Abstract In recent years, increasing numbers of microRNAs (miRNAs) have been reported to regulate insect metamorphosis. One thousand, one hundred fifty‐four miRNAs have been previously identified from Tribolium castaneum by high‐throughput sequencing; however, little is known about which miRNAs can participate in metamorphosis, leaving the role of miRNAs in regulating the underlying mechanism elusive. Here, we report the participation of miR‐3017b in the metamorphosis of T. castaneum. Temporal profiles revealed that miR‐3017b was highly expressed at the late larval stage, but significantly decreased at the early pupal stage. Overexpression of miR‐3017b caused larval to pupal to adult metamorphosis arrested. Dual‐luciferase reporter assay and miRNA–mRNA interaction assay illustrated that miR‐3017b interacts with the coding sequence of sarco/endoplasmic reticulum Ca2+ ATPase (SERCA) and suppresses its expression. Knockdown of SERCA caused metamorphosis arrested, similar to that observed in miR‐3017b overexpression beetles. Further functional mechanism analyses revealed that 20‐hydroxyecdysone application downregulates miR‐3017b and up‐regulates SERCA expression. The expression level of downstream genes in the 20E pathway was disrupted after overexpressing miR‐3017 and the knockdown of SERCA. These results provided evidence miR‐3017b‐SERCA contributes to metamorphosis by regulating the 20E pathway in T. castaneum. It could advance our understanding of the coordination of 20E and miRNA regulation in insect metamorphosis.
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