Plant Reproduction

, Volume 26, Issue 4, pp 309–315 | Cite as

On the origin and evolution of apomixis in Boechera

  • John T. Lovell
  • Olawale M. Aliyu
  • Martin Mau
  • M. Eric Schranz
  • Marcus Koch
  • Christiane Kiefer
  • Bao-Hua Song
  • Thomas Mitchell-Olds
  • Timothy F. SharbelEmail author
Original Article


The genetic mechanisms causing seed development by gametophytic apomixis in plants are predominantly unknown. As apomixis is consistently associated with hybridity and polyploidy, these confounding factors may either (a) be the underlying mechanism for the expression of apomixis, or (b) obscure the genetic factors which cause apomixis. To distinguish between these hypotheses, we analyzed the population genetic patterns of diploid and triploid apomictic lineages and their sexual progenitors in the genus Boechera (Brassicaceae). We find that while triploid apomixis is associated with hybridization, the majority of diploid apomictic lineages are likely the product of intra-specific crosses. We then show that these diploid apomicts are more likely to sire triploid apomictic lineages than conspecific sexuals. Combined with flow cytometric seed screen phenotyping for male and female components of apomixis, our analyses demonstrate that hybridization is an indirect correlate of apomixis in Boechera.


Boechera Apomixis Apomeiosis Hybridization Polyploidy 



We thank J. M. Corral and J. Beck for insightful discussions. This work was partially funded by the Apomixis Research Group, using basic level funding provided by the IPK. Additional funding comes from DFG Grant #SH337/7-1 to TFS and a μMorph training Grant to JTL. TMO was supported by NIH Grant R01-GM086496.

Supplementary material

497_2013_218_MOESM1_ESM.pdf (2.9 mb)
Supplementary material 1 (PDF 2978 kb)


  1. Alexander PJ, Windham MD, Beck JB, Al-Shehbaz IA, Allphin L, Bailey CD (2013) Molecular phylogenetics and taxonomy of the genus Boechera and related genera (Brassicaceae: Boechereae). Syst Bot 38(1):192–209CrossRefGoogle Scholar
  2. Aliyu OM, Schranz ME, Sharbel TF (2010) Quantitative variation for apomictic reproduction in the genus Boechera (Brassicaceae). Am J Bot 97(10):1719–1731CrossRefPubMedGoogle Scholar
  3. Al-Shehbaz IA (2003) Transfer of most North American species of Arabis to Boechera (Brassicaceae). Novon 13(4):381–391CrossRefGoogle Scholar
  4. Asker S, Jerling L (1992) Apomixis in plants. CRC Press, Boca RatonGoogle Scholar
  5. Beck JB, Alexander PJ, Allphin L, Al-Shehbaz IA, Rushworth C, Bailey CD, Windham MD (2012) Does hybridization drive the transition to asexuality in diploid Boechera? Evolution 66(4):985–995CrossRefPubMedGoogle Scholar
  6. Bicknell RA, Koltunow AM (2004) Understanding apomixis: recent advances and remaining conundrums. Plant Cell 16(Suppl):S228–S245PubMedGoogle Scholar
  7. Böcher TW (1951) Cytological and embryological studies in the amphi-apomictic Arabis holboellii complex. Det Kongelige Danske Videnskabernes Selskab 6(7):1–59Google Scholar
  8. Bruvo R, Michiels NK, D’Souza TG, Schulenburg H (2004) A simple method for the calculation of microsatellite genotype distances irrespective of ploidy level. Mol Ecol 13(7):2101–2106CrossRefPubMedGoogle Scholar
  9. Carman JG (1997) Asynchronous expression of duplicate genes in angiosperms may cause apomixis, bispory, tetraspory, and polyembryony. Biol J Linn Soc 61(1):51–94CrossRefGoogle Scholar
  10. Comai L, Madlung A, Josefsson C, Tyagi A (2003) Do the different parental ‘heteromes’ cause genomic shock in newly formed allopolyploids? Philos Trans R Soc Lond B 358(1434):1149–1155CrossRefGoogle Scholar
  11. Cosendai A-C, Rodewald J, Hörandl E (2011) Origin and distribution of autopolyploids via apomixis in the alpine species Ranunculus kuepferi (Ranunculaceae). Taxon 60(2):355–364Google Scholar
  12. Dobeš C, Mitchell-Olds T, Koch M (2004a) Extensive chloroplast haplotype variation indicates Pleistocene hybridization and radiation of North American Arabis drummondii, A. xdivericarpa, and A. holboellii (Brassicaceae). Mol Ecol 13(2):349–370Google Scholar
  13. Dobeš C, Mitchell-Olds T, Koch M (2004b) Intraspecific diversification in North American Boechera stricta (=Arabis drummondii), Boechera x divaricarpa, and Boechera holboellii (Brassicaceae) inferred from nuclear and chloroplast molecular markers–an integrative approach. Am J Bot 91(12):2087–2101CrossRefPubMedGoogle Scholar
  14. Dobeš C, Sharbel TF, Koch M (2007) Towards understanding the dynamics of hybridization and apomixis in the evolution of the genus Boechera (Brassicaceae). Syst Biodivers 5(3):321–331CrossRefGoogle Scholar
  15. Hopf FA, Michod RE, Sanderson MJ (1988) The effect of the reproductive system on mutation load. Theor Popul Biol 33(3):243–265CrossRefPubMedGoogle Scholar
  16. Hörandl E, Hojsgaard D (2012) The evolution of apomixis in angiosperms: a reappraisal. Plant Biosyst 146(3):681–693Google Scholar
  17. Kantama L, Sharbel TF, Schranz ME, Mitchell-Olds T, de Vries S, de Jong H (2007) Diploid apomicts of the Boechera holboellii complex display large-scale chromosome substitutions and aberrant chromosomes. Proc Natl Acad Sci USA 104(35):14026–14031CrossRefPubMedGoogle Scholar
  18. Karron JD, Ivey CT, Mitchell RJ, Whitehead MR, Peakall R, Case AL (2012) New perspectives on the evolution of plant mating systems. Ann Bot 109(3):493–503CrossRefPubMedGoogle Scholar
  19. Kiefer C, Koch MA (2012) A continental-wide perspective: the genepool of nuclear encoded ribosomal DNA and single-copy gene sequences in North American Boechera (Brassicaceae). PLoS One 7(5):e36491CrossRefPubMedGoogle Scholar
  20. Kiefer C, Dobeš C, Koch MA (2009a) Boechera or not? Phylogeny and phylogeography of eastern North American Boechera species (Brassicaceae). Taxon 58(4):1109–1121Google Scholar
  21. Kiefer C, Dobeš C, Sharbel TF, Koch MA (2009b) Phylogeographic structure of the chloroplast DNA gene pool in North American Boechera—a genus and continental-wide perspective. Mol Phylogenet Evol 52(2):303–311CrossRefPubMedGoogle Scholar
  22. Kondrashov AS (1985) Deleterious mutations as an evolutionary factor. II. Facultative apomixis and selfing. Genetics 111:635–653PubMedGoogle Scholar
  23. Madlung A, Masuelli RW, Watson B, Reynolds SH, Davison J, Comai L (2002) Remodeling of DNA methylation and phenotypic and transcriptional changes in synthetic Arabidopsis allotetraploids. Plant Physiol 129(2):733–746CrossRefPubMedGoogle Scholar
  24. Matzk F, Meister A, Schubert I (2000) An efficient screen for reproductive pathways using mature seeds of monocots and dicots. Plant J 21(1):97–108CrossRefPubMedGoogle Scholar
  25. Mogie M (1986) On the relationship between asexual reproduction and polyploidy. J Theor Biol 122:493–498CrossRefGoogle Scholar
  26. Mogie M (1992) The evolution of asexual reproduction in plants. Chapman & Hall, LondonGoogle Scholar
  27. Nelson-Jones B, Briggs D, Smith G (2002) The origin of intermediate species of the genus Sorbus. Theor Appl Genet 105(6–7):953–963PubMedGoogle Scholar
  28. Paun O, Hörandl E (2006) Evolution of hypervariable microsatellites in apomictic polyploid lineages of Ranunculus carpaticola: directional bias at dinucleotide loci. Genetics 174(1):387–398CrossRefPubMedGoogle Scholar
  29. Pongratz N, Sharbel TF, Beukeboom LW, Michiels NK (1997) Allozyme variability in sexual and parthenogenetic freshwater planarians: evidence for polyphyletic origin of parthenogenetic lineages through hybridization with coexisting sexuals. Heredity 81:38–47CrossRefGoogle Scholar
  30. R Development Core Team (2009) R: a language and environment for statistical computing. R foundation for statistical computing. Vienna, Austria (
  31. Roy BA (1995) The breeding systems of six species of Arabis (Brassicaceae). Am J Bot 82(7):869–877CrossRefGoogle Scholar
  32. Rushworth CA, Song BH, Lee CR, Mitchell-Olds T (2011) Boechera, a model system for ecological genomics. Mol Ecol 20(23):4843–4857CrossRefPubMedGoogle Scholar
  33. Schranz ME, Dobeš C, Koch MA, Mitchell-Olds T (2005) Sexual reproduction, hybridization, apomixis, and polyploidization in the genus Boechera (Brassicaceae). Am J Bot 92(11):1797–1810CrossRefPubMedGoogle Scholar
  34. Schranz ME, Kantama L, de Jong H, Mitchell-Olds T (2006) Asexual reproduction in a close relative of Arabidopsis: a genetic investigation of apomixis in Boechera (Brassicaceae). New Phytol 171(2):425–438CrossRefPubMedGoogle Scholar
  35. Sharbel TF, Voigt ML, Corral JM, Galla G, Kumlehn J, Klukas C, Schreiber F, Vogel H, Rotter B (2010) Apomictic and sexual ovules of Boechera display heterochronic global gene expression patterns. Plant Cell 22(3):655–671CrossRefPubMedGoogle Scholar
  36. Song BH, Mitchell-Olds T (2007) High genetic diversity and population differentiation in Boechera fecunda, a rare relative of Arabidopsis. Mol Ecol 16(19):4079–4088CrossRefPubMedGoogle Scholar
  37. van Dijk PJ, Vijverberg K (2005) The significance of apomixis in the evolution of the angiosperms: a reappraisal. In: Bakker FT, Chatrou LW, Gravendeel B, Pelser PB (eds) Plant species-level systematics: new perspectives on pattern & process, vol 143. Regnum Vegetabile. A R G Gantner Verlag K G, Koenigstein, pp 101–116Google Scholar
  38. Wang J, Tian L, Madlung A, Lee HS, Chen M, Lee JJ, Watson B, Kagochi T, Comai L, Chen ZJ (2004) Stochastic and epigenetic changes of gene expression in Arabidopsis polyploids. Genetics 167(4):1961–1973CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • John T. Lovell
    • 1
    • 2
  • Olawale M. Aliyu
    • 1
  • Martin Mau
    • 1
  • M. Eric Schranz
    • 3
  • Marcus Koch
    • 4
  • Christiane Kiefer
    • 5
  • Bao-Hua Song
    • 6
  • Thomas Mitchell-Olds
    • 7
  • Timothy F. Sharbel
    • 1
    Email author
  1. 1.Apomixis Research GroupLeibniz Institut für Pflanzengenetik und Kulturpflanzenforschung (IPK)GaterslebenGermany
  2. 2.Graduate Degree Program in EcologyColorado State UniversityFt. CollinsUSA
  3. 3.Biosystematics Group, Plant SciencesWageningen UniversityWageningenThe Netherlands
  4. 4.Department of Biodiversity and Plant Systematics, Centre for Organismal Studies HeidelbergHeidelberg UniversityHeidelbergGermany
  5. 5.Department of Plant Developmental BiologyMax Planck Institute for Plant Breeding ResearchCologneGermany
  6. 6.Department of BiologyUniversity of North CarolinaCharlotteUSA
  7. 7.Department of Biology, Institute for Genome Sciences and PolicyDuke UniversityDurhamUSA

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