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Mitochondrial transcript length polymorphisms are a widespread phenomenon in Arabidopsis thaliana

Abstract

Natural genetic variation affects development, physiology, biochemical properties as well as mitochondrial transcripts of the model species Arabidopsis thaliana (Arabidopsis). In a previous study, we identified mitochondrial transcript end polymorphisms in Arabidopsis accessions Columbia, C24 and Landsberg erecta. The polymorphic transcript species could either be assigned to differences in the mitochondrial DNA or to natural genetic variation in the nucleus. To analyze the distribution and to identify additional 5′ end polymorphisms we now analyzed 19 mitochondrial transcription units in 26 different accessions. We found additional 5′ end polymorphisms indicating that such transcript length differences are a widespread phenomenon in Arabidopsis. The new polymorphisms affect cox1, cox2, nad2 as well nad3-rps12 transcript species. While the cox2 polymorphism can be attributed to a recombination event in the mitochondrial DNA, the nad2 transcript polymorphism is linked to differences in the nuclear DNA. A complex pattern is found for nad3-rps12 mRNA whose 5′ ends differ between several accessions. These new polymorphisms provide an important basis for a more detailed characterization of mitochondrial 5′ end processing.

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References

  • Andrés C, Lurin C, Small I (2007) The multifarious roles of PPR proteins in plant mitochondrial gene expression. Physiol Plant 129:14–22

    Article  Google Scholar 

  • Arrieta-Montiel MP, Shedge V, Davila J, Christensen AC, Mackenzie SA (2009) Diversity of the Arabidopsis mitochondrial genome occurs via nuclear-controlled recombination activity. Genetics 183:1261–1268

    PubMed  Article  CAS  Google Scholar 

  • Bentolila S, Alfonso AA, Hanson MR (2002) A pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants. Proc Natl Acad Sci USA 99:10887–10892

    PubMed  Article  CAS  Google Scholar 

  • Bentolila S, Chateigner-Boutin AL, Hanson MR (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

    PubMed  Article  CAS  Google Scholar 

  • Bentolila S, Elliott LE, Hanson MR (2008) Genetic architecture of mitochondrial editing in Arabidopsis thaliana. Genetics 178:1693–1708

    PubMed  Article  CAS  Google Scholar 

  • Bentolila S, Knight W, Hanson M (2010) Natural variation in Arabidopsis leads to the identification of REME1, a pentatricopeptide repeat-DYW protein controlling the editing of mitochondrial transcripts. Plant Physiol 154:1966–1982

    PubMed  Article  CAS  Google Scholar 

  • Binder S, Brennicke A (1993) Transcription initiation sites in mitochondria of Oenothera berteriana. J Biol Chem 268:7849–7855

    PubMed  CAS  Google Scholar 

  • Brown GG, Formanova N, Jin H, Wargachuk R, Dendy C, Patil P, Laforest M, Zhang J, Cheung WY, Landry BS (2003) The radish Rfo restorer gene of Ogura cytoplasmic male sterility encodes a protein with multiple pentatricopeptide repeats. Plant J 35:262–272

    PubMed  Article  CAS  Google Scholar 

  • Clark RM, Schweikert G, Toomajian C, Ossowski S, Zeller G, Shinn P, Warthmann N, Hu TT, Fu G, Hinds DA, Chen H, Frazer KA, Huson DH, Scholkopf B, Nordborg M, Ratsch G, Ecker JR, Weigel D (2007) Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana. Science 317:338–342

    PubMed  Article  CAS  Google Scholar 

  • 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

    PubMed  Article  CAS  Google Scholar 

  • Delannoy E, Stanley WA, Bond CS, Small ID (2007) Pentatricopeptide repeat (PPR) proteins as sequence-specificity factors in post-transcriptional processes in organelles. Biochem Soc Trans 35:1643–1647

    PubMed  Article  CAS  Google Scholar 

  • 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 (2003) Identification of the fertility restoration locus, Rfo, in radish, as a member of the pentatricopeptide-repeat protein family. EMBO Rep 4:588–594

    PubMed  Article  CAS  Google Scholar 

  • Forner J, Weber B, Wietholter C, Meyer RC, Binder S (2005) Distant sequences determine 5’ end formation of cox3 transcripts in Arabidopsis thaliana ecotype C24. Nucleic Acids Res 33:4673–4682

    PubMed  Article  CAS  Google Scholar 

  • 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. Nucleic Acids Res 35:3676–3692

    PubMed  Article  CAS  Google Scholar 

  • Forner J, Hölzle A, Jonietz C, Thuss S, Weber B, Schwarzländer M, Meyer RC, Binder S (2008) Mitochondrial mRNA polymorphisms in different Arabidopsis thaliana accessions. Plant Physiol 148:1106–1116

    PubMed  Article  CAS  Google Scholar 

  • Fujii S, Bond CS, Small ID (2011) Selection patterns on restorer-like genes reveal a conflict between nuclear and mitochondrial genomes throughout angiosperm evolution. Proc Natl Acad Sci USA 108:1723–1728

    PubMed  Article  CAS  Google Scholar 

  • Hoffmann M, Binder S (2002) Functional importance of nucleotide identities within the pea atp9 mitochondrial promoter sequence. J Mol Biol 320:943–950

    PubMed  Article  CAS  Google Scholar 

  • 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

    PubMed  Article  Google Scholar 

  • Hu J, Wang K, Huang W, Liu G, Gao Y, Wang J, Huang Q, Ji Y, Qin X, Wan L, Zhu R, Li S, Yang D, Zhu Y (2012) The rice pentatricopeptide repeat protein RF5 restores fertility in Hong-Lian cytoplasmic male-sterile lines via a complex with the glycine-rich protein GRP162. Plant Cell 24:109–122

    PubMed  Article  CAS  Google Scholar 

  • Jonietz C, Forner J, Holzle 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

    PubMed  Article  CAS  Google Scholar 

  • 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

    PubMed  Article  CAS  Google Scholar 

  • Kazama T, Toriyama K (2003) A pentatricopeptide repeat-containing gene that promotes the processing of aberrant atp6 RNA of cytoplasmic male-sterile rice. FEBS Lett 544:99–102

    PubMed  Article  CAS  Google Scholar 

  • Keech O, Dizengremel P, Gardeström P (2005) Preparation of leaf mitochondria from Arabidopsis thaliana. Physiol Plant 124:403–409

    Article  CAS  Google Scholar 

  • Köhler D, Schmidt-Gattung S, Binder S (2010) The DEAD-box protein PMH2 is required for efficient group II intro splicing in mitochondria of Arabidopsis thaliana. Plant Mol Biol 72:459–467

    PubMed  Article  Google Scholar 

  • Koizuka N, Imai R, Fujimoto H, Hayakawa T, Kimura Y, Kohno-Murase J, Sakai T, Kawasaki S, Imamura J (2003) Genetic characterization of a pentatricopeptide repeat protein gene, orf687, that restores fertility in the cytoplasmic male-sterile Kosena radish. Plant J 34:407–415

    PubMed  Article  CAS  Google Scholar 

  • Kühn K, Weihe A, Börner T (2005) Multiple promoters are a common feature of mitochondrial genes in Arabidopsis. Nucleic Acids Res 33:337–346

    PubMed  Article  Google Scholar 

  • Kühn K, Richter U, Meyer EH, Delannoy E, Falcon de Longevialle A, O’Toole N, Börner T, Millar AH, Small ID, Whelan J (2009) Phage-type RNA polymerase RPOTmp performs gene-specific transcription in mitochondria of Arabidopsis thaliana. Plant Cell 21:2762–2779

    PubMed  Article  Google Scholar 

  • Lupold DS, Caoile AG, Stern DB (1999) Genomic context influences the activity of maize mitochondrial cox2 promoters. Proc Natl Acad Sci USA 96:11670–11675

    PubMed  Article  CAS  Google Scholar 

  • 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 (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16:2089–2103

    PubMed  Article  CAS  Google Scholar 

  • McGinnis S, Madden TL (2004) BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucleic Acids Res 32:W20–W25

    PubMed  Article  CAS  Google Scholar 

  • McKhann HI, Camilleri C, Berard A, Bataillon T, David JL, Reboud X, Le Corre V, Caloustian C, Gut IG, Brunel D (2004) Nested core collections maximizing genetic diversity in Arabidopsis thaliana. Plant J 38:193–202

    PubMed  Article  CAS  Google Scholar 

  • Millar AH, Heazlewood JL, Kristensen BK, Braun HP, Moller IM (2005) The plant mitochondrial proteome. Trends Plant Sci 10:36–43

    PubMed  Article  CAS  Google Scholar 

  • Millar AH, Whelan J, Small I (2006) Recent surprises in protein targeting to mitochondria and plastids. Curr Opin Plant Biol 9:610–615

    PubMed  Article  CAS  Google Scholar 

  • Moison M, Roux F, Quadrado M, Duval R, Ekovich M, Le D-H, Budar F (2010) Cytoplasmic phyolgeny and evidence of cyto-nuclear co-adaption in Arabidopsis thaliana. Plant J 63:728–738

    PubMed  Article  CAS  Google Scholar 

  • 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

    PubMed  Article  Google Scholar 

  • Sambrook J, Russel DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • 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 (2006) 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 18:676–687

    PubMed  Article  CAS  Google Scholar 

  • Weigel D, Glazebrook J (2002) Arabidopsis, a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Habor

    Google Scholar 

  • Zehrmann A, van der Merwe JA, Verbitskiy D, Brennicke A, Takenaka M (2008) Seven large variations in the extent of RNA editing in plant mitochondria between three ecotypes of Arabidopsis thaliana. Mitochondrion 8:319–327

    PubMed  Article  CAS  Google Scholar 

  • 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

    PubMed  Article  CAS  Google Scholar 

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Acknowledgments

We thank the Deutsche Forschungsgemeinschaft (DFG) for financial support of this project (Bi 590/10-2) and U. Tengler and C. Guha for perfect technical assistance. We are very grateful to Rhonda Meyer (Institut für Pflanzengenetik und Kulturpflanzenforschung) for Arabidopsis F1 hybrid seeds.

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Correspondence to Stefan Binder.

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Stoll, B., Stoll, K., Steinhilber, J. et al. Mitochondrial transcript length polymorphisms are a widespread phenomenon in Arabidopsis thaliana . Plant Mol Biol 81, 221–233 (2013). https://doi.org/10.1007/s11103-012-9993-z

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  • DOI: https://doi.org/10.1007/s11103-012-9993-z

Keywords

  • Arabidopsis thaliana
  • Natural genetic variation
  • Mitochondria
  • mRNA polymorphisms
  • 5′ end processing