Skip to main content
Log in

In Arabidopsis thaliana distinct alleles encoding mitochondrial RNA PROCESSING FACTOR 4 support the generation of additional 5′ termini of ccmB transcripts

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

In plant mitochondria, the 5′ ends of many transcripts are generated post-transcriptionally. We show that the pentatricopeptide repeat (PPR) protein RNA PROCESSING FACTOR 4 (RPF4) supports the generation of extra 5′ ends of ccmB transcripts in Landsberg erecta (Ler) and a number of other Arabidopsis thaliana ecotypes. RPF4 was identified in Ler applying a forward genetic approach supported by complementation studies of ecotype Columbia (Col), which generates the Ler-type extra ccmB 5′ termini only after the introduction of the RPF4 allele from Ler. Studies with chimeric RPF4 proteins composed of various parts of the RPF4 proteins from Ler and Col identified differences in the N-terminal and central PPR motifs that explain ecotype-specific variations in ccmB processing. These results fit well with binding site predictions in ccmB transcripts based on the known determinants of nucleotide base recognition by PPR motifs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Arnal N, Quadrado M, Simon M, Mireau H (2014) A restorer-of-fertility like pentatricopeptide repeat gene directs ribonucleolytic processing within the coding sequence of rps3-rpl16 and orf240a mitochondrial transcripts in Arabidopsis thaliana. Plant J 78:134–145

    Article  CAS  PubMed  Google Scholar 

  • Barkan A, Small I (2014) Pentatricopeptide repeat proteins in plants. Annu Rev Plant Biol 65:415–442

    Article  CAS  PubMed  Google Scholar 

  • Barkan A, Rojas M, Fujii S, Yap A, Chong YS, Bond CS, Small I (2012) A combinatorial amino acid code for RNA recognition by pentatricopeptide repeat proteins. PLoS Genet 8:e1002910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Binder S, Hölzle A, Jonietz C (2010) RNA processing and RNA stability in plant mitochondria. In: Kempken F (ed) Plant Mitochondria. Springer, New York, pp 107–130

    Google Scholar 

  • Binder S, Stoll K, Stoll B (2013) P-class pentatricopeptide repeat proteins are required for efficient 5′ end formation of plant mitochondrial transcripts. RNA Biol 10:1322–1330

    Article  Google Scholar 

  • Binder S, Stoll K, Stoll B (2016) Maturation of 5′ ends of plant mitochondrial RNAs. Physiol Plant 157:280–288

    Article  CAS  PubMed  Google Scholar 

  • Boussardon C, Avon A, Kindgren P, Bond CS, Challenor M, Lurin C, Small I (2014) The cytidine deaminase signature HxE(x)n CxxC of DYW1 binds zinc and is necessary for RNA editing of ndhD-1. New Phytol 203:1090–1095

    Article  CAS  PubMed  Google Scholar 

  • Chateigner-Boutin AL, Small I (2010) Plant RNA editing. RNA Biol 7:213–219

    Article  CAS  PubMed  Google Scholar 

  • Cheng S, Gutmann B, Zhong X, Ye Y, Fisher MF, Bai F, Castleden I, Song Y, Song B, Huang J, Liu X, Xu X, Lim BL, Bond CS, Yiu SM, Small I (2016) Redefining the structural motifs that determine RNA binding and RNA editing by pentatricopeptide repeat proteins in land plants. Plant J 85:532–547

    Article  CAS  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–742

    Article  CAS  PubMed  Google Scholar 

  • Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133:462–469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Derksen M, Mertens V, Pruijn GJ (2015) RNase P-mediated sequence-specific cleavage of RNA by engineered external guide sequences. Biomolecules 5:3029–3050

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edwards K, Johnstone C, Thompson C (1991) A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Res 19:1349

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  PubMed Central  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 accessions. Plant Physiol 148:1106–1116

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujii S, Suzuki T, Giege P, Higashiyama T, Koizuka N, Shikanai T (2016) The Restorer-of-fertility-like 2 pentatricopeptide repeat protein and RNase P are required for the processing of mitochondrial orf291 RNA in Arabidopsis. Plant J 86:504–513

    Article  CAS  PubMed  Google Scholar 

  • Haïli N, Arnal N, Quadrado M, Amiar S, Tcherkez G, Dahan J, Briozzo P, Colas des Francs-Small C, Vrielynck N, Mireau H (2013) The pentatricopeptide repeat MTSF1 protein stabilizes the nad4 mRNA in Arabidopsis mitochondria. Nucleic Acids Res 41:6650–6663

    Article  PubMed  PubMed Central  Google Scholar 

  • Haïli N, Planchard N, Arnal N, Quadrado M, Vrielynck N, Dahan J, Colas des Francs-Small C, Mireau H (2016) The MTL1 pentatricopeptide repeat protein is required for both translation and splicing of the mitochondrial NADH DEHYDROGENASE SUBUNIT7 mRNA in Arabidopsis. Plant Physiol 170:354–366

    Article  PubMed  Google Scholar 

  • Hammani K, Giegé P (2014) RNA metabolism in plant mitochondria. Trends Plant Sci 19:380–389

    Article  CAS  PubMed  Google Scholar 

  • Hauler A, Jonietz C, Stoll B, Stoll K, Braun H-P, Binder S (2013) RNA PROCESSING FACTOR 5 is required for efficient 5′ cleavage at a processing site conserved in RNAs of three different mitochondrial genes in Arabidopsis thaliana. Plant J 74:593–604

    Article  CAS  PubMed  Google Scholar 

  • Hayes ML, Giang K, Berhane B, Mulligan RM (2013) Identification of two pentatricopeptide repeat genes required for RNA editing and zinc binding by C-terminal cytidine deaminase-like domains. J Biol Chem 288:36519–36529

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayes ML, Dang KN, Diaz MF, Mulligan RM (2015) A conserved glutamate residue in the C-terminal deaminase domain of pentatricopeptide repeat proteins is required for RNA editing activity. J Biol Chem 290:10136–10142

    Article  CAS  PubMed  PubMed Central  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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jonietz C, Forner J, Hildebrandt T, Binder S (2011) RNA PROCESSING FACTOR 3 is crucial for the accumulation of mature ccmC transcripts in mitochondria of Arabidopsis thaliana accession Columbia. Plant Physiol 157:1430–1439

    Article  CAS  PubMed  PubMed Central  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

    Article  PubMed  Google Scholar 

  • Kubo T, Newton KJ (2008) Angiosperm mitochondrial genomes and mutations. Mitochondrion 8:5–14

    Article  CAS  PubMed  Google Scholar 

  • Lister C, Dean C (1993) Recombinant inbred lines for mapping RFLP and phenotypic markers in Arabidopsis thaliana. Plant J 4:745–750

    Article  CAS  Google Scholar 

  • Liu S, Melonek J, Boykin LM, Small I, Howell KA (2013) PPR-SMRs: ancient proteins with enigmatic functions. RNA Biol 10:1312–1321

    Article  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pfalz J, Bayraktar OA, Prikryl J, Barkan A (2009) Site-specific binding of a PPR protein defines and stabilizes 5′ and 3′ mRNA termini in chloroplasts. EMBO J 28:2042–2052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • Schmitz-Linneweber C, Small I (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci 13:663–670

    Article  CAS  PubMed  Google Scholar 

  • Shen C, Zhang D, Guan Z, Liu Y, Yang Z, Yang Y, Wang X, Wang Q, Zhang Q, Fan S, Zou T, Yin P (2016) Structural basis for specific single-stranded RNA recognition by designer pentatricopeptide repeat proteins. Nat Commun 7:11285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simon M, Simon A, Martins F, Botran L, Tisne S, Granier F, Loudet O, Camilleri C (2012) DNA fingerprinting and new tools for fine-scale discrimination of Arabidopsis thaliana accessions. Plant J 69:1094–1101

    Article  CAS  PubMed  Google Scholar 

  • Stoll B, Binder S (2016) Two NYN domain containing putative nucleases are involved in transcript maturation in Arabidopsis mitochondria. Plant J 85:278–288

    Article  CAS  PubMed  Google Scholar 

  • Stoll B, Stoll K, Steinhilber J, Jonietz C, Binder S (2012) Mitochondrial transcript length polymorphisms are a widespread phenomenon in Arabidopsis thaliana. Plant Mol Biol 81:221–233

    Article  PubMed  Google Scholar 

  • Stoll B, Zendler D, Binder S (2014) RNA processing factor 7 and polynucleotide phosphorylase are necessary for processing and stability of nad2 mRNA in Arabidopsis mitochondria. RNA Biol 11:968–976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stoll K, Jonietz C, Binder S (2015) In Arabidopsis thaliana two co-adapted cyto-nuclear systems correlate with distinct ccmC transcript sizes. Plant J 81:247–257

    Article  CAS  PubMed  Google Scholar 

  • Takenaka M, Zehrmann A, Brennicke A, Graichen K (2013) Improved computational target site prediction for pentatricopeptide repeat RNA editing factors. PLoS One 8(6):e65343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takenaka M, Verbitskiy D, Zehrmann A, Härtel B, Bayer-Császár E, Glass F, Brennicke A (2014) RNA editing in plant mitochondria—connecting RNA target sequences and acting proteins. Mitochondrion 19:191–197

    Article  CAS  PubMed  Google Scholar 

  • Wu W, Liu S, Ruwe H, Zhang D, Melonek J, Zhu Y, Hu X, Gusewski S, Yin P, Small ID, Howell KA, Huang J (2016) SOT1, a pentatricopeptide repeat protein with a small MutS-related domain, is required for correct processing of plastid 23S–4.5S rRNA precursors in Arabidopsis thaliana. Plant J 85:607–621

    Article  CAS  PubMed  Google Scholar 

  • Yagi Y, Hayashi S, Kobayashi K, Hirayama T, Nakamura T (2013a) Elucidation of the RNA recognition code for pentatricopeptide repeat proteins involved in organelle RNA editing in plants. PLoS One 8:e57286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yagi Y, Tachikawa M, Noguchi H, Satoh S, Obokata J, Nakamura T (2013b) Pentatricopeptide repeat proteins involved in plant organellar RNA editing. RNA Biol 10:1236–1242

    Article  Google Scholar 

  • Yin P, Li Q, Yan C, Liu Y, Liu J, Yu F, Wang Z, Long J, He J, Wang HW, Wang J, Zhu JK, Shi Y, Yan N (2013) Structural basis for the modular recognition of single-stranded RNA by PPR proteins. Nature 504:168–171

    Article  CAS  PubMed  Google Scholar 

  • Zoschke R, Watkins KP, Miranda RG, Barkan A (2016) The PPR-SMR protein PPR53 enhances the stability and translation of specific chloroplast RNAs in maize. Plant J 85:594–606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We are very grateful to Conny Guha and Uli Tengler for excellent technical assistance. This work was supported by DFG Grant Bi 590/10-2.

Author contributions

KS, CJ, SS, C.CdF-S and IS performed experiments and/or analyzed the data; SB conceived the project, designed and supervised experiments and wrote the article with contributions of all the authors.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stefan Binder.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1. (PDF 655 KB)

Supplementary material 2 (PDF 148 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Stoll, K., Jonietz, C., Schleicher, S. et al. In Arabidopsis thaliana distinct alleles encoding mitochondrial RNA PROCESSING FACTOR 4 support the generation of additional 5′ termini of ccmB transcripts. Plant Mol Biol 93, 659–668 (2017). https://doi.org/10.1007/s11103-017-0591-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-017-0591-y

Keywords

Navigation