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Bypassing genomic imprinting allows seed development

Nature volume 447, pages 312–315 (2007)Cite this article

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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References

  1. Barton, S. C., Surani, M. A. & Norris, M. L. Role of paternal and maternal genomes in mouse development. Nature 311, 374– 376 (1984)

    Article  ADS  CAS  Google Scholar 

  2. Surani, M. A., Barton, S. C. & Norris, M. L. Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 308, 548– 550 (1984)

    Article  ADS  CAS  Google Scholar 

  3. McGrath, J. & Solter, D. Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 37, 179– 183 (1984)

    Article  CAS  Google Scholar 

  4. Berger, F. Imprinting—a green variation. Science 303, 483– 485 (2004)

    Article  CAS  Google Scholar 

  5. 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)

    CAS  PubMed  Google Scholar 

  6. Lin, B.-Y. Association of endosperm reduction with parental imprinting in maize. Genetics 100, 475– 486 (1982)

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Lin, B.-Y. Ploidy barrier to endosperm development in maize. Genetics 107, 103– 115 (1984)

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Haig, D. & Westoby, M. Parent-specific gene expression and the triploid endosperm. Am. Nat. 134, 147– 155 (1989)

    Article  Google Scholar 

  9. Haig, D. & Westoby, M. Genomic imprinting in endosperm: its effects on seed development in crosses between species and between different ploidies of the same species, and its implications for the evolution of apomixis. Phil. Trans. R. Soc. Lond. B 333, 1– 13 (1991)

    Article  ADS  Google Scholar 

  10. Kohler, C. & Grossniklaus, U. Seed development and genomic imprinting in plants. Prog. Mol. Subcell. Biol. 38, 237– 262 (2005)

    Article  Google Scholar 

  11. Guitton, A. E. & Berger, F. Control of reproduction by Polycomb group complexes in animals and plants. Int. J. Dev. Biol. 49, 707– 716 (2005)

    Article  CAS  Google Scholar 

  12. Autran, D., Huanca-Mamani, W. & Vielle-Calzada, J. P. Genomic imprinting in plants: the epigenetic version of an Oedipus complex. Curr. Opin. Plant Biol. 8, 19– 25 (2005)

    Article  CAS  Google Scholar 

  13. Gehring, M., Choi, Y. & Fischer, R. L. Imprinting and seed development. Plant Cell 16 (Suppl). S203– S213 (2004)

    Article  CAS  Google Scholar 

  14. Scott, R. J. & Spielman, M. Genomic imprinting in plants and mammals: how life history constrains convergence. Cytogenet. Genome Res. 113, 53– 67 (2006)

    Article  CAS  Google Scholar 

  15. Jullien, P. E., Katz, A., Oliva, M., Ohad, N. & Berger, F. Polycomb group complexes self-regulate imprinting of the Polycomb group gene MEDEA in Arabidopsis. Curr. Biol. 16, 486– 492 (2006)

    Article  CAS  Google Scholar 

  16. Baroux, C., Gagliardini, V., Page, D. R. & Grossniklaus, U. Dynamic regulatory interactions of Polycomb group genes: MEDEA autoregulation is required for imprinted gene expression in Arabidopsis. Genes Dev. 20, 1081– 1086 (2006)

    Article  CAS  Google Scholar 

  17. Gehring, M. et al. DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation. Cell 124, 495– 506 (2006)

    Article  CAS  Google Scholar 

  18. Chaudhury, A. M. et al. Fertilization-independent seed development in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 94, 4223– 4228 (1997)

    Article  ADS  CAS  Google Scholar 

  19. Grossniklaus, U., Vielle-Calzada, J. P., Hoeppner, M. A. & Gagliano, W. B. Maternal control of embryogenesis by MEDEA, a polycomb group gene in Arabidopsis. Science 280, 446– 450 (1998)

    Article  ADS  CAS  Google Scholar 

  20. Ohad, N. et al. A mutation that allows endosperm development without fertilization. Proc. Natl Acad. Sci. USA 93, 5319– 5324 (1996)

    Article  ADS  CAS  Google Scholar 

  21. Kiyosue, T. et al. Control of fertilization-independent endosperm development by the MEDEA Polycomb gene in Arabidopsis. Proc. Natl Acad. Sci. USA 96, 4186– 4191 (1999)

    Article  ADS  CAS  Google Scholar 

  22. Faure, J. E., Mogensen, H. L., Dumas, C., Lorz, H. & Kranz, E. Karyogamy after electrofusion of single egg and sperm cell protoplasts from maize: cytological evidence and time course. Plant Cell 5, 747– 755 (1993)

    Article  Google Scholar 

  23. Nowack, M. K. et al. A positive signal from the fertilization of the egg cell sets off endosperm proliferation in angiosperm embryogenesis. Nature Genet. 38, 63– 67 (2006)

    Article  ADS  CAS  Google Scholar 

  24. Ingouff, M., Haseloff, J. & Berger, F. Polycomb group genes control developmental timing of endosperm. Plant J. 42, 663– 674 (2005)

    Article  CAS  Google Scholar 

  25. Kohler, C., Page, D. R., Gagliardini, V. & Grossniklaus, U. The Arabidopsis thaliana MEDEA Polycomb group protein controls expression of PHERES1 by parental imprinting. Nature Genet. 37, 28– 30 (2005)

    Article  Google Scholar 

  26. Kohler, C. et al. The Polycomb-group protein MEDEA regulates seed development by controlling expression of the MADS-box gene PHERES1. Genes Dev. 17, 1540– 1553 (2003)

    Article  Google Scholar 

  27. Maheshwari, P. & Singh, H. The female gametophyte of gymnosperms. Biological Review 42, 88– 130 (1967)

    Article  Google Scholar 

  28. Sargant, E. Recent work on the results of fertilization in Angiosperms. Ann. Bot. (Lond.) 14, 689– 712 (1900)

    Article  Google Scholar 

  29. Strasburger, E. Einige Bemerkungen zur Frage nach der “doppelten Befruchtung” bei den Angiospermen. Botanische Zeitung 58, 294– 315 (1900)

    Google Scholar 

  30. Chaudhury, A. M. et al. Fertilization-independent seed development in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 94, 4223– 4228 (1997)

    Article  ADS  CAS  Google Scholar 

  31. Pfaffl, M. W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45 (2001)

    Article  CAS  Google Scholar 

  32. Grini, P. E., Jurgens, G. & Hulskamp, M. Embryo and endosperm development is disrupted in the female gametophytic capulet mutants of Arabidopsis. Genetics 162, 1911– 1925 (2002)

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Sessions, A., Weigel, D. & Yanofsky, M. F. The Arabidopsis thaliana MERISTEM LAYER 1 promoter specifies epidermal expression in meristems and young primordia. Plant J. 20, 259– 263 (1999)

    Article  CAS  Google Scholar 

  34. Lukowitz, W., Mayer, U. & Jurgens, G. Cytokinesis in the Arabidopsis embryo involves the syntaxin-related KNOLLE gene product. Cell 84, 61– 71 (1996)

    Article  CAS  Google Scholar 

  35. Wersto, R. P. et al. Doublet discrimination in DNA cell-cycle analysis. Cytometry 46, 296– 306 (2001)

    Article  CAS  Google Scholar 

Download references

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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Authors and Affiliations

  1. Department of Botany III, University group at the Max Planck Institute for Plant Breeding Research, Max-Delbrück-Laboratorium, University of Cologne, Carl-von-Linné-Weg 10, D-50829 Cologne, Germany,

    Moritz K. Nowack, Nico Dissmeyer & Arp Schnittger

  2. Department of Molecular Biosciences, University of Oslo, PO Box 1041 Blindern, N-0316 Oslo, Norway,

    Reza Shirzadi & Paul E. Grini

  3. Institute of Molecular Medicine and Experimental Immunology, Sigmund-Freud-Straβe 25, D-53105 Bonn, Germany,

    Andreas Dolf & Elmar Endl

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  1. Moritz K. Nowack
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Correspondence to Arp Schnittger.

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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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