Sea anemones and jellyfish are rewriting the evolutionary history of microRNAs, the tiny genetic molecules that help control when and where genes are switched on and off in animals and plants. For years, scientists assumed that microRNA systems evolved independently in plants and animals, because they looked so different. But the discovery of plant-like microRNA machinery in cnidarians—an ancient group that includes sea anemones and jellyfish—has thrown that assumption into doubt. This project will settle the debate by examining microRNA pathways in the earliest animal lineages: sponges, comb jellies, placozoans, and their single-celled relatives. By reconstructing how these regulatory systems first emerged over 600 million years ago, the work will answer a fundamental question in evolutionary biology: did microRNA regulation have a single common ancestor, or did it arise multiple times? This is fundamental science with no immediate practical application. But understanding how microRNAs evolved is not just an academic exercise. Small RNA research has already opened doors to RNA-based technologies in medicine and agriculture—from gene-silencing therapies to pest-resistant crops. A clearer picture of microRNA origins could sharpen the design of future RNA interference tools by revealing which parts of the machinery are ancient and essential, and which are later innovations.
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The proposal aims to answer a fundamental question in evolutionary biology, namely "Did miRNA pathways have a common ancestor, or did they evolve independently in different lineages?" Over the last two decades, it has become evident that microRNAs (miRNAs) play a central role in almost every major biological process in both plants and animals, such as development and cell physiology. Nearly all animal models do not tolerate the loss of essential miRNA pathway components and exhibit severe defects in embryogenesis. The miRNAs have likely facilitated the evolution of spatiotemporal gene expression and cell-type specialisation. However, the evolution of these miRNAs is still a mystery. While we know that they are part of an ancient RNA interference (RNAi) mechanism involved in antiviral immunity, DNA repair and RNA-processing pathways, it is still unclear how this ancient RNAi mechanism became integrated into our post-transcriptional gene regulation. One big question in this area of research is whether miRNAs independently originated in plants and animals or if they share a common origin. Early studies from land plants and bilaterian animals (e.g. insects and vertebrates) suggested that miRNA pathways evolved separately in plants and animals, given the differences between their miRNA systems and the absence of miRNA pathways in certain groups of organisms like fungi. However, our findings in Cnidaria, a group including sea anemones and jellyfish and split from the rest of the animals very early in the evolution, have unveiled striking similarities between their miRNA system and that of plants, challenging the independent origin hypothesis. Building on my early discoveries from cnidaria, I set out to explore the miRNA-mediated post-transcriptional regulation at the root of the animal kingdom. Non-bilaterians, like sponges, comb jellies, placozoans, and cnidarians, represent the earliest forms of animal life, diverging from other animal groups over 600 million years ago. Studying these animals can provide key insights into the early evolution of gene regulation mechanisms. Equally, exploring unicellular holozoans, close relatives of animals, will reveal the biological roles of miRNAs in unicellular organisms, and further comparison to animals will reveal the role of miRNAs in the evolution of multicellularity. My research aims to reconstruct the evolutionary history of miRNA pathways in the animal kingdom. I will focus on organisms with key phylogenetic positions, including early-branching metazoans and their unicellular relatives Ichthyosporea. Together, they will provide comprehensive insights into previously uncharacterised aspects of miRNA evolution and its function in the last common ancestor of animals, providing a deeper and more holistic understanding of how miRNAs have shaped the evolution of complex life forms, offering a broader perspective on their role in both unicellular and multicellular organisms. We will address the following objectives: (1) the evolutionary history of miRNA biogenesis through characterising Argonaute-containing RNA-induced silencing complexes in early-branching metazoans; (2) the evolution of miRNA targets and their global gene regulatory network across unicellular and multicellular holozoans; (3) The mechanisms of miRNA-mediated gene silencing in the last common ancestor of animals. The findings from this research will advance our understanding of the evolutionary history of miRNAs and have broader implications for RNAi-based research and applications. Small RNA research holds immense potential in revolutionising medical and agricultural applications through RNAi. Fundamental biological insights and evolutionary studies are also facilitated by small RNA research, shedding light on gene regulation, development, cell signalling, and evolutionary mechanisms.
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