Skip to main content
SpringerLink
Log in

Transcription of atp1 is influenced by both genomic configuration and nuclear background in the highly rearranged mitochondrial genomes of Silene vulgaris

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

An extraordinary variation in mitochondrial DNA sequence exists in angiosperm Silene vulgaris. The atp1 gene is flanked by very variable regions, as deduced from four completely sequenced mitochondrial genomes of this species. This diversity contributed to a highly variable transcript profile of this gene observed across S. vulgaris populations. We examined the atp1 transcript in the KOV mitochondrial genome and found three 5′ ends, created most likely by the combination of transcription initiation and RNA processing. Most atp1 transcripts terminated about 70 bp upstream of the translation stop codon, which was present in only 10 % of them. Controlled crosses between a KOV mother and a geographically distant pollen donor (Krasnoyarsk, Russia) showed that nuclear background also affected atp1 transcription. The distant pollen donor introduced the factor(s) preventing the formation of a long 2,100 nt-transcript, because this long atp1 transcript reappeared in the progeny from self-crosses. The highly rearranged mitochondrial genomes with a variation in gene flanking regions make S. vulgaris an excellent model for the study of mitochondrial gene expression in plants.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

atp1 :

Gene encoding ATP synthase subunit 1

CMS:

Cytoplasmic male sterility

CR-RT-PCR:

Circularized RNA reverse transcriptase PCR

PEX:

Primer extension

RF:

Restorer of fertility

TAP:

Tobacco alkaline pyrophosphatase

References

  • Allen JO, Fauron CM, Minx P, Roark L, Oddiraju S et al (2007) Comparisons among two fertile and three male-sterile mitochondrial genomes of maize. Genetics 177:1173–1192

    Article  PubMed  CAS  Google Scholar 

  • Bentolila S, Stefanov S (2012) A reevaluation of rice mitochondrial evolution based on the complete sequence of male-fertile and male-sterile mitochondrial genomes. Plant Physiol 158:996–1017

    Article  PubMed  CAS  Google Scholar 

  • Bernasconi G, Antonovics J, Biere A, Charlesworth D, Delph LF et al (2009) Silene as a model system in ecology and evolution. Heredity 103:5–14

    Article  PubMed  CAS  Google Scholar 

  • Binder S, Marchfelder A, Brennicke A (1996) Regulation of gene expression in plant mitochondria. Plant Mol Biol 32:303–314

    Article  PubMed  CAS  Google Scholar 

  • Binder S, Hölzle A, Jonietz C (2011) RNA processing and RNA stability in plant mitochondria. In: Kempken F (ed) Plant mitochondria. Springer, Heidelberg, pp 107–130

    Chapter  Google Scholar 

  • Blavet N, Charif D, Oger-Desfeux C, Marais GAB, Widmer A (2011) Comparative high-throughput transcriptome sequencing and development of SiESTa, the Silene EST annotation database. BMC Genomics 12:376

    Article  PubMed  CAS  Google Scholar 

  • Calixte S, Bonen L (2008) Developmentally-specific transcripts from the ccmFN-rps1 locus in wheat mitochondria. Mol Genet Genomics 280:419–426

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Darracq A, Varré JS, Marechal-Drouard L, Courseaux A, Castric V et al (2011) Structural and content diversity of mitochondrial genome in beet: a comparative genomic analysis. Genome Biol Evol 3:723–736

    Article  PubMed  CAS  Google Scholar 

  • Darwin CR (1877) The different forms of flowers on plants of the same species. Murray, London, pp 98–117

    Book  Google Scholar 

  • Dombrowski S, Brennicke A, Binder S (1997) 3′-Inverted repeats in plant mitochondrial mRNAs are processing signals rather than transcription terminators. EMBO J 16:5069–5076

    Article  PubMed  CAS  Google Scholar 

  • Dombrowski S, Hoffmann M, Guha C, Binder S (1999) Continuous primary sequence requirements in the 18-nucleotide promoter of dicot plant mitochondria. J Biol Chem 274:10094–10099

    Article  PubMed  CAS  Google Scholar 

  • Drouin G, Daoud H, Xia J (2008) Relative rates of synonymous substitutions in the mitochondrial, chloroplast and nuclear genomes of seed plants. Mol Phylogenet Evol 49:827–831

    Article  PubMed  CAS  Google Scholar 

  • Elansary HOM, Muller K, Olson MS, Storchova H (2010) Transcription profiles of mitochondrial genes correlate with mitochondrial DNA haplotypes in a natural population of Silene vulgaris. BMC Plant Biol 10:11

    Article  PubMed  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

    Article  PubMed  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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Gagliardi D, Binder S (2007) Expression of the plant mitochondrial genome. In: Logan D (ed) Plant mitochondria. Blackwell, Ames, pp 50–95

    Chapter  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hanson MR, Bentolila S (2004) Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 16:S154–S169

    Article  PubMed  CAS  Google Scholar 

  • Hazle T, Bonen L (2007) Comparative analysis of sequences preceding protein-coding mitochondrial genes in flowering plants. Mol Biol Evol 24:1101–1112

    Article  PubMed  CAS  Google Scholar 

  • Hess WR, Borner T (1999) Organellar RNA polymerases of higher plants. Int Rev Cytol 190:1–59

    Article  PubMed  CAS  Google Scholar 

  • Holec S, Lange H, Canaday J, Gagliardi D (2008) Coping with cryptic and defective transcripts in plant mitochondria. Biochim Biophys Acta 1779:566–573

    Article  PubMed  CAS  Google Scholar 

  • Houliston GJ, Olson MS (2006) Nonneutral evolution of organelle genes in Silene vulgaris. Genetics 174:1983–1994

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Jonietz C, Forner J, Hildebrandt T, Binder S (2011) RNA PROCESSING FACTOR3 is crucial for the accumulation of mature ccmC transcripts in mitochondria of Arabidopsis accession Columbia. Plant Physiol 157:1430–1439

    Article  PubMed  CAS  Google Scholar 

  • Kühn J, Binder S (2002) RT-PCR analysis of 5′ to 3′ end-ligated mRNAs identifies the extremities of cox2 transcripts in pea mitochondria. Nucleic Acids Res 30:439–446

    Article  PubMed  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

    Article  PubMed  Google Scholar 

  • Lupold DS, Caoile AGFS, Stern DB (1999) The maize mitochondrial cox2 gene has five promoters in two genomic regions, including a complex promoter consisting of seven overlapping units. J Biol Chem 274:3897–3903

    Article  PubMed  CAS  Google Scholar 

  • Mower JP, Sloan DB, Alverson AJ (2012) Plant mitochondrial diversity: the genomics revolution. In: Wendel JF (ed) Plant genome diversity. Springer, Vienna, pp 123–144

    Chapter  Google Scholar 

  • Mulligan RM, Lau GT, Walbot W (1988) Numerous transcription initiation sites exist for the maize mitochondrial genes for subunit 9 of the ATP synthase and subunit 3 of cytochrome oxidase. Proc Natl Acad Sci USA 85:7998–8002

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Olson MS, McCauley DE (2002) Mitochondrial DNA diversity, population structure, and gender association in the gynodioecious plant Silene vulgaris. Evolution 56:253–262

    PubMed  CAS  Google Scholar 

  • Pátek M, Muth G, Wohlleben W (2003) Function of Corynebacterium glutamicum promoters in Escherichia coli, Streptomyces lividans, and Bacillus subtilis. J Biotechnol 104:325–334

    Article  PubMed  Google Scholar 

  • Raczynska KD, Le Ret M, Rurek M, Bonnard G, Augustyniak H, Gualberto JM (2006) Plant mitochondrial genes can be expressed from mRNA lacking stop codons. FEBS Lett 580:5641–5646

    Article  PubMed  CAS  Google Scholar 

  • Rapp WD, Stern DB (1992) A conserved 11 nucleotide sequence contains an essential promoter element of the maize mitochondrial atp1 gene. EMBO J 11:1065–1073

    PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Sloan DB, Alverson AJ, Štorchová H, Palmer JD, Taylor DR (2010) Extensive loss of translational genes in the structurally dynamic mitochondrial genome of the angiosperm Silene latifolia. BMC Evol Biol 10:274

    Article  PubMed  Google Scholar 

  • Sloan DB, Alverson AJ, Chuckalovcak JP, Wu M, McCauley DE, Palmer JD, Taylor DR (2012a) Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLoS Biol 10:e1001241

    Article  PubMed  CAS  Google Scholar 

  • Sloan DB, Keller SR, Berardi AF, Sanderson BJ, Karpovich JF, Taylor DR (2012b) De novo transcriptome assembly and polymorphism detection in the flowering plant Silene vulgaris (Caryophyllaceae). Mol Ecol Resour 12:333–343

    Article  PubMed  CAS  Google Scholar 

  • Sloan DB, Müller K, McCauley DE, Taylor DR, Storchova H (2012c) Intraspecific variation in mitochondrial genome sequence, structure, and gene content in Silene vulgaris, an angiosperm with pervasive cytoplasmic male sterility. New Phytol 196:1228–1239

    Article  PubMed  CAS  Google Scholar 

  • Storchova H, Olson MS (2004) Comparison between mitochondrial and chloroplast DNA variation in the native range of Silene vulgaris. Mol Ecol 13:2909–2919

    Article  PubMed  CAS  Google Scholar 

  • Storchova H, Müller K, Lau S, Olson MS (2012) Mosaic origin of a complex chimeric mitochondrial gene in Silene vulgaris. PLoS One e30401

  • Touzet P, Delph LF (2009) The effect of breeding system on polymorphism in mitochondrial genes of Silene. Genetics 181:631–644

    Article  PubMed  CAS  Google Scholar 

  • Wolfe KH, Li WH, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci 84:9054–9058

    Article  PubMed  CAS  Google Scholar 

  • Zhang QY, Liu YG (2006) Rice mitochondrial genes are transcribed by multiple promoters that are highly diverged. J Integr Plant Biol 48:1473–1477

    Article  CAS  Google Scholar 

  • Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Daniel B. Sloan and Amanda L. Robertson for critical reading of this manuscript, Kateřina Haškovcová and Ludmila Busínská for laboratory and greenhouse assistance. This work was supported by the Grant Agency of the Czech Republic (GAČR 521/09/0261) and the Ministry of Education, Youth and Sports of the Czech Republic (MŠMT Kontakt ME09035).

Author information

Authors and Affiliations

  1. Institute of Experimental Botany, Academy of Sciences of the Czech Republic, Prague, Lysolaje, 16502, Czech Republic

    Karel Müller & Helena Storchova

Authors
  1. Karel Müller
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Helena Storchova
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Helena Storchova.

Electronic supplementary material

Below is the link to the electronic supplementary material.

11103_2013_18_MOESM1_ESM.doc

Supplemental Fig. 1 Primer extension experiment (PEX). A. Two independent PEX reactions showing the start site for a long 2100 nt-atp1transcript. B. Two independent PEX reactions showing the start site for a short 1650 nt-atp1transcript. The sequence is reverse complement relative to the sequences in Fig. 4., translation start codon is located at left. Supplementary material 1 (DOC 38 kb)

Supplementary material 2 (DOCX 162 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Müller, K., Storchova, H. Transcription of atp1 is influenced by both genomic configuration and nuclear background in the highly rearranged mitochondrial genomes of Silene vulgaris . Plant Mol Biol 81, 495–505 (2013). https://doi.org/10.1007/s11103-013-0018-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-013-0018-3

Keywords

Search

Navigation