Transcriptome age of individual cell types in Caenorhabditis elegans

• Published in: Proceedings of the National Academy of Sciences - PNAS 2023-02, Vol.120 (9), p.e2216351120-e2216351120
• Main Authors: Ma, Fuqiang, Zheng, Chaogu
• Format: Article
• Language: English
• Subjects: Age; Animals; Biological Sciences; Caenorhabditis elegans; Caenorhabditis elegans - genetics; Cell differentiation; Cell fate; Chemoreception; Developmental stages; Divergence; Embryogenesis; Embryonic Development - genetics; Embryos; Gene Expression Profiling; Gene Expression Regulation, Developmental; Genes; Hypodermis; Interneurons; Morphogenesis; Nematoda - genetics; Nematodes; Nervous system; Neurons; Ribonucleic acid; RNA; Transcriptome; Transcriptomes; Transcriptomics; Variation
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.2216351120

The phylotranscriptomic analysis of development in several species revealed the expression of older and more conserved genes in midembryonic stages and younger and more divergent genes in early and late embryonic stages, which supported the hourglass mode of development. However, previous work only studied the transcriptome age of whole embryos or embryonic sublineages, leaving the cellular basis of the hourglass pattern and the variation of transcriptome ages among cell types unexplored. By analyzing both bulk and single-cell transcriptomic data, we studied the transcriptome age of the nematode throughout development. Using the bulk RNA-seq data, we identified the morphogenesis phase in midembryonic development as the phylotypic stage with the oldest transcriptome and confirmed the results using whole-embryo transcriptome assembled from single-cell RNA-seq data. The variation in transcriptome ages among individual cell types remained small in early and midembryonic development and grew bigger in late embryonic and larval stages as cells and tissues differentiate. Lineages that give rise to certain tissues (e.g., hypodermis and some neurons) but not all recapitulated the hourglass pattern across development at the single-cell transcriptome level. Further analysis of the variation in transcriptome ages among the 128 neuron types in nervous system found that a group of chemosensory neurons and their downstream interneurons expressed very young transcriptomes and may contribute to adaptation in recent evolution. Finally, the variation in transcriptome age among the neuron types, as well as the age of their cell fate regulators, led us to hypothesize the evolutionary history of some neuron types.