A Single-Cell Atlas and Lineage Analysis of the Adult Drosophila Ovary

Rust, Katja; Byrnes, Lauren; Yu, Kevin Shengyang; Park, Jason S.; Sneddon, Julie B.; Tward, Aaron D.; Nystul, Todd

doi:10.1101/798223

Cited by 5 publications

(6 citation statements)

References 78 publications

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“…As more ovarian data sets are published, there will be an opportunity to compare and contrast different analysis approaches. One such data set, focusing mainly on early ovarian somatic cells in Drosophila, was recently reported in a preprint article [118]. Despite the differences in sampling, sample preparation, and analysis methods, they report similar cell groupings and comparable marker expression patterns.…”

Section: Plos Biologymentioning

confidence: 99%

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

et al. 2020

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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, eggshell 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.

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Section: Plos Biologymentioning

confidence: 99%

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

et al. 2020

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“…For example, in the adult Drosophila brain, analysis of dopaminergic neurons revealed a Fer2+ cluster of protocerebral anterior-medial dopaminergic cells, and analysis of peptidergic neurons, another rare cell type, revealed multiple specific subtypes of petidergic neurons (Davie et al, 2018). scRNA-seq of adult Drosophila testis and ovary have revealed transcriptomes of rare germline stem cells, allowing detailed characterization of spermatogenesis and oogenesis at the single cell level (Jevitt et al, 2020;Rust et al, 2019;Witt et al, 2019). scRNA-seq of the developing larval ovary enabled the identification of a new cell type corresponding to the elusive follicle stem cell precursors (Slaidina et al, 2020).…”

Section: Characterizing Rare Cellsmentioning

confidence: 99%

“…In Drosophila, scRNA-seq analysis of the adult ovary and testis allowed the reconstruction of developmental trajectories of germ cells during oogenesis and spermatogenesis, respectively (Jevitt et al, 2020;Rust et al, 2019;Witt et al, 2019). In the ovary, pseudotime analysis revealed germ cell trajectory with three branches, one representing early stages of differentiation and other two representing the paths to oocytes and nurse cells (Jevitt et al, 2020;Rust et al, 2019). In the testis, such analysis revealed de novo gene expression bias during spermatogenesis (de novo genes represent new genes that evolve from DNA sequences that were ancestrally nongenic).…”

Section: Developmental Trajectorymentioning

confidence: 99%

“…Combining scRNA-seq with powerful genetic tools holds a great potential for making new discoveries. Indeed, recent scRNA-seq studies in Drosophila have revealed novel biological findings, such as characterizing new cell types in different tissues including the whole embryo, whole brain, ventral nerve cord, gut, blood, abdominal cuticle, testis, and ovary (Allen et al, 2020;Brunet Avalos, Maier, Bruggmann, & Sprecher, 2019;Cattenoz et al, 2020;Cho et al, 2020;Croset, Treiber, & Waddell, 2018;Davie et al, 2018;Fu, Huang, Zhang, Leemput, & Han, 2020;Ghosh et al, 2019;Guo et al, 2019;Hung et al, 2020;Jevitt et al, 2020;Karaiskos et al, 2017;Rust et al, 2019;Shin, Jones, Petkau, Panteluk, & Foley, 2019;Slaidina, Banisch, Gupta, & Lehmann, 2020;Tattikota et al, 2020;Witt, Benjamin, Svetec, & Zhao, 2019), revealing unrealized mechanisms underlying neural development and brain aging (Davie et al, 2018;Konstantinides et al, 2018;Kurmangaliyev, Yoo, LoCascio, & Zipursky, 2019;Li et al, 2017, and uncovering transcriptional regulation or signaling pathways controlling development and tumorigenesis (Ariss, Islam, Critcher, Zappia, & Frolov, 2018;Deng et al, 2019;Genovese et al, 2019;Ji et al, 2019). So far, scRNA-seq profiling has been performed in various Drosophila tissues from multiple stages (Figure 1 and Table 1), providing valuable resources for future studies of those individual tissues or tissue-tissue interactions.…”

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confidence: 99%

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Single‐cell RNA sequencing in Drosophila: Technologies and applications

2020

WIREs Developmental Biology

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Single‐cell RNA sequencing (scRNA‐seq) has emerged as a powerful tool for investigating cell states and functions at the single‐cell level. It has greatly revolutionized transcriptomic studies in many life science research fields, such as neurobiology, immunology, and developmental biology. With the fast development of both experimental platforms and bioinformatics approaches over the past decade, scRNA‐seq is becoming economically feasible and experimentally practical for many biomedical laboratories. Drosophila has served as an excellent model organism for dissecting cellular and molecular mechanisms that underlie tissue development, adult cell function, disease, and aging. The recent application of scRNA‐seq methods to Drosophila tissues has led to a number of exciting discoveries. In this review, I will provide a summary of recent scRNA‐seq studies in Drosophila, focusing on technical approaches and biological applications. I will also discuss current challenges and future opportunities of making new discoveries using scRNA‐seq in Drosophila. This article is categorized under: Technologies > Analysis of the Transcriptome

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“…The emergence of single-cell RNA-sequencing techniques has opened a new window to investigating critical early germline developmental events especially since germ cells exist in small numbers at these stages. Multiple studies have analyzed transcriptomes of germ cells at the single-cell level, but mostly at later stages of development (Slaidina et al 2020;Jevitt et al 2020;Mahadevaraju et al 2020;Rust et al 2019;Li et al 2017;Niu and Spradling 2020). Here we profile the transcriptomes of fruit fly germ cells after specification and before they have coalesced with somatic cells, and we perform this survey for both male and female germ cells.…”

Section: Introductionmentioning

confidence: 99%

Trajectory Mapping of the EarlyDrosophilaGermline Reveals Controls of Zygotic Activation and Sex Differentiation

Chen

Lai

et al. 2020

Preprint

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Germ cells in D. melanogaster are specified maternally shortly after fertilization and are transcriptionally quiescent until their zygotic genome is activated to sustain further development. To understand the molecular basis of this process, we analyzed the progressing transcriptomes of early male and female germ cells at the single-cell level between germline specification and coalescence with somatic gonadal cells. Our data comprehensively covered zygotic activation in the germline genome, and analyses on genes that exhibit germline-restricted expression revealed that polymerase pausing and differential RNA stability are important mechanisms that establish gene expression differences between the germline and soma. In addition, we observed an immediate bifurcation between the male and female germ cells as zygotic transcription begins. The main difference between the two sexes is an elevation in X chromosome expression in females relative to males signifying incomplete dosage compensation with a few select genes exhibiting even higher expression increases. These indicate that the male program is the default mode in the germline that is driven to female development with a second X chromosome.

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A Single-Cell Atlas and Lineage Analysis of the Adult Drosophila Ovary

Cited by 5 publications

References 78 publications

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

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

Single‐cell RNA sequencing in Drosophila: Technologies and applications

Trajectory Mapping of the EarlyDrosophilaGermline Reveals Controls of Zygotic Activation and Sex Differentiation

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