Pol II Docking and Pausing at Growth and Stress Genes in C. elegans

Fluctuations in nutrient availability profoundly impact gene expression. Previous work revealed postrecruitment regulation of RNA polymerase II (Pol II) during starvation and recovery in Caenorhabditis elegans, suggesting that promoter-proximal pausing promotes rapid response to feeding. To test this hypothesis, we measured Pol II elongation genome wide by two complementary approaches and analyzed elongation in conjunction with Pol II binding and expression. We confirmed bona fide pausing during starvation and also discovered Pol II docking. Pausing occurs at active stress-response genes that become downregulated in response to feeding. In contrast, “docked” Pol II accumulates without initiating upstream of inactive growth genes that become rapidly upregulated upon feeding. Beyond differences in function and expression, these two sets of genes have different core promoter motifs, suggesting alternative transcriptional machinery. Our work suggests that growth and stress genes are both regulated postrecruitment during starvation but at initiation and elongation, respectively, coordinating gene expression with nutrient availability. [Display omitted] •Pol II pausing and backtracking occur during starvation in C. elegans•Pol II also binds upstream of TSSs without initiating transcription•Docking and pausing occur at growth and stress genes, respectively•Docked genes are TATA-less and are upregulated in response to feeding Baugh and colleagues show that RNA polymerase II pauses and backtracks during early elongation in C. elegans. A key factor that promotes pausing in other animals is lacking in the worm, implying variation in regulation of early elongation. They also made the surprising discovery that the polymerase is recruited to the DNA upstream of many growth genes during starvation without initiation. The authors propose that postrecruitment control of initiation coordinates growth with nutrient availability.