Abstract
We examined RNA profiles of wheat mitochondrial genes during the developmental period when seeds leave dormancy, germinate and develop into seedlings. Mitochondrial RNAs isolated from 0 h to 6 days post-imbibition were subjected to Northern analysis, using coding-specific and intron-specific probes. Stable, edited mRNAs were observed in dormant seeds and precursor RNAs were subsequently detected early in embryo germination. The respiratory chain genes (nad7, cox1, cox2, atp6) showed mRNA profiles which paralleled those of the ribosomal RNAs, whereas ribosomal protein genes (rps2, rps3, rps7) had proportionately lower steady-state mRNA levels in later stages of seedling development. The relative levels of precursors compared with the respective mRNAs shifted down during development, consistent with transcription outpacing RNA processing in the early stages but co-ordination being more effective several days after imbibition. In the case of multiply split genes containing group II introns, complex patterns of splicing intermediates were observed, suggesting a lack of strict polarity of intron removal, although splicing efficiency appears to differ among introns. Excised intron RNAs typically are relatively more abundant in embryos than seedlings. These observations are consistent with a transient imbalance of RNA-processing machinery at the onset of seed germination, which is a period of rapid mitochondrial biogenesis.
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Bentolila S, Alfonso AA, Hanson MR (2002) A pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants. Proc Natl Acad Sci USA 99:10887–20892
Bewley JD, Black M (1994) Seeds: physiology of development and germination, 2nd edn. Plenum, New York
Bonen L, Bird S (1988) 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
Bonen L, Vogel J (2001) The ins and outs of group II introns. Trends Genet 17:322–331
Bonen L, Boer PH, Gray MW (1984) The wheat cytochrome oxidase subunit II gene has an intron insert and three radical amino acid changes relative to maize. EMBO J 3:2531–2536
Bonen L, Boer PH, McIntosh JE, Gray MW (1987) Nucleotide sequence of the wheat mitochondrial gene for subunit I of cytochrome oxidase. Nucleic Acids Res 15:6734
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
Brangeon J, Sabar M, Gutierres S, Combettes B, Bove J, Gendy C, Chetrit P, Colas des Francs-Small C, Pla M, Vedel F, Paepe R de (2000) Defective splicing of the first nad4 intron associated with lack of several complex I subunits in the Nicotiana sylvestris NMS1 nuclear mutant. Plant J 21:269–280
Carrillo C, Bonen L (1997) RNA editing status of nad7 intron domains in wheat mitochondria. Nucleic Acids Res 25:403–409
Carrillo C, Chapedelaine Y, Bonen L (2001) Variation in sequence and RNA editing within core domains of mitochondrial group II introns among plants. Mol Gen Genet 264:595–603
Cho Y, Qiu YL, Kuhlman P, Palmer JD (1998) Explosive invasion of plant mitochondria by a group I intron. Proc Natl Acad Sci USA 95:14244–14249
Daley D, Considine MJ, Howell KA, Millar AH, Day DA, Whelan J (2003) Respiratory gene expression in soybean cotyledon during post-germination development. Plant Mol Biol 51:745–755
Ehrenshaft M, Brambl R (1990) Respiration and mitochondrial biogenesis in germinating embryos of maize. Plant Physiol 93:295–304
Gagliardi D, Stepien PP, Temperley RJ, Lightowlers RN, Chrzanowska-Lightowers ZMA (2004) Messenger RNA stability in mitochondria: different means to an end. Trends Genet 20:260–267
Giegé P, Hoffmann M, Binder S, Brennicke A (2000) RNA degradation buffers asymmetries of transcription in Arabidopsis mitochondria. EMBO Rep 1:164–170
Granlund M, Michel F, Norgren M (2001) Mutually exclusive distribution of IS 1548 and GBSi1, an active group II intron identified in isolates of group B Streptococci. J Bacteriol 183:2560–2569
Grosskopf D, Mulligan RM (1996) Developmental- and tissue-specificity of RNA editng in mitochondria of suspension-cultured maize cells and seedlings. Curr Genet 29:556–563
Hoffmann M, Kuhn J, Daschner K, Binder S (2001) The RNA world of plant mitochondria. Prog Nucleic Acids Res Mol Biol 70:119–154
Hollander V, Kuck U (1999) Group II intron splicing in chloroplasts: identification of mutations determining intron stability and fate of exon RNA. Nucleic Acids Res 27:2345–2353
Ikeda TM, Gray MW (1999) Characterization of a DNA-binding protein implicated in transcription in wheat mitochondria. Mol Cell Biol 19:8113–8122
Kim JK, Hollingsworth ML (1993) Splicing of group II introns in spinach chloroplasts (in vivo): analysis of lariat formation. Curr Genet 23:175–180
Logan DC, Millar AH, Sweetlove LJ, Hill SA, Leaver CJ (2001) Mitochondrial biogenesis during germination in maize embryos. Plant Physiol 125:662–672
Michel F, Ferat JL (1995) Structure and activities of group II introns. Annu Rev Biochem 64:435–461
Mohr G, Lambowitz AM (2003) Putative proteins related to group II intron reverse transcriptase/maturases are encoded by nuclear genes in higher plants. Nucleic Acids Res 31:647–652
Murray HL, Mikheeva S, Coljee VW, Turczyk BM, Donahue WF, Bar-Shalom A, Jarrell KA (2001) Excision of group II introns as circles. Mol Cell 8:201–211
Nakazono M, Itadani H, Wakasugi T, Tsutsumi N, Sugiura M, Hirai A (1995) The rps3-rpl16-nad3-rps12 gene cluster in rice mitochondrial DNA is transcribed from alternative promoters. Curr Genet 27:184–189
Ostheimer GJ, Williams-Carrier R, Belcher S, Osborne E, Gierke J, Barkan A (2003) Group II splicing factors derived by diversification of an ancient RNA-binding domain. EMBO J 22:3919–3929
Rasmusson AG, Soole KL, Elthon TE (2004) Alternative NAD(P)H dehydrogenases of plant mitochondria. Annu Rev Plant Biol 55:23–39
Small ID, Peeters N (2000) A PPR motif: a TPR-related motif prevalent in plant organellar proteins. Trends Biochem Sci 25:46–47
Subramanian S, Fallahi M, Bonen L (2001) Truncated and dispersed rpl2 and rps19 pseudogenes are co-transcribed with neighbouring downstream genes in wheat mitochondria. Curr Genet 39:264–272
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, but not in dicotyledons. Mol Gen Genet 258:530–537
Vermel M, Guermann B, Delage L, Grienenberger JM, Marechal-Drouard L, Gualberto JM (2002) A family of RRM-type RNA-binding proteins specific to plant mitochondria. Proc Natl Acad Sci USA 99:5866–5871
Vogel J, Borner T (2002) Lariat formation and a hydrolytic pathway in plant chloroplast group II intron splicing. EMBO J 21:3794–3803
Zhuo D, Bonen L (1993) Characterization of the S7 ribosomal protein gene in wheat mitochondria. Mol Gen Genet 236:395–401
Acknowledgements
We thank Dr. R. Pandeya (Agriculture and Agri-Food Canada, Ottawa) for kindly providing the wheat seeds used in this study and thank Sophie Calixte for excellent technical assistance. Financial support for this research by the Natural Sciences and Engineering Research Council of Canada (L.B.) and Ontario Graduate Scholarship (J.L.P.T.) is gratefully acknowledged.
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Communicated by A. Brennicke
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Li-Pook-Than, J., Carrillo, C. & Bonen, L. Variation in mitochondrial transcript profiles of protein-coding genes during early germination and seedling development in wheat. Curr Genet 46, 374–380 (2004). https://doi.org/10.1007/s00294-004-0544-2
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DOI: https://doi.org/10.1007/s00294-004-0544-2