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A transcriptomic hourglass in plant embryogenesis

Abstract

Animal and plant development starts with a constituting phase called embryogenesis, which evolved independently in both lineages1. Comparative anatomy of vertebrate development—based on the Meckel-Serrès law2 and von Baer’s laws of embryology3 from the early nineteenth centuryshows that embryos from various taxa appear different in early stages, converge to a similar form during mid-embryogenesis, and again diverge in later stages. This morphogenetic series is known as the embryonic ‘hourglass’4,5, and its bottleneck of high conservation in mid-embryogenesis is referred to as the phylotypic stage6. Recent analyses in zebrafish and Drosophila embryos provided convincing molecular support for the hourglass model, because during the phylotypic stage the transcriptome was dominated by ancient genes7 and global gene expression profiles were reported to be most conserved8. Although extensively explored in animals, an embryonic hourglass has not been reported in plants, which represent the second major kingdom in the tree of life that evolved embryogenesis. Here we provide phylotranscriptomic evidence for a molecular embryonic hourglass in Arabidopsis thaliana, using two complementary approaches. This is particularly significant because the possible absence of an hourglass based on morphological features in plants suggests that morphological and molecular patterns might be uncoupled. Together with the reported developmental hourglass patterns in animals, these findings indicate convergent evolution of the molecular hourglass and a conserved logic of embryogenesis across kingdoms.

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Figure 1: Evolutionary age and sequence divergence of A. thaliana genes.
Figure 2: Transcriptome indices across A. thaliana embryogenesis.
Figure 3: Relative expression levels over embryo stages.
Figure 4: Convergent evolution of a molecular hourglass in animal and plant embryogenesis.

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References

  1. Meyerowitz, E. M. Plants compared to animals: the broadest comparative study of development. Science 295, 1482–1485 (2002)

    Article  ADS  CAS  Google Scholar 

  2. Meckel, J. F. Beyträge zur vergleichenden Anatomie (Reclam, Leipzig, 1811)

  3. von Baer, K. E. Über Entwicklungsgeschichte der Thiere: Beobachtung und Reflexion (Gebrüder Bornträger, Königsberg, 1828)

    Book  Google Scholar 

  4. Duboule, D. Temporal colinearity and the phylotypic progression: a basis for the stability of a vertebrate Bauplan and the evolution of morphologies through heterochrony. Dev. Suppl. 1994135–142 (1994)

  5. Raff, R. A. The Shape of Life: Genes, Development and the Evolution of Animal Form (Univ. Chicago Press, 1996)

    Book  Google Scholar 

  6. Sander, K. in Development and Evolution (eds Goodwin, B. C., Holder, N. & Wylie, C. C. ) 137–159 (Cambridge Univ. Press, 1983)

    Google Scholar 

  7. Domazet-Lošo, T. & Tautz, D. A phylogenetically based transcriptome age index mirrors ontogenetic divergence patterns. Nature 468, 815–818 (2010)

    Article  ADS  Google Scholar 

  8. Kalinka, A. T. et al. Gene expression divergence recapitulates the developmental hourglass model. Nature 468, 811–814 (2010)

    Article  ADS  CAS  Google Scholar 

  9. De Smet, I., Lau, S., Mayer, U. & Jürgens, G. Embryogenesis — the humble beginnings of plant life. Plant J. 61, 959–970 (2010)

    Article  CAS  Google Scholar 

  10. Peris, C. I., Rademacher, E. H. & Weijers, D. Green beginnings — pattern formation in the early plant embryo. Curr. Top. Dev. Biol. 91, 1–27 (2010)

    Article  CAS  Google Scholar 

  11. Xiang, D. et al. Genome-wide analysis reveals gene expression and metabolic network dynamics during embryo development in Arabidopsis. Plant Physiol. 156, 346–356 (2011)

    Article  CAS  Google Scholar 

  12. Domazet-Lošo, T., Brajković, J. & Tautz, D. A phylostratigraphy approach to uncover the genomic history of major adaptations in metazoan lineages. Trends Genet. 23, 533–539 (2007)

    Article  Google Scholar 

  13. Levin, M., Hashimshony, T., Wagner, F. & Yanai, I. Developmental milestones punctuate gene expression in the Caenorhabditis embryo. Dev. Cell 22, 1101–1108 (2012)

    Article  CAS  Google Scholar 

  14. Koch, M. A., Haubold, B. & Mitchell-Olds, T. Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol. Biol. Evol. 17, 1483–1498 (2000)

    Article  CAS  Google Scholar 

  15. Arakaki, M. et al. Contemporaneous and recent radiations of the world's major succulent plant lineages. Proc. Natl Acad. Sci. USA 108, 8379–8384 (2011)

    Article  ADS  CAS  Google Scholar 

  16. Koch, M. A. & Kiefer, M. Genome evolution among cruciferous plants: a lecture from the comparison of the genetic maps of three diploid species — Capsella rubella, Arabidopsis lyrata subsp. petraea, and A. thaliana.. Am. J. Bot. 92, 761–767 (2005)

    Article  Google Scholar 

  17. Oh, D.-H. et al. Genome structures and halophyte-specific gene expression of the extremophile Thellungiella parvula in comparison with Thellungiella salsuginea (Thellungiella halophila) and Arabidopsis. Plant Physiol. 154, 1040–1052 (2010)

    Article  CAS  Google Scholar 

  18. Zuber, H. et al. The seed composition of Arabidopsis mutants for the group 3 sulfate transporters indicates a role in sulfate translocation within developing seeds. Plant Physiol. 154, 913–926 (2010)

    Article  CAS  Google Scholar 

  19. Le, B. H. et al. Global analysis of gene activity during Arabidopsis seed development and identification of seed-specific transcription factors. Proc. Natl Acad. Sci. USA 107, 8063–8070 (2010)

    Article  ADS  CAS  Google Scholar 

  20. Nodine, M. D. & Bartel, D. P. Maternal and paternal genomes contribute equally to the transcriptome of early plant embryos. Nature 482, 94–97 (2012)

    Article  ADS  CAS  Google Scholar 

  21. Slack, J. M., Holland, P. W. & Graham, C. F. The zootype and the phylotypic stage. Nature 361, 490–492 (1993)

    Article  ADS  CAS  Google Scholar 

  22. Lau, S., Slane, D., Herud, O., Kong, J. & Jürgens, G. Early embryogenesis in flowering plants: setting up the basic body pattern. Annu. Rev. Plant Biol. 63, 483–506 (2012)

    Article  CAS  Google Scholar 

  23. Park, S. & Harada, J. J. Arabidopsis embryogenesis. Methods Mol. Biol. 427, 3–16 (2008)

    Article  CAS  Google Scholar 

  24. Irie, N. & Kuratani, S. Comparative transcriptome analysis reveals vertebrate phylotypic period during organogenesis. Nature Commun 2, 248 (2011)

    Article  ADS  Google Scholar 

  25. Irie, N. & Sehara-Fujisawa, A. The vertebrate phylotypic stage and an early bilaterian-related stage in mouse embryogenesis defined by genomic information. BMC Biol. 5, 1 (2007)

    Article  Google Scholar 

  26. Katoh, K., Kuma, K., Toh, H. & Miyata, T. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 33, 511–518 (2005)

    Article  CAS  Google Scholar 

  27. Suyama, M., Torrents, D. & Bork, P. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 34, W609–W612 (2006)

    Article  CAS  Google Scholar 

  28. Thornton, K. Libsequence: a C++ class library for evolutionary genetic analysis. Bioinformatics 19, 2325–2327 (2003)

    Article  CAS  Google Scholar 

  29. Goodstein, D. M. et al. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 40, D1178–1186 (2012)

    Article  Google Scholar 

  30. Wu, Z. et al. A model-based background adjustment for oligonucleotide expression arrays. J. Am. Stat. Assoc. 99, 909–917 (2004)

    Article  MathSciNet  Google Scholar 

  31. Carbon, S. et al. AmiGO: online access to ontology and annotation data. Bioinformatics 25, 288–289 (2009)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to S. Abel, L. I. A. Calderón Villalobos, C. Delker, T. Greb, D. Grubb, J. J. Harada, D. Jackson, R. Paxton, A. Soro and C. Wasternack for discussions, to S. Neumann for support with the IPB-cluster, and the 'Exzellenznetzwerk für Biowissenschaften' of the Federal State of Sachsen-Anhalt, Germany, for financial support of M.Q.

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Authors and Affiliations

Authors

Contributions

M.Q. conceived the study. M.Q. and I.G. supervised the project. H.-G.D., A.G., K.K.U. and M.B. analysed the data. M.Q., H.-G.D., A.G., K.K.U., M.B. and I.G. interpreted the results. M.Q. and I.G. wrote the manuscript.

Corresponding author

Correspondence to Marcel Quint.

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Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Notes, Supplementary Figures 1-17, Supplementary Tables 1, 5 and 6 (see separate files for Supplementary Tables 2, 3 and 4). (PDF 1654 kb)

Supplementary Table 2

This file contains the phylostrata information and Ka/Ks raw data for each A. thaliana gene for which we identified an ortholog in A. lyrata. (XLS 5974 kb)

Supplementary Table 3

This file contains the phylostrata information and Ka/Ks raw data for each A. thaliana gene for which we identified an ortholog in A. lyrata. (XLS 10378 kb)

Supplementary Table 4

This file contains the phylostrata information and Ka/Ks raw data for each A. thaliana gene for which we identified an ortholog in A. lyrata. (XLS 10352 kb)

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Quint, M., Drost, HG., Gabel, A. et al. A transcriptomic hourglass in plant embryogenesis. Nature 490, 98–101 (2012). https://doi.org/10.1038/nature11394

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