Sequence analysis of two alleles reveals that intra-and intergenic recombination played a role in the evolution of the radish fertility restorer (Rfo)

BMC Plant Biology

Volumn 10, Issue , 2010, Pages

  Hernandez Mora, José R ^a   Rivals, Eric ^b   Mireau, Hakim ^a   Budar, Françoise ^a  

^a INSTITUT JEAN PIERRE BOURGIN   (France)

^b LIRMM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

EMBRYOPHYTA; EUKARYOTA; RAPHANUS SATIVUS;

PLANT DNA; SPACER DNA;

ALLELE; AMINO ACID SEQUENCE; ARTICLE; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENETIC RECOMBINATION; GENETICS; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PHYLOGENY; PLANT GENE; PLANT INFERTILITY; RADISH; SEQUENCE ANALYSIS;

ALLELES; AMINO ACID SEQUENCE; DNA, INTERGENIC; DNA, PLANT; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT INFERTILITY; RAPHANUS; RECOMBINATION, GENETIC; SEQUENCE ANALYSIS; SEQUENCE ANALYSIS, DNA;

EID: 77950944724     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-10-35     Document Type: Article

References (70)

1. Aubourg S, Boudet N, Kreis M, Lecharny A. In Arabidopsis thaliana, 1% of the genome codes for a novel protein family unique to plants. Plant Mol Biol 2000, 42(4):603-13. 10.1023/A:1006352315928, 10809006.
2. Small I, Peeters N. The PPR motif: A TPR-related motif prevalent in plant organellar proteins. trends Biochem Sci 2000, 25:46-47. 10.1016/S0968-0004(99)01520-0, 10664580.
3. Lurin C, Andres C, Aubourg S, Bellaoui M, Bitton F, Bruyere 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. Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 2004, 16(8):2089-103. 10.1105/tpc.104.022236, 519200, 15269332.
4. O'Toole N, Hattori M, Andres C, Iida K, Lurin C, Schmitz-Linneweber C, Sugita M, Small I. On the expansion of the pentatricopeptide repeat gene family in plants. Mol Biol Evol 2008, 25(6):1120-8. 10.1093/molbev/msn057, 18343892.
5. Saha D, Prasad AM, Srinivasan R. Pentatricopeptide repeat proteins and their emerging roles in plants. Plant Physiol Biochem 2007, 45(8):521-34. 10.1016/j.plaphy.2007.03.026, 17560114.
6. Schmitz-Linneweber C, Small I. Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci 2008, 13(12):663-70. 10.1016/j.tplants.2008.10.001, 19004664.
7. Andres C, Lurin C, Small I. The multifarious roles of PPR proteins in plant mitochondrial gene expression. Physiologia plantarum 2007, 129:14-22.
8. Fisk DG, Walker MB, Barkan A. Molecular cloning of the maize gene crp1 reveals similarity between regulators of mitochondrial and chloroplast gene expression. Embo J 1999, 18(9):2621-30. 10.1093/emboj/18.9.2621, 1171341, 10228173.
9. Yamazaki H, Tasaka M, Shikanai T. PPR motifs of the nucleus-encoded factor, PGR3, function in the selective and distinct steps of chloroplast gene expression in Arabidopsis. Plant J 2004, 38(1):152-63. 10.1111/j.1365-313X.2004.02035.x, 15053768.
10. Uyttewaal M, Arnal N, Quadrado M, Martin-Canadell A, Vrielynck N, Hiard S, Gherbi H, Bendahmane A, Budar F, Mireau H. Characterization of Raphanus sativus Pentatricopeptide Repeat Proteins Encoded by the Fertility Restorer Locus for Ogura Cytoplasmic Male Sterility. Plant Cell 2008, 20(12):3331-45. 10.1105/tpc.107.057208, 2630448, 19098270.
11. Falcon de Longevialle A, Hendrickson L, Taylor NL, Delannoy E, Lurin C, Badger M, Millar AH, Small I. 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 2008, 56(1):157-68. 10.1111/j.1365-313X.2008.03581.x, 18557832.
12. Falcon de Longevialle A, Meyer EH, Andres C, Taylor NL, Lurin C, Millar AH, Small ID. The Pentatricopeptide Repeat Gene OTP43 Is Required for trans-Splicing of the Mitochondrial nad1 Intron 1 in Arabidopsis thaliana. Plant Cell 2007, 19(10):3256-3265. 10.1105/tpc.107.054841, 2174710, 17965268.
13. Meierhoff K, Felder S, Nakamura T, Bechtold N, Schuster G. HCF152, an Arabidopsis RNA binding pentatricopeptide repeat protein involved in the processing of chloroplast psbB-psbT-psbH-petB-petD RNAs. Plant Cell 2003, 15(6):1480-95. 10.1105/tpc.010397, 156381, 12782738.
14. Schmitz-Linneweber C, Williams-Carrier RE, Williams-Voelker PM, Kroeger TS, Vichas A, Barkan A. A Pentatricopeptide Repeat Protein Facilitates the trans-Splicing of the Maize Chloroplast rps12 Pre-mRNA. Plant Cell 2006, 18(10):2650-63. 10.1105/tpc.106.046110, 1626628, 17041147.
15. Beick S, Schmitz-Linneweber C, Williams-Carrier R, Jensen B, Barkan A. The pentatricopeptide repeat protein PPR5 stabilizes a specific tRNA precursor in maize chloroplasts. Mol Cell Biol 2008, 28(17):5337-47. 10.1128/MCB.00563-08, 2519714, 18591259.
16. Hashimoto M, Endo T, Peltier G, Tasaka M, Shikanai T. A nucleus-encoded factor, CRR2, is essential for the expression of chloroplast ndhB in Arabidopsis. Plant J 2003, 36(4):541-9. 10.1046/j.1365-313X.2003.01900.x, 14617084.
17. Hattori M, Miyake H, Sugita M. A Pentatricopeptide repeat protein is required for RNA processing of clpP Pre-mRNA in moss chloroplasts. J Biol Chem 2007, 282(14):10773-82. 10.1074/jbc.M608034200, 17283080.
18. Robbins JC, Heller WP, Hanson MR. A comparative genomics approach identifies a PPR-DYW protein that is essential for C-to-U editing of the Arabidopsis chloroplast accD transcript. RNA 2009, 15(6):1142-53. 10.1261/rna.1533909, 2685521, 19395655.
19. Kotera E, Tasaka M, Shikanai T. A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts. Nature 2005, 433(7023):326-30. 10.1038/nature03229, 15662426.
20. Okuda K, Myouga F, Motohashi R, Shinozaki K, Shikanai T. Conserved domain structure of pentatricopeptide repeat proteins involved in chloroplast RNA editing. Proc Natl Acad Sci USA 2007, 104(19):8178-83. 10.1073/pnas.0700865104, 1876591, 17483454.
21. Okuda K, Chateigner-Boutin AL, Nakamura T, Delannoy E, Sugita M, Myouga F, Motohashi R, Shinozaki K, Small I, Shikanai T. Pentatricopeptide Repeat Proteins with the DYW Motif Have Distinct Molecular Functions in RNA Editing and RNA Cleavage in Arabidopsis Chloroplasts. Plant Cell 2009, 21(1):146-56. 10.1105/tpc.108.064667, 2648089, 19182104.
22. Chateigner-Boutin AL, Ramos-Vega M, Guevara-Garcia A, Andres C, de la Luz Gutierrez-Nava M, Cantero A, Delannoy E, Jimenez LF, Lurin C, Small I, Leon P. CLB19, a pentatricopeptide repeat protein required for editing of rpoA and clpP chloroplast transcripts. Plant J 2008, 56(4):590-602. 10.1111/j.1365-313X.2008.03634.x, 18657233.
23. Zhou W, Cheng Y, Yap A, Chateigner-Boutin AL, Delannoy E, Hammani K, Small I, Huang J. 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 2008,
24. Zehrmann A, Verbitskiy D, Merwe JA, Brennicke A, Takenaka M. A DYW Domain-Containing Pentatricopeptide Repeat Protein Is Required for RNA Editing at Multiple Sites in Mitochondria of Arabidopsis thaliana. Plant Cell 2009, 21(2):558-67. 10.1105/tpc.108.064535, 2660620, 19252080.
25. Rivals E, Bruyere C, Toffano-Nioche C, Lecharny A. Formation of the Arabidopsis pentatricopeptide repeat family. Plant Physiol 2006, 141(3):825-39. 10.1104/pp.106.077826, 1489915, 16825340.
26. McCauley DE, Olson MS. Do Recent Findings in Plant Mitochondrial Molecular and Population Genetics Have Implications for the Study of Gynodioecy and Cyto-Nuclear Conflict?. Evolution Int J Org Evolution 2008, 62(5):1013-25.
27. Havey MJ. The use of cytoplasmic male sterility for hybrid seed production. Molecular Biology and Biotechnology of Plant Organelles 2004, 623-634. Springer, Daniell H, Chase C.
28. Chase CD. Cytoplasmic male sterility: a window to the world of plant mitochondrial-nuclear interactions. Trends Genet 2007, 23(2):81-90. 10.1016/j.tig.2006.12.004, 17188396.
29. Bentolila S, Alfonso AA, Hanson MR. A pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants. Proc Natl Acad Sci USA 2002, 99(16):10887-92. 10.1073/pnas.102301599, 125068, 12136123.
30. Kazama T, Toriyama K. A pentatricopeptide repeat-containing gene that promotes the processing of aberrant atp6 RNA of cytoplasmic male-sterile rice. FEBS Lett 2003, 544(1-3):99-102. 10.1016/S0014-5793(03)00480-0, 12782297.
31. Komori T, Ohta S, Murai N, Takakura Y, Kuraya Y, Suzuki S, Hiei Y, Imaseki H, Nitta N. Map-based cloning of a fertility restorer gene, Rf-1, in rice (Oryza sativa L.). Plant J 2004, 37(3):315-25. 10.1046/j.1365-313X.2003.01961.x, 14731253.
32. Akagi H, Nakamura A, Yokozeki-Misono Y, Inagaki A, Takahashi H, Mori K, Fujimura T. Positional cloning of the rice Rf-1 gene, a restorer of BT-type cytoplasmic male sterility that encodes a mitochondria-targeting PPR protein. Theor Appl Genet 2004, 108(8):1449-57. 10.1007/s00122-004-1591-2, 14968308.
33. Brown GG, Formanova N, Jin H, Wargachuk R, Dendy C, Patil P, Laforest M, Zhang J, Cheung WY, Landry BS. The radish Rfo restorer gene of Ogura cytoplasmic male sterility encodes a protein with multiple pentatricopeptide repeats. Plant J 2003, 35(2):262-72. 10.1046/j.1365-313X.2003.01799.x, 12848830.
34. Desloire S, Gherbi H, Laloui W, Marhadour S, Clouet V, Cattolico L, Falentin C, Giancola S, Renard M, Budar F, Small I, Caboche M, Delourme R, Bendahmane A. Identification of the fertility restoration locus, Rfo, in radish, as a member of the pentatricopeptide-repeat protein family. EMBO Rep 2003, 4(6):588-594. 10.1038/sj.embor.embor848, 1319198, 12740605.
35. Koizuka N, Imai R, Fujimoto H, Hayakawa T, Kimura Y, Kohno-Murase J, Sakai T, Kawasaki S, Imamura J. Genetic characterization of a pentatricopeptide repeat protein gene, orf687, that restores fertility in the cytoplasmic male-sterile Kosena radish. Plant J 2003, 34(4):407-415. 10.1046/j.1365-313X.2003.01735.x, 12753581.
36. Kato H, Tezuka K, Feng YY, Kawamoto T, Takahashi H, Mori K, Akagi H. Structural diversity and evolution of the Rf-1 locus in the genus Oryza. Heredity 2007, 99(5):516-24. 10.1038/sj.hdy.6801026, 17622268.
37. 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. 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 2006, 18(3):676-87. 10.1105/tpc.105.038240, 1383642, 16489123.
38. Touzet P, Budar F. Unveiling the molecular arms race between two conflicting genomes in cytoplasmic male sterility?. Trends Plant Sci 2004, 9(12):568-70. 10.1016/j.tplants.2004.10.001, 15564120.
39. Michelmore RW, Meyers BC. Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res 1998, 8(11):1113-30.
40. Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW. Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 2003, 15(4):809-34. 10.1105/tpc.009308, 152331, 12671079.
41. Geddy R, Brown GG. Genes encoding pentatricopeptide repeat (PPR) proteins are not conserved in location in plant genomes and may be subject to diversifying selection. BMC Genomics 2007, 8(1):130. 10.1186/1471-2164-8-130, 1892557, 17521445.
42. Bonnet A. Breeding in France of a radish F1 hybrid obtained by use of cytoplasmic male sterility. Eucarpia Cruciferae Newslett 1977, 2:5.
43. Noe L, Kucherov G. YASS: enhancing the sensitivity of DNA similarity search. Nucleic Acids Res 2005, (33 Web Server):W540-3. 10.1093/nar/gki478, 1160238, 15980530.
44. Burge CB, Karlin S. Finding the genes in genomic DNA. Curr Opin Struct Biol 1998, 8(3):346-54. 10.1016/S0959-440X(98)80069-9, 9666331.
45. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25(17):3389-402. 10.1093/nar/25.17.3389, 146917, 9254694.
46. Small I, Peeters N, Legeai F, Lurin C. Predotar: A tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics 2004, 4(6):1581-90. 10.1002/pmic.200300776, 15174128.
47. Emanuelsson O, Brunak S, von Heijne G, Nielsen H. Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2007, 2(4):953-71. 10.1038/nprot.2007.131, 17446895.
48. Etherington GJ, Dicks J, Roberts IN. Recombination Analysis Tool (RAT): a program for the high-throughput detection of recombination. Bioinformatics 2005, 21(3):278-81. 10.1093/bioinformatics/bth500, 15333462.
49. Giancola S, Rao Y, Chaillou S, Hiard S, Martin-Canadell A, Pelletier G, Budar F. Cytoplasmic suppression of Ogura cytoplasmic male sterility in European natural populations of Raphanus raphanistrum. Theor Appl Genet 2007, 114(8):1333-43. 10.1007/s00122-007-0520-6, 17318491.
50. Zhang Y, Cheng YT, Bi D, Palma K, Li X. MOS2, a protein containing G-patch and KOW motifs, is essential for innate immunity in Arabidopsis thaliana. Curr Biol 2005, 15(21):1936-42. 10.1016/j.cub.2005.09.038, 16271871.
51. Seah S, Telleen AC, Williamson VM. Introgressed and endogenous Mi-1 gene clusters in tomato differ by complex rearrangements in flanking sequences and show sequence exchange and diversifying selection among homologues. Theor Appl Genet 2007, 114(7):1289-302. 10.1007/s00122-007-0519-z, 17318492.
52. Noel L, Moores TL, Biezen EA, Parniske M, Daniels MJ, Parker JE, Jones JD. Pronounced intraspecific haplotype divergence at the RPP5 complex disease resistance locus of Arabidopsis. Plant Cell 1999, 11(11):2099-112. 10.1105/tpc.11.11.2099, 144120, 10559437.
53. Wicker T, Yahiaoui N, Keller B. Illegitimate recombination is a major evolutionary mechanism for initiating size variation in plant resistance genes. Plant J 2007, 51(4):631-41. 10.1111/j.1365-313X.2007.03164.x, 17573804.
54. Peterson D, Tomkins J, Frisch D, Wing R, Paterson A. Construction of plant bacterial artificial chromosome (BAC) libraries: an illustrated guide. Journal of Agricultural Genomics 2000, 5., http://www.mgel.msstate.edu/pubs/Peterson%20et%20al%202000.pdf
55. Dellaporta J, Wood J, Hicks J. A plant DNA minipreparation: Version II. Plant Mol Biol Rep 1983, 1:19-21.
56. Burge C, Karlin S. Prediction of complete gene structures in human genomic DNA. J Mol Biol 1997, 268(1):78-94. 10.1006/jmbi.1997.0951, 9149143.
57. New GENSCAN Web Server at MIT. , http://genes.mit.edu/GENSCAN.html
58. atgc PPR. , http://atgc.lirmm.fr/PPR
59. Uricaru R, Bréhélin L, Rivals E. A new type of Hidden Markov Models to predict complex motif organization in protein sequences. Proceeding of Journées Ouvertes Biologie Informatique Mathématiques (JOBIM): Marseille 2007, 97-102. Brun C, Didier G.
60. Predotar v. 1.03. , http://urgi.versailles.inra.fr/predotar/predotar.html
61. TargetP 1.1 server. , http://www.cbs.dtu.dk/services/TargetP
62. YASS: genomic DNA/RNA similarity search tool. , http://bioinfo.lifl.fr/yass/yass.php
63. Phylogeny.fr. , http://www.phylogeny.fr
64. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, Claverie JM, Gascuel O. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 2008, (36 Web Server):W465-9. 10.1093/nar/gkn180, 2447785, 18424797.
65. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32(5):1792-7. 10.1093/nar/gkh340, 390337, 15034147.
66. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 2000, 17(4):540-52.
67. Anisimova M, Gascuel O. Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Syst Biol 2006, 55(4):539-52. 10.1080/10635150600755453, 16785212.
68. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52(5):696-704. 10.1080/10635150390235520, 14530136.
69. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ. Jalview Version 2--a multiple sequence alignment editor and analysis workbench. Bioinformatics 2009, 25(9):1189-91. 10.1093/bioinformatics/btp033, 2672624, 19151095.
70. Chevenet F, Brun C, Banuls AL, Jacq B, Christen R. TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinformatics 2006, 7:439. 10.1186/1471-2105-7-439, 1615880, 17032440.