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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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.

Author information

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.

Correspondence to Marcel Quint.

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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, H., 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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