Abstract

The biology and behavior of adults differ substantially from those of developing animals, and cell-specific information is critical for deciphering the biology of multicellular animals. Thus, adult tissue-specific transcriptomic data are critical for understanding molecular mechanisms that control their phenotypes. We used adult cell-specific isolation to identify the transcriptomes of C. elegans’ four major tissues (or “tissue-ome”), identifying ubiquitously expressed and tissue-specific “enriched” genes. These data newly reveal the hypodermis’ metabolic character, suggest potential worm-human tissue orthologies, and identify tissue-specific changes in the Insulin/IGF-1 signaling pathway. Tissue-specific alternative splicing analysis identified a large set of collagen isoforms. Finally, we developed a machine learning-based prediction tool for 76 sub-tissue cell types, which we used to predict cellular expression differences in IIS/FOXO signaling, stage-specific TGF-β activity, and basal vs. memory-induced CREB transcription. Together, these data provide a rich resource for understanding the biology governing multicellular adult animals.

Highlights

  • Animals progress through many stages of development before reaching adulthood, and as adults, they exhibit metabolic and behavioral differences from developing animals

  • While tissue-specific expression has been measured in other organisms, the combination of extremely small tissue size and adult cuticle impermeability have previously prevented the analysis of adult worm tissue expression, which is necessary in order to understand adult processes, including systemic aging, tissue-specific aging, and cell non-autonomous control of aging

  • Subsampling analysis [15], which determines whether sequencing has been performed to sufficient depth, suggests that this estimate of gene expression is stable across multiple sequencing depths (S1A Fig), and gene expression differences represent true differences between tissues

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Summary

Introduction

Animals progress through many stages of development before reaching adulthood, and as adults, they exhibit metabolic and behavioral differences from developing animals. To understand the biology underlying tissue-specific adult behavior, it is critical to identify adult, tissue-specific transcriptomes. While tissue-specific expression has been measured in other organisms, the combination of extremely small tissue size and adult cuticle impermeability have previously prevented the analysis of adult worm tissue expression, which is necessary in order to understand adult processes, including systemic aging, tissue-specific aging, and cell non-autonomous control of aging. Adult tissue-specific expression can be used to better understand signaling and cell autonomous processes and to compare expression to that in other adult organisms. The delineation of adult tissue expression presented here, combined with the genetic and molecular tools available in the worm, provide a unique chance to more directly model aging and disease compared to more complex organisms

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