Journal Article

Ancient animal microRNAs and the evolution of tissue identity

Hannon, Gregory J., Snyman, Heidi, Christodoulou, Foteini, Bork, Peer, Raible, Florian, Arendt, Detlev, Trachana, Kalliopi, Tomer, Raju, Simakov, Oleg, Klaus, Sebastian

2010

Overview

An oral tradition for microRNA Recent work suggests that microRNAs, the ubiquitous, small, non-coding genetic elements with important regulatory roles, were important in the evolution of complexity in multicellular animals. What was the role of these microRNAs when they first evolved? A deep sequencing study of the marine ragworm Platynereis dumerilii , and comparison with other bilaterian animals, suggests that the most ancient known microRNA, miR-100, was initially active in neurosecretory cells around the mouth. Other highly conserved varieties were first present in specific tissues and organ systems, such as ciliated cells and parts of the nervous system, musculature and gut. This work suggests that the last common ancestor of bilaterian animals already had all these structures. Recent work suggests that microRNAs might have been important in the evolution of complexity in multicellular animals. Here it is shown that the most ancient known microRNA, miR–100, was initially active in neurosecretory cells around the mouth. Other highly conserved varieties were first present in specific tissues and organ systems. Thus, microRNA expression was initially restricted to an ancient set of ancient animal cell types and tissues. The spectacular escalation in complexity in early bilaterian evolution correlates with a strong increase in the number of microRNAs 1 , 2 . To explore the link between the birth of ancient microRNAs and body plan evolution, we set out to determine the ancient sites of activity of conserved bilaterian microRNA families in a comparative approach. We reason that any specific localization shared between protostomes and deuterostomes (the two major superphyla of bilaterian animals) should probably reflect an ancient specificity of that microRNA in their last common ancestor. Here, we investigate the expression of conserved bilaterian microRNAs in Platynereis dumerilii , a protostome retaining ancestral bilaterian features 3 , 4 , in Capitella , another marine annelid, in the sea urchin Strongylocentrotus , a deuterostome, and in sea anemone Nematostella , representing an outgroup to the bilaterians. Our comparative data indicate that the oldest known animal microRNA, miR-100, and the related miR-125 and let-7 were initially active in neurosecretory cells located around the mouth. 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. These findings reveal that microRNA evolution and the establishment of tissue identities were closely coupled in bilaterian evolution. Also, they outline a minimum set of cell types and tissues that existed in the protostome–deuterostome ancestor.

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: 631/181 / 631/337/384/331 / Animals / Annelida / Annelida - anatomy & histology / Annelida - cytology / Annelida - genetics / Bilateria / Biological and medical sciences / Biological Evolution / Brain / Brain - metabolism / Capitella / Central nervous system / Cilia - physiology / Conserved Sequence - genetics / Correlation / Deuterostomia / Digestive System - cytology / Digestive System - metabolism / Echinoidea / Evolution / Fundamental and applied biological sciences. Psychology / Genetic aspects / Genetics of eukaryotes. Biological and molecular evolution / Humanities and Social Sciences / Hybridization / Identification and classification / In Situ Hybridization / Information processing / letter / Localization / Marine / MicroRNA / MicroRNAs - analysis / MicroRNAs - genetics / Molecular evolution / Molecular Sequence Data / multidisciplinary / Natural history / Nematostella / Organ Specificity / Organs / Phylogeny / Physiological aspects / Platynereis dumerilii / Polychaeta - anatomy & histology / Polychaeta - cytology / Polychaeta - genetics / Science / Science (multidisciplinary) / Sea Anemones - anatomy & histology / Sea Anemones - cytology / Sea Anemones - genetics / Sea urchins / Sea Urchins - anatomy & histology / Sea Urchins - cytology / Sea Urchins - genetics / Strongylocentrotus / Tissues / Vertebrates