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Bypassing genomic imprinting allows seed development

Abstract

In developing progeny of mammals the two parental genomes are differentially expressed according to imprinting marks, and embryos with only a uniparental genetic contribution die1,2,3. Gene expression that is dependent on the parent of origin has also been observed in the offspring of flowering plants, and mutations in the imprinting machinery lead to embryonic lethality, primarily affecting the development of the endosperm—a structure in the seed that nourishes the embryo, analogous to the function of the mammalian placenta4. Here we have generated Arabidopsis thaliana seeds in which the endosperm is of uniparental, that is, maternal, origin. We demonstrate that imprinting in developing seeds can be bypassed and viable albeit smaller seedlings can develop from seeds lacking a paternal contribution to the endosperm. Bypassing is only possible if the mother is mutant for any of the FIS-class genes, which encode Polycomb group chromatin-modifying factors. Thus, these data provide functional evidence that the action of the FIS complex balances the contribution of the paternal genome. As flowering plants have evolved a special reproduction system with a parallel fusion of two female with two male gametes, our findings support the hypothesis that only with the evolution of double fertilization did the action of the FIS genes become a requirement for seed development. Furthermore, our data argue for a gametophytic origin of endosperm in flowering plants, thereby supporting a hypothesis raised in 1900 by Eduard Strasburger.

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Figure 1: Rescue of seed abortion in mea -/-  ×  cdka;1–yfp +/- crosses.
Figure 2: The small mea -/-  ×  cdka;1 +/- seeds develop with a uniparental diploid endosperm.
Figure 3: Quantitative real-time PCR monitoring PHE1 expression in mea-/-×  cdka;1+/- seeds.

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Acknowledgements

The authors thank F. Berger, E. Erkenbrack, C. Köhler, M. Koornneef and J. Larkin for critical reading and helpful comments on the manuscript. We are grateful to F. Berger for providing mutant and marker lines used in this study. We thank A. Chaudhury for the homozygous mea (fis1) mutant line. For the in situ hybridization analyses, we thank B. Sæther at NARC, a part of the Norwegian Research Council National Programme for Research in Functional Genomics (FUGE). We thank D. Falkenhahn for embedding and thick-sectioning for the laser dissection microscopy. We are grateful to H. Barbier and M. Reymond for their help with statistical analyses. M.K.N. and N.D. are fellows of the International Max Planck Research School (IMPRS). P.E.G. and R.S. were supported by a grant from the Norwegian Research Council. This work was supported by a grant of the Volkswagen-Stiftung to A.S.

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Nowack, M., Shirzadi, R., Dissmeyer, N. et al. Bypassing genomic imprinting allows seed development. Nature 447, 312–315 (2007). https://doi.org/10.1038/nature05770

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