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Paternally expressed imprinted genes associate with hybridization barriers in Capsella

Nature Plants volume 4, pages 352–357 (2018)Cite this article

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Abstract

Hybrid seed lethality is a widespread type of reproductive barrier among angiosperm taxa1,2 that contributes to species divergence by preventing gene flow between natural populations3,4. Besides its ecological importance, it is an important obstacle to plant breeding strategies5. Hybrid seed lethality is mostly due to a failure of the nourishing endosperm tissue, resulting in embryo arrest3,6,7. The cause of this failure is a parental dosage imbalance in the endosperm that can be a consequence of either differences in parental ploidy levels or differences in the 'effective ploidy', also known as the endosperm balance number (EBN)8,9. Hybrid seed defects exhibit a parent-of-origin pattern3,6,7, suggesting that differences in number or expression strength of parent-of-origin-specific imprinted genes underpin, as the primary or the secondary cause, the molecular basis of the EBN7,10. Here, we have tested this concept in the genus Capsella and show that the effective ploidy of three Capsella species correlates with the number and expression level of paternally expressed genes (PEGs). Importantly, the number of PEGs and the effective ploidy decrease with the selfing history of a species: the obligate outbreeder Capsella grandiflora had the highest effective ploidy, followed by the recent selfer Capsella rubella and the ancient selfer Capsella orientalis. PEGs were associated with the presence of transposable elements and their silencing mark, DNA methylation in CHH context (where H denotes any base except C). This suggests that transposable elements have driven the imprintome divergence between Capsella species. Together, we propose that variation in transposable element insertions, the resulting differences in PEG number and divergence in their expression level form one component of the effective ploidy variation between species of different breeding system histories, and, as a consequence, allow the establishment of endosperm-based hybridization barriers.

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Fig. 1: Hybrid seed lethality between Capsella species is due to endosperm failure.
Fig. 2: Species-specific number and expression of paternally expressed imprinted genes is an indicator for endosperm effective ploidy.
Fig. 3: Species-specific PEGs exhibit species-specific CHH methylation.

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References

  1. Ramsey, J. & Schemske, D. W. Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annu. Rev. Ecol. Syst. 29, 467–501 (1998).

    Article  Google Scholar 

  2. Lafon-Placette, C. & Köhler, C. Endosperm-based postzygotic hybridization barriers: developmental mechanisms and evolutionary drivers. Mol. Ecol. 25, 2620–2629 (2016).

    Article  PubMed  Google Scholar 

  3. Lafon-Placette, C. et al. Endosperm-based hybridization barriers explain the pattern of gene flow between Arabidopsis lyrata and Arabidopsis arenosa in Central Europe. Proc. Natl Acad. Sci. USA 114, E1027–E1035 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. Hämälä, T., Mattila, T. M., Leinonen, P. H., Kuittinen, H. & Savolainen, O. Role of seed germination in adaptation and reproductive isolation in Arabidopsis lyrata. Mol. Ecol. 26, 3484–3496 (2017).

    Article  PubMed  CAS  Google Scholar 

  5. Sahijram, L. & Rao, B. M. in Plant Biology and Biotechnology 363–384 (Springer, New Delhi, 2015).

  6. Rebernig, C. A., Lafon-Placette, C., Hatorangan, M. R., Slotte, T. & Köhler, C. Non-reciprocal interspecies hybridization barriers in the Capsella Genus are established in the endosperm. PLoS Genet. 11, e1005295 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Florez-Rueda, A. M. et al. Genomic imprinting in the endosperm is systematically perturbed in abortive hybrid tomato seeds. Mol. Biol. Evol. 33, 2935–2946 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Johnston, S. A. & Hanneman, R. E. Manipulations of endosperm balance number overcome crossing barriers between diploid Solanum species. Science 217, 446–448 (1982).

    Article  PubMed  CAS  Google Scholar 

  9. Birchler, J. A. Interploidy hybridization barrier of endosperm as a dosage interaction. Front. Plant Sci. 5, 281 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  10. Wolff, P., Jiang, H., Wang, G., Santos-González, J. & Köhler, C. Paternally expressed imprinted genes establish postzygotic hybridization barriers in Arabidopsis thaliana. eLife Sci. 4, e10074 (2015).

    Article  Google Scholar 

  11. Kirkbride, R. C. et al. An epigenetic role for disrupted paternal gene expression in postzygotic seed abortion in Arabidopsis interspecific hybrids. Mol. Plant 8, 1766–1775 (2015).

    Article  PubMed  CAS  Google Scholar 

  12. Douglas, G. M. et al. Hybrid origins and the earliest stages of diploidization in the highly successful recent polyploid Capsella bursa-pastoris. Proc. Natl Acad. Sci. 112, 2806–2811 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Sicard, A. et al. Divergent sorting of a balanced ancestral polymorphism underlies the establishment of gene-flow barriers in Capsella. Nat. Commun. 6, 7960 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Scott, R. J., Spielman, M., Bailey, J. & Dickinson, H. G. Parent-of-origin effects on seed development in Arabidopsis thaliana. Development 125, 3329–3341 (1998).

    PubMed  CAS  Google Scholar 

  15. Hatorangan, M. R., Laenen, B., Steige, K., Slotte, T. & Köhler, C. Rapid evolution of genomic imprinting in two species of the Brassicaceae. Plant Cell 28, 1815–1827 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Klosinska, M., Picard, C. L. & Gehring, M. Conserved imprinting associated with unique epigenetic signatures in the Arabidopsis genus. Nat. Plants 2, 16145 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Varrault, A. et al. Zac1 regulates an imprinted gene network critically involved in the control of embryonic growth. Dev. Cell 11, 711–722 (2006).

    Article  PubMed  CAS  Google Scholar 

  18. Rodrigues, J. A. & Zilberman, D. Evolution and function of genomic imprinting in plants. Genes Dev. 29, 2517–2531 (2015).

    PubMed  PubMed Central  CAS  Google Scholar 

  19. Ågren, J. A. et al. Mating system shifts and transposable element evolution in the plant genus Capsella. BMC Genom. 15, 602 (2014).

    Article  Google Scholar 

  20. Boutin, T. S., Le Rouzic, A. & Capy, P. How does selfing affect the dynamics of selfish transposable elements? Mob. DNA 3, 5 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. St. Onge, K. R., Källman, T., Slotte, T., Lascoux, M. & Palmé, A. E. Contrasting demographic history and population structure in Capsella rubella and Capsella grandiflora, two closely related species with different mating systems. Mol. Ecol. 20, 3306–3320 (2011).

    Article  Google Scholar 

  22. Hurka, H., Friesen, N., German, D. A., Franzke, A. & Neuffer, B. ‘Missing link’ species Capsella orientalis and Capsella thracica elucidate evolution of model plant genus Capsella (Brassicaceae). Mol. Ecol. 21, 1223–1238 (2012).

    Article  PubMed  Google Scholar 

  23. Seymour, D. K., Koenig, D., Hagmann, J., Becker, C. & Weigel, D. Evolution of DNA methylation patterns in the Brassicaceae is driven by differences in genome organization. PLoS Genet. 10, e1004785 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Krueger, F. & Andrews, S. R. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics 27, 1571–1572 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Ramírez, F., Dündar, F., Diehl, S., Grüning, B. A. & Manke, T. deepTools: a flexible platform for exploring deep-sequencing data. Nucl. Acids Res. 42, 187–191 (2014).

    Article  CAS  Google Scholar 

  26. Bewick, A. J. et al. FASTmC: a suite of predictive models for nonreference-based estimations of DNA methylation. G3 (Bethesda) 6, 447–452 (2015).

    Article  CAS  Google Scholar 

  27. Anders, S., Pyl, P. T. & Huber, W. HTSeq-150; a Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166–169 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Belmonte, M. F. et al. Comprehensive developmental profiles of gene activity in regions and subregions of the Arabidopsis seed. Proc. Natl Acad. Sci. 110, 435–444 (2013).

    Article  Google Scholar 

  29. Anders, S. & Huber, W. Differential expression analysis for sequence count data. Genome Biol. 11, R106 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

Sequencing was performed by the SNP&SEQ Technology Platform, Science for Life Laboratory at Uppsala University, a national infrastructure supported by the Swedish Research Council (VRRFI) and the Knut and Alice Wallenberg Foundation. This research was supported by a European Research Council Starting Independent Researcher grant (to C.K.). C.L.-P. was supported by a grant from the Nilsson-Ehle Foundation.

Author information

Author notes

  1. Clément Lafon-Placette

    Present address: Department of Botany, Charles University, Prague, Czech Republic

  2. Kim A. Steige

    Present address: Institute of Botany, Biocenter, University of Cologne, Cologne, Germany

  3. These authors contributed equally: Clément Lafon-Placette and Marcelinus R. Hatorangan.

Authors and Affiliations

  1. Department of Plant Biology, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, Uppsala, Sweden

    Clément Lafon-Placette, Marcelinus R. Hatorangan & Claudia Köhler

  2. Department of Ecology, Environment and Plant Sciences, Science for Life Laboratory, Stockholm University, Stockholm, Sweden

    Kim A. Steige & Tanja Slotte

  3. Department of Ecology and Genetics, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden

    Amandine Cornille & Martin Lascoux

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Contributions

C.L.-P., M.R.H. and C.K. designed research. C.L.-P. and M.R.H. performed the experiments. A.C., K.A.S., T.S. and M.L. characterized the plant material. C.L.-P., M.R.H. and C.K. analysed the data. C.L.-P., M.R.H. and C.K. wrote the paper.

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Correspondence to Claudia Köhler.

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Supplementary information

Supplementary Information

Supplementary Figures 1–8, Supplementary Table 1, Supplementary Table 3–5 and Supplementary Table 7

Reporting Summary

Supplementary Table 2

List of imprinted genes in C. grandiflora, C. rubella and C. orientalis. Cr, C. rubella; Cg, C. grandiflora; Co, C. orientalis; M, maternal allele count; P, paternal allele count; Chi2pval, Chi-square test corrected P value; MEG, maternally expressed gene; PEG, paternally expressed gene

Supplementary Table 6

Raw and normalized read counts for reciprocal crosses CgA × CgB, CrA × CrB and CoA × CoB. Genes were classified as ‘passed’ if, in at least one library of the CgA × CgB reciprocal crosses and in one library of the Cr A × Cr B reciprocal crosses, the expression level was equal or higher than 80% of the expression level in Cr or Cg seeds, respectively

Supplementary Table 8

Calculation of false discovery rate (FDR) of detecting non-endosperm-preferred genes prior and post filtering. The FDR of detecting non-endosperm-preferred genes prior and post filtering was calculated based on the 50 most highly expressed genes in seed coat and embryo samples of heart stage A. thaliana seeds

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Lafon-Placette, C., Hatorangan, M.R., Steige, K.A. et al. Paternally expressed imprinted genes associate with hybridization barriers in Capsella. Nature Plants 4, 352–357 (2018). https://doi.org/10.1038/s41477-018-0161-6

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