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Synthesis of cellulose and formation of tunic structure are unique traits in the tunicate animal group. However, the regulatory mechanism of tunic formation remains obscure. Here, we identified a novel microRNA cluster of three microRNAs, including  miR4018a ,  miR4000f , and  miR4018b  in  Ciona savignyi .  In situ  hybridization and promoter assays showed that  miR4018a/4000f/4018b  cluster was expressed in the mesenchymal cells in the larval trunk, and the expression levels were downregulated during the later tailbud stage and larval metamorphosis. Importantly, overexpression of  miR4018a/4000f/4018b  cluster in mesenchymal cells abolished the cellulose synthesis in  Ciona  larvae and caused the loss of tunic cells in metamorphic larvae, indicating the regulatory roles of  miR4018a/4000f/4018b  cluster in cellulose synthesis and mesenchymal cell differentiation into tunic cells. To elucidate the molecular mechanism, we further identified the target genes of  miR4018a/4000f/4018b  cluster using the combination approaches of TargetScan prediction and RNA-seq data.  Left–right determination factor  ( Lefty ) was confirmed as one of the target genes after narrow-down screening and an experimental luciferase assay. Furthermore, we showed that  Lefty  was expressed in the mesenchymal and tunic cells, indicating its potentially regulatory roles in mesenchymal cell differentiation and tunic formation. Notably, the defects in tunic formation and loss of tunic cells caused by overexpression of  miR4018a/4000f/4018b  cluster could be restored when  Lefty  was overexpressed in  Ciona  larvae, suggesting that  miR4018a/4000f/4018b  regulated the differentiation of mesenchymal cells into tunic cells through the  Lefty  signaling pathway during ascidian metamorphosis. Our findings, thus, reveal a novel microRNA- Lefty  molecular pathway that regulates mesenchymal cells differentiating into tunic cells required for the tunic formation in tunicate species.

A microRNA Cluster-Lefty Pathway is Required for Cellulose Synthesis During Ascidian Larval Metamorphosis