Abstract |
This thesis addresses the emerging link between the evolution of microRNAs and the evolution of complex bilaterian body plans. Recent deep sequencing of various metazoan animals revealed that early metazoans possessed at least one conserved microRNA, miR- 100 (plus an unknown number of non conserved microRNAs), growing to 36 microRNAs
in the last common ancestor of protostomes and deuterostomes. To further explore the putative link between the evolution of stem bilaterians and microRNAs, I set out to determine the ancient sites of activity of conserved microRNA families in a comparative approach.
I investigated the full set of 36 conserved bilaterian microRNAs in two slow-evolving protostome animals, the marine annelids Platynereis and Capitella, in a slow-evolving deuterostome, the sea urchin Strongylocentrotus and in a basal metazoan, the sea anemone Nematostella. The resulting comparative expression data showed that in these animals,
other than in the fast-evolving fly Drosophila and nematode Caenorhabditis, microRNAs largely retain their ancient expression sites.
The oldest animal microRNA, miR-100, together with the co-transcribed let-7 and miR-125, was found expressed in a small group of neurosecretory cells located around the mouth, in cnidarians, annelids and sea urchin. This is where the conserved role of
let-7 and miR-125 in developmental timing must have evolved. Other sets of ancient microRNAs were first present in locomotor ciliated cells, specific brain centres, or, more broadly, one of four major organ systems: central nervous system, sensory tissue, musculature and gut.
Insights into the contribution of the step-wise acquisition of microRNA families towards
bilaterian complexity are given in the second part of this thesis. Using Platynereis and
Capitella developing annelids, I localized the expression of 7 microRNAs specific to the
protostome, 6 to the lophotrochozoan, 2 to the annelid and 2 to the Platynereis lineage.
In most cases lineage specific microRNAs appeared to reinforce the regulatory signature of ancient bilaterian microRNAs by joining their expression in the above stated tissues.
However few of them were highly restricted to subsets of these ancient bilaterian tissues.
In conclusion, the expression data of this comparative study suggest that both ancient bilaterian and “younger” lineage -specific microRNAs evolved in a tissue -specific context and conferred developmental robustness to an ancient set of animal cell types and tissues.
They also imply that these microRNA-defined tissues were in place already in the last common ancestor of protostomes and deuterostomes. By this property, microRNAs provide a new tool for reconstructing ancient animal body plans at important evolutionary
nodes, focussing here on the protostome-deuterostome divergence.
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