An atlas of the C. elegans starvation response reveals that transcription is necessary to initiate transcriptional silencing in quiescent primordial germ cells

Abstract

Starvation profoundly impacts development, but how different tissues respond to starvation is unclear. We generated a cellular atlas of gene expression in fed and starved C. elegans L1 larvae. We identified 79 cell types in both conditions, and we detected [~]98% of protein-coding genes, 44% of which were differentially expressed. Starvation affected translation-related genes across the animal, and most "housekeeping" genes were downregulated. However, tissue-specific patterns of differential expression, transcription factor activity, and GO term enrichments are widespread, suggesting tissue-specific gene regulatory mechanisms and functional consequences. We inferred tissue-specific effects on transcription factor activity, identifying known and novel putative nutrient-dependent transcriptional regulators. Surprisingly, we found extensive transcription in starved primordial germ cells (PGCs), which are known to hyper-compact their chromatin and silence transcription during L1 starvation. We validated PGC transcription of aak-1/AMPK, and we showed that zygotic aak-1/AMPK is required for PGC chromatin hyper-compaction, supporting reproductive success upon recovery. This work provides a valuable resource characterizing nutritional control of transcription in an animal, and it reveals that transcription of aak-1/AMPK is necessary to silence transcription in quiescent PGCs.