Abstract
An increase in the unspliced cox2 transcript and accompanying decrease in the frequency of RNA editing near the exon/intron junction (intron binding site 1, IBS1) have been reported in cold-treated wheat. Here, an attempt was made to clarify whether a similar phenomenon occurs in rice. Levels of unspliced cox2 transcript increased and its editing at the IBS was abolished after cold treatment. The accumulation of COXII protein remained unaffected. The accumulation of intron-containing transcripts of another eight mitochondrial genes, 23 introns in total, was analyzed by Northern blotting and semi-quantitative RT-PCR. An increase in 14 of the 23 intron-adjoining cDNA after cold treatment was observed. Six RNA editing sites in the IBS of four genes were tested as to their status by sequencing cDNA. One of these sites in the nad7 transcript showed a close association with splicing, with editing and splicing occurring simultaneously, irrespective of cold treatment. Two other sites in the intron-containing cox2 and rps3 transcripts were sensitive to cold, where editing frequency began to decrease 1 day after cold treatment, and finally exhibited a tight association with splicing 14 days later. The other sites were efficiently edited. The intron-spliced transcripts were fully edited at all six sites.
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Abbreviations
- IBS:
-
Intron binding site
- EBS:
-
Exon binding site
- CBB:
-
Coomassie brilliant blue
- UTR:
-
Untranslated region
References
Armstrong A et al (2008) Dynamic changes in the mitochondrial electron transport chain underpinning cold acclimation of leaf respiration. Plant Cell Environ 31:1156–1169
Bonen L (2008) Cis- and trans-splicing of group II introns in plant mitochondria. Mitochondrion 8:26–34
Bonen L, Vogel J (2001) The ins and outs of group II introns. Trends Genet 17:322–330
Börner GV, Mörl M, Wissinger B, Brennicke A, Schmelzer C (1995) RNA editing of a group II intron in Oenothera as a prerequisite for splicing. Mol Gen Genet 246:739–744
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
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
Covey-Crump EM, Bykova N, Affourtit C, Hoefnagel MHN, Gardestrom P, Atkin OK (2007) Temperature-dependent changes in respiration rates and redox poise of the ubiquinone pool in protoplasts and isolated mitochondria of potato leaves. Physiol Plant 129:175–184
de Longevialle AF, Meyer EH, Andres 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
Dombrovska O, Qiu YL (2004) Distribution of introns in the mitochondrial gene nad1 in land plants: phylogenetic and molecular evolutionary implications. Mol Phylogenet Evol 32:246–263
Estiati A (2000) Studies on genome structure and gene content in sugar beet (Beta vulgaris L.) mitochondrial DNA. Dissertation, Hokkaido University
Farré J-C, Araya A (2001) RNA splicing in higher plant mitochondria: determination of functional elements in group II intron from a chimeric coxII gene in electroporated wheat mitohcondria. Plant J 29:203–213
Giegé P, Brennicke A (1999) RNA editing in Arabidopsis mitochondria effects 441 C to U changes in ORF. Proc Natl Acad Sci USA 96:15324–15329
Grewe F, Viehoever P, Weisshaar B, Knoop V (2009) A trans-splicing group I intron and tRNA-hyperediting in the mitochondrial genome of the lycophyte Isoetes engelmannii. Nucleic Acids Res 37:5093–5104
Handa H (2003) The complete nucleotide sequence and RNA editing content of the mitochondrial genome of rapeseed (Brassica napus L.): comparative analysis of the mitochondrial genomes of rapeseed and Arabidopsis thaliana. Nucleic Acids Res 31:5907–5916
Holec S, Lange H, Canaday J, Gagliardi D (2008) Coping with cryptic and defective transcripts in plant mitochondria. Biochim Biophys Acta 1779:566–573
Kabaki N, Yoneyama T, Tajima K (1982) Physiological mechanism of growth retardation in rice seedlings as affected by temperature. Jpn J Crop Sci 51:82–88
Kacperska A (1993) Water potential alterations—a prerequisite or a triggering stimulus for the development of freezing tolerance in over wintering herbaceous plant? In: Li P, Christersson L (eds) Advance in plant cold hardiness. CRC Press, Boca Raton, pp 73–91
Karcher D, Bock R (1998) Site-selective inhibition of plastid RNA editing by heat shock and antibiotics: a role for plastid translation in RNA editing. Nucleic Acids Res 26:1185–1190
Karcher D, Bock R (2002) Temperature sensitivity of RNA editing and intron splicing reactions in the plastid ndhB transcript. Curr Genet 41:48–52
Kemble RJ (1987) A rapid, single leaf, nucleic acid assay for determining the cytoplasmic organelle complement of rapeseed and related Brassica species. Theor Appl Genet 73:364–370
Knoop V (2004) The mitochondrial DNA of land plants: peculiarities in phylogenetic perspective. Curr Genet 46:123–139
Kratsch HA, Wise RR (2000) The ultrastructure of chilling stress. Plant Cell Environ 23:337–350
Kubo T, Mikami T (2007) Organization and variation of angiosperm mitochondrial genome. Physiol Plant 129:6–13
Kubo T, Newton KJ (2008) Angiosperm mitochondrial genomes and mutations. Mitochondrion 8:5–14
Kuhn K, Bohne AV, Liere K, Weihe A, Börner T (2007) Arabidopsis phage-type RNA polymerases: accurate in vitro transcription of organellar genes. Plant Cell 19:959–971
Kunzmann A, Brennicke A, Marchfelder A (1998) 5′ end maturation and RNA editing have to precede tRNA 3′ processing in plant mitochondria. Proc Natl Acad Sci USA 95:108–113
Kurihara-Yonemoto S, Handa H (2001) Low temperature affects the processing pattern and RNA editing status of the mitochondrial cox2 transcripts in wheat. Curr Genet 40:203–208
Kurimoto K et al (2004) Maintenance of growth rate at low temperature in rice and wheat cultivars with a high degree of respiratory homeostasis is associated with a high efficiency of respiratory ATP production. Plant Cell Physiol 45:1015–1022
Laemmli UK (1970) Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227:680–685
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
Li-Pook-Than J, Carrillo C, Niknejad N, Calixte S, Crosthwait J, Bonen L (2007) Relationship between RNA splicing and exon editing near intron junctions in wheat mitochondria. Physiol Plant 129:23–33
Logan DC, Millar AH, Sweetlove LJ, Hill SA, Leaver CJ (2001) Mitochondrial biogenesis during germination in maize embryos. Plant Physiol 125:662–672
Marechal-Drouard L, Kumar R, Remacle C, Small I (1996) RNA editing of larch mitochondrial tRNAHis precursors is a prerequisite for processing. Nucleic Acids Res 24:3229–3234
Mizuno N, Sugie A, Kobayashi F, Takumi S (2008) Mitochondrial alternative pathway is associated with development of freezing tolerance in common wheat. J Plant Physiol 165:462–467
Mower JP, Palmer JD (2006) Patterns of partial RNA editing in mitochondrial genes of Beta vulgaris. Mol Genet Genomics 276:285–293
Nagamine T (1991) Genetic control of tolerance to chilling injury at seedling stage in rice, Oryza sativa L. Jpn J Breed 41:35–40
Nakagawa N, Sakurai N (2006) A mutation in At-nMat1a, which encodes a nuclear gene having high similarity to group II intron maturase, causes impaired splicing of mitochondrial NAD4 transcript and altered carbon metabolism in Arabidopsis thaliana. Plant Cell Physiol 47:772–783
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
Notsu Y, Masood S, Nishikawa T, Kubo N, Akiduki G, Nakazono M, Hirai A, Kadowaki K (2002) The complete sequence of the rice (Oryza sativa L.) mitochondrial genome: frequent DNA sequence acquisition and loss during the evolution of flowering plants. Mol Genet Genomics 268:434–445
Rüdinger M, Funk HT, Rensing SA, Maier UG, Knoop V (2009) RNA editing: only eleven sites are present in the Physcomitrella patens mitochondrial transcriptome and a universal nomenclature proposal. Mol Genet Genomics 281:473–481
Saisho D, Nakazono M, Lee KH, Tsutsumi N, Akita S, Hirai A (2001) The gene for alternative oxidase-2 (AOX2) from Arabidopsis thaliana consists of five exons unlike other AOX genes and is transcribed at an early stage during germination. Genes Genet Syst 76:89–97
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
Scheffler IE (1999) Mitochondria. Wiley-Liss, New Jersey
Shikanai T (2006) RNA editing in plant organelles: machinery, physiological function and evolution. Cell Mol Life Sci 63:698–708
Sutton CA, Conklin PL, Pruitt KD, Hanson MR (1991) Editing of pre-mRNAs can occur before cis- and trans-splicing in Petunia mitochondria. Mol Cell Biol 11:4274–4277
Takenaka M, Verbitskiy D, van der Merwe JA, Zehrmann A, Brennicke A (2008) The process of RNA editing in plant mitochondria. Mitochondrion 8:35–46
Verbitskiy D, Takenaka M, Neuwirt J, van der Merwe JA, Brennicke A (2006) Partially edited RNAs are intermediates of RNA editing in plant mitochondria. Plant J 47:408–416
Wen JQ, Oono K, Imai R (2002) Two novel mitogen-activated protein signaling components, OsMEK1 and OsMAP1, are involved in a moderate low-temperature signaling pathway in rice. Plant Physiol 129:1880–1891
Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci 10:88–94
Yang AJ, Mulligan M (1991) RNA editing intermediates of cox2 transcripts in maize mitochondria. Mol Cell Biol 11:4278–4281
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
Acknowledgments
We would like to thank Drs. T. Mikami, H. Handa, S. Matsuba and T. Akiyama for their helpful comments and discussion.
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Communicated by R. Bock.
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294_2010_320_MOESM1_ESM.ppt
Semi-quantitative RT-PCR of rice nad1, nad2, nad4, nad5, nad7, rps3, rpl2, and ccmF C . Complementary DNA derived from cold-treated (12°C) and control (25°C) rice plantlets was subjected to PCR, as described in Materials and methods and Table S1. Amplicons were electrophoresed on 2% agarose gels after the number of amplification cycles shown above the images, along with a negative control, in which the reverse transcriptase was omitted (−RT) (PPT 741 kb)
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Kurihara-Yonemoto, S., Kubo, T. Increased accumulation of intron-containing transcripts in rice mitochondria caused by low temperature: is cold-sensitive RNA editing implicated?. Curr Genet 56, 529–541 (2010). https://doi.org/10.1007/s00294-010-0320-4
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DOI: https://doi.org/10.1007/s00294-010-0320-4