Mapping of wheat mitochondrial mRNA termini and comparison with breakpoints in DNA homology among plants

Plant Molecular Biology

Volumn 80, Issue 4-5, 2012, Pages 539-552

  Choi, Boyoung ^a,b   Acero, Maria M ^a,c   Bonen, Linda ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

^b Celltrion Inc   (South Korea)

^c AGRICULTURE AND AGRI FOOD CANADA   (Canada)

Author keywords

Arabidopsis; DNA rearrangements; Mitochondria; mRNA processing; Wheat

Indexed keywords

MITOCHONDRIAL DNA; PLANT DNA; PLANT RNA;

3' UNTRANSLATED REGION; ARABIDOPSIS; ARTICLE; CHEMISTRY; COMPARATIVE STUDY; CONFORMATION; GENETICS; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; RNA EDITING; SEQUENCE HOMOLOGY; WHEAT;

3' UNTRANSLATED REGIONS; ARABIDOPSIS; BASE SEQUENCE; DNA, MITOCHONDRIAL; DNA, PLANT; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; RNA EDITING; RNA, PLANT; SEQUENCE HOMOLOGY, NUCLEIC ACID; TRITICUM;

AEGILOPS KOTSCHYI; ARABIDOPSIS; MAGNOLIOPHYTA; TRITICUM AESTIVUM;

EID: 84867651968     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11103-012-9966-2     Document Type: Article

References (65)

1. Allen JO, Fauron CM, Minx P, Roark L, Oddiraju S, Lin GN, Meyer L, Sun H, Kim K, Wang C, Du F, Xu D, Gibson M, Cifrese J, Clifton SW, Newton KJ (2007) Comparisons among two fertile and three male-sterile mitochondrial genomes of maize. Genetics 177: 1173-1192.
2. Binder S, Brennicke A (2002) Gene expression in plant mitochondria: transcriptional and post-transcriptional control. Philos Trans R Soc Lond 358: 181-189.
3. Bonen L (2008) Cis- and trans-splicing of group II introns in plant mitochondria. Mitochondrion 8: 26-34.
4. Bonen L, Bird S (1986) Sequence analysis of the wheat mitochondrial atp6 gene reveals a fused upstream reading frame and markedly divergent N termini among plant ATP6 proteins. Gene 73: 47-56.
5. Bonen L, Chapdelaine Y, Garber P (1992) Wheat mitochondrial protein-coding genes and their expression. In: Saskuma T, Kinoshita TK (eds) Nuclear and organellar genomes of wheat species. Memorial Foundation, Yokohama, pp 140-148.
6. Bonen L, Williams K, Bird S, Wood C (1994) The NADH dehydrogenase subunit 7 gene is interrupted by four group II introns in the wheat mitochondrial genome. Mol Gen Genet 244: 81-89.
7. Bonnard G, Grienenberger JM (1995) A gene proposed to encode a transmembrane domain of an ABC transporter is expressed in wheat mitochondria. Mol Gen Genet 246: 91-99.
8. Byers E, Rueger J, Bonen L (2010) Impact of genomic environment on mitochondrial rps7 mRNA features in grasses. Mol Gen Genomics 284: 207-216.
9. Calixte S, Bonen L (2008) Developmentally-specific transcripts from the ccmFN-rps1 locus in wheat mitochondria. Mol Gen Genomics 280: 419-426.
10. Chapdelaine C, Bonen L (1991) The wheat mitochondrial gene for subunit I of the NADH dehydrogenase complex: a trans-splicing model for this gene-in-pieces. Cell 65: 465-472.
11. Chase CD (2007) Cytoplasmic male sterility: a window to the world of plant mitochondrial-nuclear interactions. Trends Genet 23: 81-90.
12. Covello PS, Gray MW (1990) Differences in editing at homologous sites in messenger RNAs from angiosperm mitochondria. Nucl Acids Res 18: 5189-5196.
13. Covello PS, Gray MW (1991) Sequence analysis of wheat mitochondrial transcripts capped in vitro: definitive identification of transcription initiation sites. Curr Genet 20: 245-251.
14. Davila JI, Arrieta-Montiel MP, Wamboldt Y, Cao J, Hagmann J, Shedge V, Xu YZ, Weigel D, Mackenzie SA (2011) Double-strand break repair processes drive evolution of the mitochondrial genome in Arabidopsis. BMC Biol 9: 64.
15. Faivre-Nitschke SE, Nazoa P, Gualberto JM, Grienenberger JM, Bonnard G (2001) Wheat mitochondria ccmB encodes the membrane domain of a putative ABC transporter involved in cytochrome c biogenesis. Biochim Biophys Acta 1519: 199-208.
16. Fang Y, Wu H, Zhang T, Yang M, Yin Y, Pan L, Yu X, Zhang X, Hu S, Al-Mssallem IS, Yu J (2012) A complete sequence and transcriptomic analyses of date palm (Phoenix dactylifera L.) mitochondrial genome. PLoS ONE 7: e37164.
17. Farré JC, Araya A (1999) The mat-r open reading frame is transcribed from a non-canonical promoter and contains an internal promoter to co-transcribe exons nad1e and nad5III in wheat mitochondria. Plant Mol Biol 40: 959-967.
18. Forner J, Weber B, Thuss S, Wildum S, Binder S (2007) Mapping of mitochondrial mRNA termini in Arabidopsis thaliana: t-elements contribute to 5′ and 3′ end formation. Nucl Acids Res 35: 3676-3692.
19. Fujii S, Toda T, Kikuchi S, Suzuki R, Yokoyama K, Tsuchida H, Yano K, Toriyama K (2011) Transcriptome map of plant mitochondria reveals islands of unexpected transcribed regions. BMC Genomics 12: 279.
20. Giegé P, Rayapuram N, Meyer EH, Grienenberger JM, Bonnard G (2004) CcmFc involved in cytochrome c maturation is present in a large sized complex in wheat mitochondria. FEBS Lett 563: 165-169.
21. Gonzalez DH, Bonnard G, Grienenberger JM (1993) A gene involved in the biogenesis of cytochromes is co-transcribed with a ribosomal protein gene in wheat mitochondria. Curr Genet 24: 248-255.
22. Gualberto JM, Wintz H, Weil JH, Grienenberger JM (1988) The genes coding for subunit 3 of NADH dehydrogenase and for ribosomal protein S12 are present in the wheat and maize mitochondrial genomes and are co-transcribed. Mol Gen Genet 215: 118-127.
23. Gualberto JM, Domon C, Weil JH, Grienenberger JM (1990) Structure and transcription of the gene coding for subunit 3 of cytochrome oxidase in wheat mitochondria. Curr Genet 17: 41-47.
24. Gualberto JM, Bonnard G, Lamattina L, Grienenberger JM (1991) Expression of the wheat mitochondrial nad3-rps12 transcription unit: correlation between editing and mRNA maturation. Plant Cell 3: 1109-1120.
25. Hanic-Joyce PJ, Spencer DF, Gray MW (1990) In vitro processing of transcripts containing novel tRNA-like sequences ('t-elements') encoded by wheat mitochondrial DNA. Plant Mol Biol 15: 551-559.
26. Hanson MR, Bentolila S (2004) Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 16: S154-S169.
27. Haouazine N, Pereira de Souza A, Jubier MF, Lancelin D, Delcher E, Lejeune B (1992) The wheat mitochondrial genome contains an ORF showing sequence homology to the gene encoding the subunit 6 of the NADH-ubiquinone oxidoreductase. Plant Mol Biol 20: 395-404.
28. Hazle T, Bonen L (2007) Comparative analysis of sequences preceding protein-coding mitochondrial genes in flowering plants. Mol Biol Evol 24: 1101-1112.
29. Holec S, Lange H, Canaday J, Gagliardi D (2008) Coping with cryptic and defective transcripts in plant mitochondria. Biochim Biophys Acta 1779: 566-573.
30. Hölzle A, Jonietz C, Törjek O, Altmann T, Binder S, Forner J (2011) A RESTORER OF FERTILITY-like PPR gene is required for 5′-end processing of the nad4 mRNA in mitochondria of Arabidopsis thaliana. Plant J 65: 737-744.
31. Iwabuchi M, Kyozuka J, Shimamoto K (1993) Processing followed by complete editing of an altered mitochondrial atp6 RNA restores fertility of cytoplasmic male sterile rice. EMBO J 12: 1437-1446.
32. Jonietz C, Forner J, Hölzle A, Thuss S, Binder S (2010) RNA PROCESSING FACTOR2 is required for 5′ end processing of nad9 and cox3 mRNAs in mitochondria of Arabidopsis thaliana. Plant Cell 22: 443-453.
33. Jonietz C, Forner J, Hildebrandt T, Binder S (2011) RNA PROCESSINGFACTOR 3 is crucial for the accumulation of mature ccmC transcripts in mitochondria of Arabidopsis thaliana accession Columbia. Plant Physiol 157: 1430-1439.
34. Joyce PB, Gray MW (1989) Chloroplast-like transfer RNA genes expressed in wheat mitochondria. Nucleic Acids Res 17: 5461-5476.
35. Kubo T, Newton KJ (2008) Angiosperm mitochondrial genomes and mutations. Mitochondrion 8: 5-14.
36. Lamattina L, Grienenberger JM (1991) RNA editing of the transcript coding for subunit 4 of NADH dehydrogenase in wheat mitochondria: uneven distribution of the editing sites among the four exons. Nucleic Acids Res 19: 3275-3282.
37. Lamattina L, Gonzalez D, Gualberto J, Grienenberger JM (1993) Higher plant mitochondria encode an homologue of the nuclear-encoded 30-kDa subunit of bovine mitochondrial complex I. Eur J Biochem 217: 831-838.
38. Laser B, Kück U (1995) The mitochondrial atpA/atp9 co-transcript in wheat and triticale: RNA processing depends on the nuclear genotype. Curr Genet 29: 50-57.
39. Liere K, Weihe A, Börner T (2011) The transcription machineries of plant mitochondria and chloroplasts: composition, function, and regulation. J Plant Physiol 168: 1345-1360.
40. Li-Pook-Than J, Carrillo C, Bonen L (2004) Variation in mitochondrial transcript profiles of protein-coding genes during early germination and seedling development in wheat. Curr Genet 46: 374-380.
41. Liu AW, Narayanan KK, André CP, Kaleikau EK, Walbot V (1992) Co-transcription of orf25 and coxIII in rice mitochondria. Curr Genet 21: 507-513.
42. Liu H, Cui P, Zhan K, Lin Q, Zhuo G, Guo X, Ding F, Yang W, Liu D, Hu S, Yu J, Zhang A (2011) Comparative analysis of mitochondrial genomes between a wheat K-type cytoplasmic male sterility (CMS) line and its maintainer line. BMC Genomics 12: 163.
43. Maréchal A, Brisson N (2010) Recombination and the maintenance of plant organelle genome stability. New Phytol 186: 299-317.
44. McGinnis S, Madden TL (2004) BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucl Acids Res 32: W20-W25.
45. Millar AH, Whelan J, Soole KL, Day DA (2011) Organization and regulation of mitochondrial respiration in plants. Ann Rev Plant Biol 62: 79-104.
46. Morawala-Patell V, Gualberto JM, Lamattina L, Grienenberger JM, Bonnard G (1998) Cis- and trans-splicing and RNA editing are required for the expression of nad2 in wheat mitochondria. Mol Gen Genet 258: 503-511.
47. Mulligan RM, Maloney AP, Walbot V (1988) RNA processing and multiple transcription initiation sites result in transcript size heterogeneity in maize mitochondria. Mol Gen Genet 211: 373-380.
48. Ogihara Y, Kurihara Y, Futami K, Tsuji K, Murai K (1999) Photoperiod-sensitive cytoplasmic male sterility in wheat: nuclear-mitochondrial incompatibility results in differential processing of the mitochondrial orf25 gene. Curr Genet 36: 354-362.
49. Ogihara Y, Yamazaki Y, Murai K et al. (14 authors) (2005) Structural dynamics of cereal mitochondrial genomes as revealed by complete nucleotide sequencing of the wheat mitochondrial genome. Nucl Acids Res 33: 6235-6250.
50. Pereira de Souza A, Jubier MF, Delcher E, Lancelin D, Lejeune B (1991) A trans-splicing model for the expression of the tripartite nad5 gene in wheat and maize mitochondria. Plant Cell 3: 1363-1378.
51. Perrin R, Meyer EH, Zaepfel M, Kim YJ, Mache R, Grienenberger JM, Gualberto JM, Gagliardi D (2004) Two exoribonucleases act sequentially to process mature 3′-ends of atp9 mRNAs in Arabidopsis mitochondria. J Biol Chem 279: 25440-25446.
52. Raczynska KD, Le Ret M, Rurek M, Bonnard G, Augustzniak H, Gualberto JM (2006) Plant mitochondrial genes can be expressed from mRNAs lacking stop codons. FEBS Lett 580: 5641-5646.
53. Saalaoui E, Litvak S, Araya A (1990) The apocytochrome b from an alloplasmic line of wheat (T. aestivum, cytoplasm-T. timopheevi) exists in two differently expressed forms. Plant Sci 66: 237-246.
54. Schmitz-Linneweber C, Small I (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci 13: 663-670.
55. Song J, Hedgcoth C (1994) Influence of nuclear background on transcription of a chimeric gene (orf256) and coxI in fertile and cytoplasmic male sterile wheats. Genome 37: 203-209.
56. Spencer DF, Bonen L, Gray MW (1981) Primary sequence of wheat mitochondrial 5S ribosomal ribonucleic acid: functional and evolutionary implications. Biochemistry 20: 4022-4029.
57. Spencer DF, Schnare MN, Gray MW (1984) Pronounced structural similarities between the small subunit ribosomal RNA genes of wheat mitochondria and Escherichia coli. Proc Natl Acad Sci USA 81: 493-497.
58. Spencer DF, Schnare MN, Coulthart MB, Gray MW (1992) Sequence and organization of a 7. 2 kb region of wheat mitochondrial DNA containing the large subunit (26S) rRNA gene. Plant Mol Biol 20: 347-352.
59. Subramanian S, Fallahi M, Bonen L (2001) Truncated and dispersed rpl2 and rps19 pseudogenes are cotranscribed with neighboring downstream genes in wheat mitochondria. Curr Genet 39: 264-272.
60. Unseld M, Marienfeld JR, Brandt P, Brennicke A (1997) The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366, 924 nucleotides. Nat Genet 15: 57-61.
61. Vaitilingom M, Stupar M, Grienenberger JM, Gualberto JM (1998) A gene coding for an RPS2 protein is present in the mitochondrial genome of several cereals. Mol Gen Genet 258: 530-537.
62. Wang D, Rousseau-Gueutin M, Timmis JN (2012) Plastid sequences contribute to some plant mitochondrial genes. Mol Biol Evol (in press).
63. Wolfe KH, Li WH, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci USA 84: 9054-9058.
64. Zhu Y, Saraike T, Yamamoto Y, Hagita H, Takumi S, Murai K (2008) Orf260cra, a novel mitochondrial gene, is associated with the homeotic transformation of stamens into pistil-like structures (pistillody) in alloplasmic wheat. Plant Cell Physiol 49: 1723-1733.
65. Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucl Acids Res 31: 3406-3415.