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Paternally expressed imprinted genes associate with hybridization barriers in Capsella

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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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.

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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.

Corresponding author

Correspondence to Claudia Köhler.

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The authors declare no competing interests.

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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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