Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Delayed activation of the paternal genome during seed development

Abstract

Little is known about the timing of the maternal-to-zygotic transition during seed development in flowering plants. Because plant embryos can develop from somatic cells or microspores1, maternal contributions are not considered to be crucial in early embryogensis2. Early-acting embryo-lethal mutants in Arabidopsis, includingemb30/gnom which affects the first zygotic division3,4, have fuelled the perception that both maternal and paternal genomes are active immediately after fertilization. Here we show that none of the paternally inherited alleles of 20 loci that we tested is expressed during early seed development in Arabidopsis. For genes that are expressed at later stages, the paternally inherited allele becomes active three to four days after fertilization. The genes that we tested are involved in various processes and distributed throughout the genome, indicating that most, if not all, of the paternal genome may be initially silenced. Our findings are corroborated by genetic studies showing that emb30/gnom has a maternal-effect phenotype that is paternally rescuable in addition to its zygotic lethality. Thus, contrary to previous interpretations, early embryo and endosperm development are mainly under maternal control.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Silencing of paternally inherited genes during seed development in Arabidopsis. a, If an ET2612 female is crossed to a wild-type male, GUS expression is detected in the free nuclear endosperm 12 h.a.p.
Figure 2: Allele-specific expression profile of PRL during early seed development.
Figure 3: Silencing of the paternally inherited EMB30 allele during early embryogenesis.

References

  1. 1

    Mordhorst, A. P., Toonen, M. A. J. & de Vries, S. C. Plant embryogenesis. Crit. Rev. Plant Sci. 16, 535–576 ( 1997).

    Article  Google Scholar 

  2. 2

    Walbot, V. Sources and consequences of phenotypic and genotypic plasticity in flowering plants. Trends Plant Sci. 1, 27– 32 (1996)

    Article  Google Scholar 

  3. 3

    Meinke, D. W. Embryo-lethal mutants of Arabidopsis thaliana: analysis of mutants with a wide range of lethal phases. Theor. Appl. Genet. 69, 543–552 (1985)

    CAS  Article  Google Scholar 

  4. 4

    Mayer, U., Büttner, G. & Jürgens G. Apical-basal pattern formation in the Arabidopsis embryo: studies on the role of the gnom gene. Development 117, 149 –162 (1993).

    Google Scholar 

  5. 5

    van Went, J. L. & Willemse, M. T. M. in Embryology of Angiosperms (ed. Johri, B.) 273–318 (Springer, Berlin, 1984).

    Book  Google Scholar 

  6. 6

    Bowman, J. L. & Mansfield, S. G. in Arabidopsis: An Atlas of Morphology and Development (ed. Bowman, J.) 351– 361 (Springer, New York, 1994).

    Book  Google Scholar 

  7. 7

    Berger, F. Endosperm development. Curr. Opin. Plant Biol. 2, 28–32 (1999).

    CAS  Article  Google Scholar 

  8. 8

    Zalokar, M. Autoradiographic study of protein and RNA formation during early development in Drosophila eggs. Dev. Biol. 49, 425–437 (1976).

    CAS  Article  Google Scholar 

  9. 9

    Newman, E. D. & Rothman, J. H. The maternal-to-zygotic transition in embryonic patterning of Caenorhabditis elegans. Curr. Opin. Genet. Dev. 8, 472–480 (1998).

    Article  Google Scholar 

  10. 10

    Bensaude, O., Babinet, C., Morange, M. & Jacob, F. Heat shock proteins, first major products of zygotic gene activity in mouse embryo. Nature 305, 331–332 ( 1983).

    ADS  CAS  Article  Google Scholar 

  11. 11

    Zimmerman, J. L. & Cohill, P. R. Heat shock and thermotolerance in plant and animal embryogenesis. New. Biol. 7, 641–650 (1991).

    Google Scholar 

  12. 12

    Meinke, D. W. in Arabidopsis (eds Meyerowitz, E. M. & Somerville, C. R.) 253 –295 (Cold Spring Harbor Lab. Press, Cold Spring Harbor, 1994).

    Google Scholar 

  13. 13

    Sundaresan, V. et al. Patterns of gene action in plant development revealed by enhancer trap and gene trap transposable elements. Genes Dev. 9, 1797–1810 (1995).

    CAS  Article  Google Scholar 

  14. 14

    Springer, P. S., McCombie, W. R., Sundaresan, V. & Martienssen, R. A. Gene trap tagging of PROLIFERA, an essential MCM2-3-5-like gene in Arabidopsis. Science 268, 877– 880 (1995).

    ADS  CAS  Article  Google Scholar 

  15. 15

    Liu, Y-G., Mitsukawa, N., Oosumi, T. & Whittier, R. F. Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J. 8, 457–463 (1995).

    CAS  Article  Google Scholar 

  16. 16

    Shevell, D. E. et al. EMB30 is essential for normal cell division, cell expansion, and cell adhesion in Arabidopsis and encodes a protein that has similarity to Sec7. Cell 77, 1051– 1062 (1994).

    CAS  Article  Google Scholar 

  17. 17

    Busch, M., Mayer, U. & Jürgens, G. Molecular analysis of the Arabidopsis pattern formation of gene GNOM: gene structure and intragenic complementation. Mol. Gen. Genet. 250, 681– 691 (1996).

    CAS  PubMed  Google Scholar 

  18. 18

    Howell, S. H. Molecular Genetics of Plant Development (Cambridge Univ. Press, New York, 1999).

    Google Scholar 

  19. 19

    Steinmann, T. et al. Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 286, 316–318 (1999).

    CAS  Article  Google Scholar 

  20. 20

    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).

    ADS  CAS  Article  Google Scholar 

  21. 21

    Vielle-Calzada, J-P. et al. Maintenance of genomic imprinting at the Arabidopsis medea locus requires zygotic DDM1 activity. Genes Dev. 13, 2971–2982 (1999).

    CAS  Article  Google Scholar 

  22. 22

    Nur, U. Heterochromatization and euchromatization of whole genomes in scale insects (Coccoidea: Homoptera). Development (Suppl.) 1, 29– 34 (1990).

    Google Scholar 

  23. 23

    Buglia, G., Predazzi, V. & Ferraro, M. Cytosine methylation is not involved in the heterochromatization of the paternal genome of mealybug Planococcus citri. Chrom. Res. 7, 71–73 ( 1999).

    CAS  Article  Google Scholar 

  24. 24

    Goto, T. & Monk, M. Regulation of X-chromosome inactivation in development in mice and humans. Microbiol. Mol. Biol. Rev. 62, 362–368 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. 25

    Ueda, K. & Tanaka, I. The appearance of male gamete-specific histones gH2B and gH3 during pollen development in Lilium longiflorum. Dev. Biol. 169, 210–217 (1995).

    CAS  Article  Google Scholar 

  26. 26

    Xu, H., Swoboda, I., Bhalla, P. L. & Singh, M. B. Male gametic cell-specific expression of H2A and H3 histone genes. Plant Mol. Biol. 39, 607–614 (1999).

    CAS  Article  Google Scholar 

  27. 27

    Oakeley, E. J., Podesta, A. & Jost, J. P. Developmental changes in DNA methylation of the two tobacco pollen nuclei during maturation. Proc. Natl Acad. Sci. USA 94, 11721–11725 ( 1997).

    ADS  CAS  Article  Google Scholar 

  28. 28

    Moore, J. M., Vielle-Calzada, J-P., Gagliano, W. B. & Grossniklaus, U. Genetic characterization of hadad, a mutant disrupting female gametogenesis in Arabidopsis thaliana. Cold Spring Harbor Symp. Quant. Biol. 62, 35–47 ( 1997).

    CAS  Article  Google Scholar 

  29. 29

    Torii, K. U. et al. The RING finger motif of photomorphogenic repressor COP1 specifically interacts with the RING-H2 motif of a novel Arabidopsis protein. J. Biol. Chem. 274, 27674–27681 (1999).

    CAS  Article  Google Scholar 

Download references

Acknowledgements

We thank J. Moore and W. Gagliano for help in generating transposants, J. Thomas, A. Coluccio and D. Page for technical assistance, E. Vollbrecht and M. Affolter for reviewing the manuscript, and R. Pruitt, V. Sundaresan and E. Vollbrecht for continuous interest in this project. This work was supported in part by the Cold Spring Harbor Laboratory President's Council, a grant from the NRICG Program of the US Department of Agriculture to U.G., a fellowship of the Fonds National Suisse de la Recherche Scientifique to J-P.V-C., and scholarships of the Janggen Poehn-Foundation and the Searle Family Trust to U.G.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Ueli Grossniklaus.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Vielle-Calzada, JP., Baskar, R. & Grossniklaus, U. Delayed activation of the paternal genome during seed development. Nature 404, 91–94 (2000). https://doi.org/10.1038/35003595

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing