A transcriptomic hourglass in plant embryogenesis

Abstract

Animal and plant development starts with a constituting phase called embryogenesis, which evolved independently in both lineages. Comparative anatomy of vertebrate development--based on the Meckel-Serrès law and von Baer's laws of embryology from the early nineteenth century--shows 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', and its bottleneck of high conservation in mid-embryogenesis is referred to as the phylotypic stage. 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 genes and global gene expression profiles were reported to be most conserved. 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.