A single-cell atlas of adult Drosophila ovary identifies transcriptional programs and somatic cell lineage regulating oogenesis

• Published in: PLoS biology Vol. 18; no. 4; p. e3000538
• Main Authors: Jevitt, Allison, Chatterjee, Deeptiman, Xie, Gengqiang, Wang, Xian-Feng, Otwell, Taylor, Huang, Yi-Chun, Deng, Wu-Min
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 27-04-2020; Public Library of Science (PLoS)
• Subjects: Animals; Animals, Genetically Modified; Biochemistry; Biology and Life Sciences; Broken symmetry; Cell adhesion & migration; Cell cycle; Cell differentiation; Cell Differentiation - genetics; Cell Lineage; Cell migration; Corpus luteum; Datasets; Drosophila; Drosophila melanogaster - cytology; Drosophila melanogaster - genetics; Eggs; Female; Gene amplification; Gene expression; Gene Expression Profiling; Gene regulation; Gene sequencing; Genes; Genetic aspects; Genetic Markers; Genetic transcription; Genomics; Hemocytes; Hemocytes - cytology; Hemocytes - physiology; Identification and classification; Immune system; Insects; Medicine; Medicine and Health Sciences; Methods and Resources; Mitosis - genetics; Molecular biology; Oogenesis; Oogenesis - genetics; Ovarian Follicle - cytology; Ovaries; Ovary - cytology; Ovary - physiology; Ovulation; Ovulation - genetics; Phagocytes; Physiological aspects; Research and Analysis Methods; Ribonucleic acid; RNA; Sequence Analysis, RNA; Single-Cell Analysis - methods; Software; Somatic cells; Stem cells; Tissues; Transcription; Transcriptomics; United States; Louisiana; Florida; United States > US
• ISSN: 1545-7885; 1544-9173; 1545-7885
• DOI: 10.1371/journal.pbio.3000538

Oogenesis is a complex developmental process that involves spatiotemporally regulated coordination between the germline and supporting, somatic cell populations. This process has been modeled extensively using the Drosophila ovary. Although different ovarian cell types have been identified through traditional means, the large-scale expression profiles underlying each cell type remain unknown. Using single-cell RNA sequencing technology, we have built a transcriptomic data set for the adult Drosophila ovary and connected tissues. Using this data set, we identified the transcriptional trajectory of the entire follicle-cell population over the course of their development from stem cells to the oogenesis-to-ovulation transition. We further identify expression patterns during essential developmental events that take place in somatic and germline cell types such as differentiation, cell-cycle switching, migration, symmetry breaking, nurse-cell engulfment, egg-shell formation, and corpus luteum signaling. Extensive experimental validation of unique expression patterns in both ovarian and nearby, nonovarian cells also led to the identification of many new cell type-and stage-specific markers. The inclusion of several nearby tissue types in this data set also led to our identification of functional convergence in expression between distantly related cell types such as the immune-related genes that were similarly expressed in immune cells (hemocytes) and ovarian somatic cells (stretched cells) during their brief phagocytic role in nurse-cell engulfment. Taken together, these findings provide new insight into the temporal regulation of genes in a cell-type specific manner during oogenesis and begin to reveal the relatedness in expression between cell and tissues types.