Advertisement

Plant Molecular Biology

, Volume 81, Issue 4–5, pp 495–505 | Cite as

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

  • Karel Müller
  • Helena Storchova
Article

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.

Keywords

Transcription Mitochondria atp1 Silene vulgaris Crosses 

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

Notes

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).

Supplementary material

11103_2013_18_MOESM1_ESM.doc (38 kb)
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)
11103_2013_18_MOESM2_ESM.docx (162 kb)
Supplementary material 2 (DOCX 162 kb)

References

  1. 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 177:1173–1192PubMedCrossRefGoogle Scholar
  2. 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 158:996–1017PubMedCrossRefGoogle Scholar
  3. Bernasconi G, Antonovics J, Biere A, Charlesworth D, Delph LF et al (2009) Silene as a model system in ecology and evolution. Heredity 103:5–14PubMedCrossRefGoogle Scholar
  4. Binder S, Marchfelder A, Brennicke A (1996) Regulation of gene expression in plant mitochondria. Plant Mol Biol 32:303–314PubMedCrossRefGoogle Scholar
  5. Binder S, Hölzle A, Jonietz C (2011) RNA processing and RNA stability in plant mitochondria. In: Kempken F (ed) Plant mitochondria. Springer, Heidelberg, pp 107–130CrossRefGoogle Scholar
  6. 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 12:376PubMedCrossRefGoogle Scholar
  7. Calixte S, Bonen L (2008) Developmentally-specific transcripts from the ccmFN-rps1 locus in wheat mitochondria. Mol Genet Genomics 280:419–426PubMedCrossRefGoogle Scholar
  8. Covello PS, Gray MW (1991) Sequence analysis of wheat mitochondrial transcripts capped in vitro - definitive identification of transcription initiation sites. Curr Genet 20:245–251PubMedCrossRefGoogle Scholar
  9. 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 3:723–736PubMedCrossRefGoogle Scholar
  10. Darwin CR (1877) The different forms of flowers on plants of the same species. Murray, London, pp 98–117CrossRefGoogle Scholar
  11. Dombrowski S, Brennicke A, Binder S (1997) 3′-Inverted repeats in plant mitochondrial mRNAs are processing signals rather than transcription terminators. EMBO J 16:5069–5076PubMedCrossRefGoogle Scholar
  12. 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 274:10094–10099PubMedCrossRefGoogle Scholar
  13. 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 49:827–831PubMedCrossRefGoogle Scholar
  14. 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 10:11PubMedCrossRefGoogle Scholar
  15. 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 33:4673–4682PubMedCrossRefGoogle Scholar
  16. 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 35:3676–3692PubMedCrossRefGoogle Scholar
  17. 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 148:1106–1116PubMedCrossRefGoogle Scholar
  18. Gagliardi D, Binder S (2007) Expression of the plant mitochondrial genome. In: Logan D (ed) Plant mitochondria. Blackwell, Ames, pp 50–95CrossRefGoogle Scholar
  19. 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 31:5907–5916PubMedCrossRefGoogle Scholar
  20. Hanson MR, Bentolila S (2004) Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 16:S154–S169PubMedCrossRefGoogle Scholar
  21. Hazle T, Bonen L (2007) Comparative analysis of sequences preceding protein-coding mitochondrial genes in flowering plants. Mol Biol Evol 24:1101–1112PubMedCrossRefGoogle Scholar
  22. Hess WR, Borner T (1999) Organellar RNA polymerases of higher plants. Int Rev Cytol 190:1–59PubMedCrossRefGoogle Scholar
  23. Holec S, Lange H, Canaday J, Gagliardi D (2008) Coping with cryptic and defective transcripts in plant mitochondria. Biochim Biophys Acta 1779:566–573PubMedCrossRefGoogle Scholar
  24. Houliston GJ, Olson MS (2006) Nonneutral evolution of organelle genes in Silene vulgaris. Genetics 174:1983–1994PubMedCrossRefGoogle Scholar
  25. 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 22:443–453PubMedCrossRefGoogle Scholar
  26. 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 157:1430–1439PubMedCrossRefGoogle Scholar
  27. 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 30:439–446PubMedCrossRefGoogle Scholar
  28. Kühn K, Weihe A, Börner T (2005) Multiple promoters are a common feature of mitochondrial genes in Arabidopsis. Nucleic Acids Res 33:337–346PubMedCrossRefGoogle Scholar
  29. 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 274:3897–3903PubMedCrossRefGoogle Scholar
  30. Mower JP, Sloan DB, Alverson AJ (2012) Plant mitochondrial diversity: the genomics revolution. In: Wendel JF (ed) Plant genome diversity. Springer, Vienna, pp 123–144CrossRefGoogle Scholar
  31. 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 85:7998–8002PubMedCrossRefGoogle Scholar
  32. 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 268:434–445PubMedCrossRefGoogle Scholar
  33. Olson MS, McCauley DE (2002) Mitochondrial DNA diversity, population structure, and gender association in the gynodioecious plant Silene vulgaris. Evolution 56:253–262PubMedGoogle Scholar
  34. Pátek M, Muth G, Wohlleben W (2003) Function of Corynebacterium glutamicum promoters in Escherichia coli, Streptomyces lividans, and Bacillus subtilis. J Biotechnol 104:325–334PubMedCrossRefGoogle Scholar
  35. 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 580:5641–5646PubMedCrossRefGoogle Scholar
  36. Rapp WD, Stern DB (1992) A conserved 11 nucleotide sequence contains an essential promoter element of the maize mitochondrial atp1 gene. EMBO J 11:1065–1073PubMedGoogle Scholar
  37. Schmitz-Linneweber C, Small I (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends in Plant Sci 13:663–670CrossRefGoogle Scholar
  38. 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 10:274PubMedCrossRefGoogle Scholar
  39. 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:e1001241PubMedCrossRefGoogle Scholar
  40. 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 12:333–343PubMedCrossRefGoogle Scholar
  41. 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 196:1228–1239PubMedCrossRefGoogle Scholar
  42. Storchova H, Olson MS (2004) Comparison between mitochondrial and chloroplast DNA variation in the native range of Silene vulgaris. Mol Ecol 13:2909–2919PubMedCrossRefGoogle Scholar
  43. Storchova H, Müller K, Lau S, Olson MS (2012) Mosaic origin of a complex chimeric mitochondrial gene in Silene vulgaris. PLoS One e30401Google Scholar
  44. Touzet P, Delph LF (2009) The effect of breeding system on polymorphism in mitochondrial genes of Silene. Genetics 181:631–644PubMedCrossRefGoogle Scholar
  45. Wolfe KH, Li WH, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci 84:9054–9058PubMedCrossRefGoogle Scholar
  46. Zhang QY, Liu YG (2006) Rice mitochondrial genes are transcribed by multiple promoters that are highly diverged. J Integr Plant Biol 48:1473–1477CrossRefGoogle Scholar
  47. Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Institute of Experimental BotanyAcademy of Sciences of the Czech RepublicPrague, LysolajeCzech Republic

Personalised recommendations