699 710.
67. Tanaka, R. Tanaka, A. (2007) Tetrapyrrole biosynthesis in higher plants. Annu. Rev. Plant Biol. 58, 321 346.
68. 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.