, Volume 237, Issue 2, pp 509–515 | Cite as

Biparental inheritance of organelles in Pelargonium: evidence for intergenomic recombination of mitochondrial DNA

  • Janina Apitz
  • Andreas WeiheEmail author
  • Frank Pohlheim
  • Thomas Börner
Original Article


While uniparental transmission of mtDNA is widespread and dominating in eukaryotes leaving mutation as the major source of genotypic diversity, recently, biparental inheritance of mitochondrial genes has been demonstrated in reciprocal crosses of Pelargonium zonale and P. inquinans. The thereby arising heteroplasmy carries the potential for recombination between mtDNAs of different descent, i.e. between the parental mitochondrial genomes. We have analyzed these Pelargonium hybrids for mitochondrial intergenomic recombination events by examining differences in DNA blot hybridization patterns of the mitochondrial genes atp1 and cob. Further investigation of these genes and their flanking regions using nucleotide sequence polymorphisms and PCR revealed DNA segments in the progeny, which contained both P. zonale and P. inquinans sequences suggesting an intergenomic recombination in hybrids of Pelargonium. This turns Pelargonium into an interesting subject for studies of recombination and evolutionary dynamics of mitochondrial genomes.


Biparental inheritance Heteroplasmy Intergenomic recombination Mitochondria Pelargonium Sublimons 






The excellent technical assistance of Cornelia Stock is gratefully acknowledged.

Supplementary material

425_2012_1768_MOESM1_ESM.pdf (2.7 mb)
Supplementary material 1 (PDF 2725 kb)
425_2012_1768_MOESM2_ESM.pdf (2.1 mb)
Supplementary material 2 (PDF 2174 kb)
425_2012_1768_MOESM3_ESM.docx (20 kb)
Supplementary material 3 (DOCX 20 kb)


  1. Akagi H, Shimada H, Fujimura T (1995) High-frequency inter-parental recombination between mitochondrial genomes of rice cybrids. Curr Genet 29:58–65PubMedCrossRefGoogle Scholar
  2. Arimura S, Yamamoto J, Aida GP, Nakazono M, Tsutsumi N (2004) Frequent fusion and fission of plant mitochondria with unequal nucleoid distribution. Proc Natl Acad Sci USA 101:7805–7808PubMedCrossRefGoogle Scholar
  3. Arrieta-Montiel M, Mackenzie S (2011) Plant mitochondrial genomes and recombination. In: Kempken F (ed) Plant mitochondria, advances in plant biology, 1st edn. Springer, New York, pp 65–82CrossRefGoogle Scholar
  4. 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 183:1261–1268PubMedCrossRefGoogle Scholar
  5. Barr CM, Neiman M, Taylor DR (2005) Inheritance and recombination of mitochondrial genomes in plants, fungi and animals. New Phytol 168:39–50PubMedCrossRefGoogle Scholar
  6. Belliard G, Vedel F, Pelletier G (1979) Mitochondrial recombination in cytoplasmic hybrids of Nicotiana tabacum by protoplast fusion. Nature 281:401–403CrossRefGoogle Scholar
  7. Bentley KE, Mandel JR, McCauley DE (2010) Paternal leakage and heteroplasmy of mitochondrial genomes in Silene vulgaris: evidence from experimental crosses. Genetics 185:961–968PubMedCrossRefGoogle Scholar
  8. Birky CW (1995) Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc Natl Acad Sci USA 92:11331–11338PubMedCrossRefGoogle Scholar
  9. Fan W, Lin CS, Potluri P, Procaccio V, Wallace DC (2012) mtDNA lineage analysis of mouse L-cell lines reveals the accumulation of multiple mtDNA mutants and intermolecular recombination. Genes Develop 26:384–394PubMedCrossRefGoogle Scholar
  10. Hagemann R (2004) The sexual inheritance of plant organelles. In: Daniel H, Chase C (eds) Molecular biology and biotechnology of plant organelles, 1st edn. Springer, Dordrecht, pp 93–113CrossRefGoogle Scholar
  11. Janska H, Sarria R, Woloszynska M, Arrieta-Montiel M, Mackenzie SA (1998) Stoichiometric shifts in the common bean mitochondrial genome leading to male sterility and spontaneous reversion to fertility. Plant Cell 10:1163–1180PubMedGoogle Scholar
  12. Jaramillo-Correa JP, Bousquet J (2005) Mitochondrial genome recombination in the zone of contact between two hybridizing conifers. Genetics 171:1951–1962PubMedCrossRefGoogle Scholar
  13. Khanuja SPS, Shasany AK, Darokar MP, Kumar S (1999) Rapid isolation of DNA from dry and fresh samples of plants producing large amounts of secondary metabolites and essential oils. Plant Mol Biol Report 17:1–7CrossRefGoogle Scholar
  14. Lackner LL, Nunnari JM (2009) The molecular mechanism and cellular functions of mitochondrial division. BBA-Mol Basis Dis 1792:1138–1144CrossRefGoogle Scholar
  15. Logan DC (2010) Mitochondrial fusion, division and positioning in plants. Biochem Soc Trans 38:789–795PubMedCrossRefGoogle Scholar
  16. Maréchal A, Brisson N (2010) Recombination and the maintenance of plant organelle genome stability. New Phytol 186:299–317PubMedCrossRefGoogle Scholar
  17. Mogensen HL (1996) The hows and whys of cytoplasmic inheritance in seed plants. Am J Bot 83:383–404CrossRefGoogle Scholar
  18. Parkinson CL, Mower JP, Qiu YL, Shirk AJ, Song K, Young ND, DePamphilis CW, Parker JD (2005) Multiple major increases and decreases in mitochondrial substitution ratesin the plant family Geraniceae. BMC Evol Biol 5:73PubMedCrossRefGoogle Scholar
  19. Pohlheim F (1986) Hybrid variegation in crosses between Pelargonium zonale (L.) l`Herit. Ex Ait. and Pelargonium inquinans (L.) l`Herit. Ex Ait Plant Breed 97:93–96CrossRefGoogle Scholar
  20. Rothenberg M, Hanson MR (1987) Recombination between parental mitochondrial DNA following protoplast fusion can occur in a region which normally does not undergo intragenomic recombination in parental plants. Curr Genet 12:235–240CrossRefGoogle Scholar
  21. Rowlands RT, Turner G (1975) Three-marker extranuclear mitochondrial crosses in Aspergillus nidulans. Mol Genet Genomics 141:69–79CrossRefGoogle Scholar
  22. Saville BJ, Kohli Y, Anderson JB (1998) mtDNA recombination in a natural population. Proc Natl Acad Sci USA 95:1331–1335PubMedCrossRefGoogle Scholar
  23. Sheahan MB, McCurdy DW, Rose RJ (2005) Mitochondria as a connected population: ensuring continuity of the mitochondrial genome during plant cell dedifferentiation through massive mitochondrial fusion. Plant J 44:744–755PubMedCrossRefGoogle Scholar
  24. Small I, Suffolk R, Leaver CJ (1989) Evolution of plant mitochondrial genomes via substoichiometric intermediates. Cell 58:69–76PubMedCrossRefGoogle Scholar
  25. Städler T, Delph LF (2002) Ancient mitochondrial haplotypes and evidence for intragenic recombination in a gynodioecious plant. Proc Natl Acad Sci USA 99:11730–11735PubMedCrossRefGoogle Scholar
  26. Takano H, Onoue K, Kawano S (2010) Mitochondrial fusion and inheritance of the mitochondrial genome. J Plant Res 123:131–138PubMedCrossRefGoogle Scholar
  27. Wagner DB, Dong J, Carlson MR, Yanchu AD (1991) Paternal leakage of mitochondrial DNA in Pinus. Theor Appl Genet 82:510–514CrossRefGoogle Scholar
  28. Weihe A, Apitz J, Salinas A, Pohlheim F, Börner T (2009) Biparental inheritance of plastidial and mitochondrial DNA and hybrid variegation in Pelargonium. Mol Genet Genomics 282:587–593PubMedCrossRefGoogle Scholar
  29. Woloszynska M (2010) Heteroplasmy and stoichiometric complexity of plant mitochondrial genomes—though this be madness, yet there’s method in’t. J Exp Bot 61:657–671PubMedCrossRefGoogle Scholar
  30. Woloszynska M, Kieleczawa J, Ornatowska M, Wozniak M, Janska H (2001) The origin and maintenance of the small repeat in the bean mitochondrial genome. Mol Genet Genomics 265:865–872PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Janina Apitz
    • 1
  • Andreas Weihe
    • 1
    Email author
  • Frank Pohlheim
    • 2
  • Thomas Börner
    • 1
  1. 1.Institut für BiologieHumboldt-Universität zu BerlinBerlinGermany
  2. 2.KleinmachnowGermany

Personalised recommendations