Choreographic dendritic arborization takes place within a defined time frame, but the timing mechanism is currently not known. Here, we report that the precisely timed
lin-4-
lin-14 regulatory circuit triggers an initial dendritic growth activity, whereas the precisely timed
lin-28-
let-7-
lin-41 regulatory circuit signals a subsequent developmental decline in dendritic growth ability, hence restricting dendritic arborization within a set time frame. Loss-of-function mutations in the
lin-4 microRNA gene cause limited dendritic outgrowth, whereas loss-of-function mutations in its direct target, the
lin-14 transcription factor gene, cause precocious and excessive outgrowth. In contrast, loss-of-function mutations in the
let-7 microRNA gene prevent a developmental decline in dendritic growth ability, whereas loss-of-function mutations in its direct target, the
lin-41 tripartite motif protein gene, cause further decline.
lin-4 and
let-7 regulatory circuits are expressed in the right place at the right time to set start and end times for dendritic arborization. Replacing the
lin-4 upstream cis-regulatory sequence at the
lin-4 locus with a late-onset
let-7 upstream cis-regulatory sequence delays dendrite arborization, whereas replacing the
let-7 upstream cis-regulatory sequence at the
let-7 locus with an early-onset
lin-4 upstream cis-regulatory sequence causes a precocious decline in dendritic growth ability. Our results indicate that the
lin-4-
lin-14 and the
lin-28-
let-7-
lin-41 regulatory circuits control the timing of dendrite arborization through antagonistic regulation of the DMA-1 receptor level on dendrites. The LIN-14 transcription factor likely directly represses
dma-1 gene expression through a transcriptional means, whereas the LIN-41 tripartite motif protein likely indirectly promotes
dma-1 gene expression through a posttranscriptional means.