Abstract
AbstractComplex multicellularity has emerged independently across a few eukaryotic lineages and is often associated with the rise of elaborate, tightly coordinated developmental processes. How multicellularity and development are interconnected in evolution is a major question in biology. The hourglass model of embryonic evolution depicts how developmental processes are conserved during evolution, predicting morphological and molecular divergence in early and late embryo stages, bridged by a conserved mid-embryonic (phylotypic) period linked to the formation of the basic body plan. Initially found in animal embryos, molecular hourglass patterns have recently been proposed for land plants and fungi. However, whether the hourglass pattern is an intrinsic feature of all developmentally complex eukaryotic lineages remains elusive. Here, we tested the prevalence of a (molecular) hourglass in the brown algae, the third most developmentally complex lineage on earth that has evolved multicellularity independently from animals, fungi, and plants. By exploring the evolutionary transcriptome of brown algae with distinct morphological complexities, we uncovered an hourglass pattern during embryogenesis in developmentally complex species. Filamentous algae without a canonical embryogenesis display an evolutionary transcriptome that is most conserved in multicellular stages of the life cycle, whereas unicellular stages are more rapidly evolving. Our findings suggest that transcriptome conservation in brown algae is associated with cell differentiation stages, but not necessarily linked to embryogenesis. Together with previous work in animals, plants and fungi, we provide further evidence for the generality of a developmental hourglass pattern across complex multicellular eukaryotes.
Publisher
Cold Spring Harbor Laboratory
Reference92 articles.
1. Aggarwal CC , Hinneburg A , Keim DA . 2001. On the Surprising Behavior of Distance Metrics in High Dimensional Space. In: Van den Bussche J , Vianu V , editors. Database Theory — ICDT 2001. Lecture Notes in Computer Science. Berlin, Heidelberg: Springer. p. 420–434.
2. An explanatory evo-devo model for the developmental hourglass;F1000Research,2014
3. Alexa A , Rahnenfuhrer J. 2023. topGO: Enrichment Analysis for Gene Ontology. Available from: https://bioconductor.org/packages/topGO/
4. von Baer KE . 1828. Über Entwickelungsgeschichte der Thiere; Beobachtung und Reflexion. Königsberg: Bornträger
5. Barrera-Redondo J , Lipinska AP , Liu P , Dinatale E , Cossard G , Bogaert K , Hoshino M , Avia K , Leiria G , Avdievich E , et al. 2024. Origin and evolutionary trajectories of brown algal sex chromosomes. Available from: https://www.biorxiv.org/content/10.1101/2024.01.15.575685v1