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1.
bioRxiv ; 2024 Jan 20.
Article in English | MEDLINE | ID: mdl-38293065

ABSTRACT

A catalog of transcription factor (TF) binding sites in the genome is critical for deciphering regulatory relationships. Here we present the culmination of the modERN (model organism Encyclopedia of Regulatory Networks) consortium that systematically assayed TF binding events in vivo in two major model organisms, Drosophila melanogaster (fly) and Caenorhabditis elegans (worm). We describe key features of these datasets, comprising 604 TFs identifying 3.6M sites in the fly and 350 TFs identifying 0.9 M sites in the worm. Applying a machine learning model to these data identifies sets of TFs with a prominent role in promoting target gene expression in specific cell types. TF binding data are available through the ENCODE Data Coordinating Center and at https://epic.gs.washington.edu/modERNresource, which provides access to processed and summary data, as well as widgets to probe cell type-specific TF-target relationships. These data are a rich resource that should fuel investigations into TF function during development.

2.
Sci Adv ; 9(25): eadg0506, 2023 06 23.
Article in English | MEDLINE | ID: mdl-37352352

ABSTRACT

Gene activity defines cell identity, drives intercellular communication, and underlies the functioning of multicellular organisms. We present the single-cell resolution atlas of gene activity of a fertile adult metazoan: Caenorhabditis elegans. This compendium comprises 180 distinct cell types and 19,657 expressed genes. We predict 7541 transcription factor expression profile associations likely responsible for defining cellular identity. We predict thousands of intercellular interactions across the C. elegans body and the ligand-receptor pairs that mediate them, some of which we experimentally validate. We identify 172 genes that show consistent expression across cell types, are involved in basic and essential functions, and are conserved across phyla; therefore, we present them as experimentally validated housekeeping genes. We developed the WormSeq application to explore these data. In addition to the integrated gene-to-systems biology, we present genome-scale single-cell resolution testable hypotheses that we anticipate will advance our understanding of the molecular mechanisms, underlying the functioning of a multicellular organism and the perturbations that lead to its malfunction.


Subject(s)
Caenorhabditis elegans Proteins , Caenorhabditis elegans , Animals , Caenorhabditis elegans/genetics , Caenorhabditis elegans/metabolism , Caenorhabditis elegans Proteins/genetics , Caenorhabditis elegans Proteins/metabolism , Transcription Factors/metabolism , Gene Expression Regulation , Gene Expression
3.
Genetics ; 223(4)2023 04 06.
Article in English | MEDLINE | ID: mdl-36652461

ABSTRACT

Transcription factors (TFs) play a key role in development and in cellular responses to the environment by activating or repressing the transcription of target genes in precise spatial and temporal patterns. In order to develop a catalog of target genes of Drosophila melanogaster TFs, the modERN consortium systematically knocked down the expression of TFs using RNAi in whole embryos followed by RNA-seq. We generated data for 45 TFs which have 18 different DNA-binding domains and are expressed in 15 of the 16 organ systems. The range of inactivation of the targeted TFs by RNAi ranged from log2fold change -3.52 to +0.49. The TFs also showed remarkable heterogeneity in the numbers of candidate target genes identified, with some generating thousands of candidates and others only tens. We present detailed analysis from five experiments, including those for three TFs that have been the focus of previous functional studies (ERR, sens, and zfh2) and two previously uncharacterized TFs (sens-2 and CG32006), as well as short vignettes for selected additional experiments to illustrate the utility of this resource. The RNA-seq datasets are available through the ENCODE DCC (http://encodeproject.org) and the Sequence Read Archive (SRA). TF and target gene expression patterns can be found here: https://insitu.fruitfly.org. These studies provide data that facilitate scientific inquiries into the functions of individual TFs in key developmental, metabolic, defensive, and homeostatic regulatory pathways, as well as provide a broader perspective on how individual TFs work together in local networks during embryogenesis.


Subject(s)
Drosophila Proteins , Drosophila , Animals , Drosophila/metabolism , Drosophila melanogaster/metabolism , RNA Interference , Transcription Factors/metabolism , Drosophila Proteins/genetics , Drosophila Proteins/metabolism , Receptors, Estrogen/genetics , Receptors, Estrogen/metabolism , DNA-Binding Proteins/genetics
4.
Genome Res ; 31(10): 1952-1969, 2021 10.
Article in English | MEDLINE | ID: mdl-33888511

ABSTRACT

Recently developed single-cell technologies allow researchers to characterize cell states at ever greater resolution and scale. Caenorhabditis elegans is a particularly tractable system for studying development, and recent single-cell RNA-seq studies characterized the gene expression patterns for nearly every cell type in the embryo and at the second larval stage (L2). Gene expression patterns give insight about gene function and into the biochemical state of different cell types; recent advances in other single-cell genomics technologies can now also characterize the regulatory context of the genome that gives rise to these gene expression levels at a single-cell resolution. To explore the regulatory DNA of individual cell types in C. elegans, we collected single-cell chromatin accessibility data using the sci-ATAC-seq assay in L2 larvae to match the available single-cell RNA-seq data set. By using a novel implementation of the latent Dirichlet allocation algorithm, we identify 37 clusters of cells that correspond to different cell types in the worm, providing new maps of putative cell type-specific gene regulatory sites, with promise for better understanding of cellular differentiation and gene regulation.


Subject(s)
Caenorhabditis elegans , Chromatin , Animals , Caenorhabditis elegans/genetics , Chromatin/genetics , Chromatin Immunoprecipitation Sequencing , DNA/genetics , Gene Expression Regulation
5.
Nucleic Acids Res ; 49(3): e17, 2021 02 22.
Article in English | MEDLINE | ID: mdl-33347581

ABSTRACT

Chromatin immunoprecipitation (IP) followed by sequencing (ChIP-seq) is the gold standard to detect transcription-factor (TF) binding sites in the genome. Its success depends on appropriate controls removing systematic biases. The predominantly used controls, i.e. DNA input, correct for uneven sonication, but not for nonspecific interactions of the IP antibody. Another type of controls, 'mock' IP, corrects for both of the issues, but is not widely used because it is considered susceptible to technical noise. The tradeoff between the two control types has not been investigated systematically. Therefore, we generated comparable DNA input and mock IP experiments. Because mock IPs contain only nonspecific interactions, the sites predicted from them using DNA input indicate the spurious-site abundance. This abundance is highly correlated with the 'genomic activity' (e.g. chromatin openness). In particular, compared to cell lines, complex samples such as whole organisms have more spurious sites-probably because they contain multiple cell types, resulting in more expressed genes and more open chromatin. Consequently, DNA input and mock IP controls performed similarly for cell lines, whereas for complex samples, mock IP substantially reduced the number of spurious sites. However, DNA input is still informative; thus, we developed a simple framework integrating both controls, improving binding site detection.


Subject(s)
Chromatin Immunoprecipitation Sequencing/methods , Transcription Factors/metabolism , Antibodies , Binding Sites , Cell Line , DNA , Humans
6.
G3 (Bethesda) ; 10(11): 3977-3990, 2020 11 05.
Article in English | MEDLINE | ID: mdl-32868407

ABSTRACT

Whether generated within a lab setting or isolated from the wild, variant alleles continue to be an important resource for decoding gene function in model organisms such as Caenorhabditis elegans With advances in massively parallel sequencing, multiple whole-genome sequenced (WGS) strain collections are now available to the research community. The Million Mutation Project (MMP) for instance, analyzed 2007 N2-derived, mutagenized strains. Individually, each strain averages ∼400 single nucleotide variants amounting to ∼80 protein-coding variants. The effects of these variants, however, remain largely uncharacterized and querying the breadth of these strains for phenotypic changes requires a method amenable to rapid and sensitive high-throughput analysis. Here we present a pooled competitive fitness approach to quantitatively phenotype subpopulations of sequenced collections via molecular inversion probes (PhenoMIP). We phenotyped the relative fitness of 217 mutant strains on multiple food sources and classified these into five categories. We also demonstrate on a subset of these strains, that their fitness defects can be genetically mapped. Overall, our results suggest that approximately 80% of MMP mutant strains may have a decreased fitness relative to the lab reference, N2 The costs of generating this form of analysis through WGS methods would be prohibitive while PhenoMIP analysis in this manner is accomplished at less than one-tenth of projected WGS costs. We propose methods for applying PhenoMIP to a broad range of population selection experiments in a cost-efficient manner that would be useful to the community at large.


Subject(s)
Caenorhabditis elegans Proteins , Caenorhabditis elegans , Animals , Caenorhabditis elegans/genetics , Caenorhabditis elegans Proteins/genetics , Molecular Probes , Mutation , Phenotype
7.
Nat Genet ; 52(7): 750, 2020 Jul.
Article in English | MEDLINE | ID: mdl-32541926

ABSTRACT

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

8.
J Neurogenet ; 34(3-4): 238-246, 2020.
Article in English | MEDLINE | ID: mdl-33446017

ABSTRACT

John Sulston changed the way we do science, not once, but three times - initially with the complete cell lineage of the nematode Caenorhabditis elegans, next with completion of the genome sequences of the worm and human genomes and finally with his strong and active advocacy for open data sharing. His contributions were widely recognized and in 2002 he received the Nobel Prize in Physiology and Medicine.


Subject(s)
Developmental Biology/history , Neurosciences/history , Animals , Caenorhabditis elegans/cytology , Caenorhabditis elegans/embryology , Caenorhabditis elegans/genetics , Caenorhabditis elegans/physiology , Cell Lineage , Cloning, Molecular/methods , Contig Mapping/history , Cryopreservation , Gene Library , Genome , History, 20th Century , History, 21st Century , Human Genome Project/history , Humans , Larva , Nervous System/cytology , Nervous System/embryology , Nervous System/growth & development , Neurons/cytology , Sequence Analysis, DNA/history , Synaptic Transmission
9.
G3 (Bethesda) ; 10(1): 417-430, 2020 01 07.
Article in English | MEDLINE | ID: mdl-31757929

ABSTRACT

Individuals within a species can exhibit vast variation in copy number of repetitive DNA elements. This variation may contribute to complex traits such as lifespan and disease, yet it is only infrequently considered in genotype-phenotype associations. Although the possible importance of copy number variation is widely recognized, accurate copy number quantification remains challenging. Here, we assess the technical reproducibility of several major methods for copy number estimation as they apply to the large repetitive ribosomal DNA array (rDNA). rDNA encodes the ribosomal RNAs and exists as a tandem gene array in all eukaryotes. Repeat units of rDNA are kilobases in size, often with several hundred units comprising the array, making rDNA particularly intractable to common quantification techniques. We evaluate pulsed-field gel electrophoresis, droplet digital PCR, and Nextera-based whole genome sequencing as approaches to copy number estimation, comparing techniques across model organisms and spanning wide ranges of copy numbers. Nextera-based whole genome sequencing, though commonly used in recent literature, produced high error. We explore possible causes for this error and provide recommendations for best practices in rDNA copy number estimation. We present a resource of high-confidence rDNA copy number estimates for a set of S. cerevisiae and C. elegans strains for future use. We furthermore explore the possibility for FISH-based copy number estimation, an alternative that could potentially characterize copy number on a cellular level.


Subject(s)
DNA Copy Number Variations , Genotyping Techniques/methods , Animals , Caenorhabditis elegans , Genotyping Techniques/standards , Practice Guidelines as Topic , RNA, Ribosomal/genetics , Saccharomyces cerevisiae , Whole Genome Sequencing/methods , Whole Genome Sequencing/standards
10.
Science ; 365(6459)2019 09 20.
Article in English | MEDLINE | ID: mdl-31488706

ABSTRACT

Caenorhabditis elegans is an animal with few cells but a wide diversity of cell types. In this study, we characterize the molecular basis for their specification by profiling the transcriptomes of 86,024 single embryonic cells. We identify 502 terminal and preterminal cell types, mapping most single-cell transcriptomes to their exact position in C. elegans' invariant lineage. Using these annotations, we find that (i) the correlation between a cell's lineage and its transcriptome increases from middle to late gastrulation, then falls substantially as cells in the nervous system and pharynx adopt their terminal fates; (ii) multilineage priming contributes to the differentiation of sister cells at dozens of lineage branches; and (iii) most distinct lineages that produce the same anatomical cell type converge to a homogenous transcriptomic state.


Subject(s)
Caenorhabditis elegans/embryology , Caenorhabditis elegans/genetics , Cell Lineage , Embryonic Development , Animals , Cell Differentiation , Gene Expression Regulation, Developmental , RNA-Seq , Single-Cell Analysis , Transcriptome
11.
Genome Res ; 29(6): 1036-1045, 2019 06.
Article in English | MEDLINE | ID: mdl-31123079

ABSTRACT

We have used RNA-seq in Caenorhabditis elegans to produce transcription profiles for seven specific embryonic cell populations from gastrulation to the onset of terminal differentiation. The expression data for these seven cell populations, covering major cell lineages and tissues in the worm, reveal the complex and dynamic changes in gene expression, both spatially and temporally. Also, within genes, start sites and exon usage can be highly differential, producing transcripts that are specific to developmental periods or cell lineages. We have also found evidence of novel exons and introns, as well as differential usage of SL1 and SL2 splice leaders. By combining this data set with the modERN ChIP-seq resource, we are able to support and predict gene regulatory relationships. The detailed information on differences and similarities between gene expression in cell lineages and tissues should be of great value to the community and provides a framework for the investigation of expression in individual cells.


Subject(s)
Alternative Splicing , Caenorhabditis elegans/genetics , Embryonic Development/genetics , Transcriptome , Animals , Caenorhabditis elegans/embryology , Computational Biology/methods , Exons , Gene Expression Profiling , Gene Expression Regulation, Developmental , Introns , Molecular Sequence Annotation , Organ Specificity , RNA Editing , RNA Splice Sites
12.
Nature ; 568(7752): E11, 2019 Apr.
Article in English | MEDLINE | ID: mdl-30948799

ABSTRACT

In this Review, the year of publication of reference 54 should be 2005, not 2015. In Box 2, "1982: GenBank ( https://www.ncbi.nlm.nih.gov/genbank/statistics/ )" should read "1982: Genbank/ENA/DDBJ" and "2007: NCBI Short Read Archive" should read "2007: NCBI and ENA Short Read Archives"; this is because the launches of these American, European and Japanese databases were coordinated. These errors have not been corrected.

13.
Proc Natl Acad Sci U S A ; 115(28): 7386-7391, 2018 07 10.
Article in English | MEDLINE | ID: mdl-29941601

ABSTRACT

Gene duplication and deletion are pivotal processes shaping the structural and functional repertoire of genomes, with implications for disease, adaptation, and evolution. We employed a mutation accumulation (MA) framework partnered with high-throughput genomics to assess the molecular and transcriptional characteristics of newly arisen gene copy-number variants (CNVs) in Caenorhabditis elegans populations subjected to varying intensity of selection. Here, we report a direct spontaneous genome-wide rate of gene duplication of 2.9 × 10-5/gene per generation in C. elegans, the highest for any species to date. The rate of gene deletion is sixfold lower (5 × 10-6/gene per generation). Deletions of highly expressed genes are particularly deleterious, given their paucity in even the N = 1 lines with minimal efficacy of selection. The increase in average transcript abundance of new duplicates arising under minimal selection is significantly greater than twofold compared with single copies of the same gene, suggesting that genes in segmental duplications are frequently overactive at inception. The average increase in transcriptional activity of gene duplicates is greater in the N = 1 MA lines than in MA lines with larger population bottlenecks. There is an inverse relationship between the ancestral transcription levels of new gene duplicates and population size, with duplicate copies of highly expressed genes less likely to accumulate in larger populations. Our results demonstrate a fitness cost of increased transcription following duplication, which results in purifying selection against new gene duplicates. However, on average, duplications also provide a significant increase in gene expression that can facilitate adaptation to novel environmental challenges.


Subject(s)
Adaptation, Physiological/genetics , Caenorhabditis elegans , Gene Deletion , Gene Dosage , Gene Duplication , Transcription, Genetic , Animals , Caenorhabditis elegans/genetics , Caenorhabditis elegans/metabolism , Genome-Wide Association Study
14.
Genetics ; 208(3): 937-949, 2018 03.
Article in English | MEDLINE | ID: mdl-29284660

ABSTRACT

To develop a catalog of regulatory sites in two major model organisms, Drosophila melanogaster and Caenorhabditis elegans, the modERN (model organism Encyclopedia of Regulatory Networks) consortium has systematically assayed the binding sites of transcription factors (TFs). Combined with data produced by our predecessor, modENCODE (Model Organism ENCyclopedia Of DNA Elements), we now have data for 262 TFs identifying 1.23 M sites in the fly genome and 217 TFs identifying 0.67 M sites in the worm genome. Because sites from different TFs are often overlapping and tightly clustered, they fall into 91,011 and 59,150 regions in the fly and worm, respectively, and these binding sites span as little as 8.7 and 5.8 Mb in the two organisms. Clusters with large numbers of sites (so-called high occupancy target, or HOT regions) predominantly associate with broadly expressed genes, whereas clusters containing sites from just a few factors are associated with genes expressed in tissue-specific patterns. All of the strains expressing GFP-tagged TFs are available at the stock centers, and the chromatin immunoprecipitation sequencing data are available through the ENCODE Data Coordinating Center and also through a simple interface (http://epic.gs.washington.edu/modERN/) that facilitates rapid accessibility of processed data sets. These data will facilitate a vast number of scientific inquiries into the function of individual TFs in key developmental, metabolic, and defense and homeostatic regulatory pathways, as well as provide a broader perspective on how individual TFs work together in local networks and globally across the life spans of these two key model organisms.


Subject(s)
Caenorhabditis elegans/genetics , Caenorhabditis elegans/metabolism , Databases, Genetic , Drosophila/genetics , Drosophila/metabolism , Genome-Wide Association Study , Transcription Factors/metabolism , Animals , Binding Sites , Chromatin Immunoprecipitation , Genome-Wide Association Study/methods , Models, Biological , Nucleotide Motifs , Protein Binding
15.
Nature ; 550(7676): 345-353, 2017 10 19.
Article in English | MEDLINE | ID: mdl-29019985

ABSTRACT

This review commemorates the 40th anniversary of DNA sequencing, a period in which we have already witnessed multiple technological revolutions and a growth in scale from a few kilobases to the first human genome, and now to millions of human and a myriad of other genomes. DNA sequencing has been extensively and creatively repurposed, including as a 'counter' for a vast range of molecular phenomena. We predict that in the long view of history, the impact of DNA sequencing will be on a par with that of the microscope.


Subject(s)
Sequence Analysis, DNA , Animals , Genomics , History, 20th Century , History, 21st Century , Humans , Metagenome/genetics , Microscopy , Sequence Analysis, DNA/history , Sequence Analysis, DNA/methods , Sequence Analysis, DNA/trends
16.
Genetics ; 207(2): 447-463, 2017 10.
Article in English | MEDLINE | ID: mdl-28827289

ABSTRACT

Mutants remain a powerful means for dissecting gene function in model organisms such as Caenorhabditis elegans Massively parallel sequencing has simplified the detection of variants after mutagenesis but determining precisely which change is responsible for phenotypic perturbation remains a key step. Genetic mapping paradigms in C. elegans rely on bulk segregant populations produced by crosses with the problematic Hawaiian wild isolate and an excess of redundant information from whole-genome sequencing (WGS). To increase the repertoire of available mutants and to simplify identification of the causal change, we performed WGS on 173 temperature-sensitive (TS) lethal mutants and devised a novel mapping method. The mapping method uses molecular inversion probes (MIP-MAP) in a targeted sequencing approach to genetic mapping, and replaces the Hawaiian strain with a Million Mutation Project strain with high genomic and phenotypic similarity to the laboratory wild-type strain N2 We validated MIP-MAP on a subset of the TS mutants using a competitive selection approach to produce TS candidate mapping intervals with a mean size < 3 Mb. MIP-MAP successfully uses a non-Hawaiian mapping strain and multiplexed libraries are sequenced at a fraction of the cost of WGS mapping approaches. Our mapping results suggest that the collection of TS mutants contains a diverse library of TS alleles for genes essential to development and reproduction. MIP-MAP is a robust method to genetically map mutations in both viable and essential genes and should be adaptable to other organisms. It may also simplify tracking of individual genotypes within population mixtures.


Subject(s)
Caenorhabditis elegans/genetics , Chromosome Mapping/methods , Chromosomes/genetics , Mutation , Thermotolerance/genetics , Whole Genome Sequencing/methods , Animals , Caenorhabditis elegans/physiology , Caenorhabditis elegans Proteins/genetics , Chromosome Mapping/standards , Whole Genome Sequencing/standards
17.
Science ; 357(6352): 661-667, 2017 08 18.
Article in English | MEDLINE | ID: mdl-28818938

ABSTRACT

To resolve cellular heterogeneity, we developed a combinatorial indexing strategy to profile the transcriptomes of single cells or nuclei, termed sci-RNA-seq (single-cell combinatorial indexing RNA sequencing). We applied sci-RNA-seq to profile nearly 50,000 cells from the nematode Caenorhabditis elegans at the L2 larval stage, which provided >50-fold "shotgun" cellular coverage of its somatic cell composition. From these data, we defined consensus expression profiles for 27 cell types and recovered rare neuronal cell types corresponding to as few as one or two cells in the L2 worm. We integrated these profiles with whole-animal chromatin immunoprecipitation sequencing data to deconvolve the cell type-specific effects of transcription factors. The data generated by sci-RNA-seq constitute a powerful resource for nematode biology and foreshadow similar atlases for other organisms.


Subject(s)
Caenorhabditis elegans/cytology , Caenorhabditis elegans/genetics , Cell Nucleus/genetics , Single-Cell Analysis/methods , Transcriptome , Animals , Caenorhabditis elegans/growth & development , Chromatin Immunoprecipitation , HEK293 Cells , Humans , Larva/genetics , Mice , NIH 3T3 Cells , Neurons/metabolism , RNA/genetics , Sequence Analysis, RNA , Transcription Factors/genetics
18.
Mol Biol Evol ; 34(6): 1319-1334, 2017 06 01.
Article in English | MEDLINE | ID: mdl-28087770

ABSTRACT

Mitochondrial genomes of metazoans, given their elevated rates of evolution, have served as pivotal markers for phylogeographic studies and recent phylogenetic events. In order to determine the dynamics of spontaneous mitochondrial mutations in small populations in the absence and presence of selection, we evolved mutation accumulation (MA) lines of Caenorhabditis elegans in parallel over 409 consecutive generations at three varying population sizes of N = 1, 10, and 100 hermaphrodites. The N =1 populations should have a minimal influence of natural selection to provide the spontaneous mutation rate and the expected rate of neutral evolution, whereas larger population sizes should experience increasing intensity of selection. New mutations were identified by Illumina paired-end sequencing of 86 mtDNA genomes across 35 experimental lines and compared with published genomes of natural isolates. The spontaneous mitochondrial mutation rate was estimated at 1.05 × 10-7/site/generation. A strong G/C→A/T mutational bias was observed in both the MA lines and the natural isolates. This suggests that the low G + C content at synonymous sites is the product of mutation bias rather than selection as previously proposed. The mitochondrial effective population size per worm generation was estimated to be 62. Although it was previously concluded that heteroplasmy was rare in C. elegans, the vast majority of mutations in this study were heteroplasmic despite an experimental regime exceeding 400 generations. The frequencies of frameshift and nonsynonymous mutations were negatively correlated with population size, which suggests their deleterious effects on fitness and a potent role for selection in their eradication.


Subject(s)
Genome, Mitochondrial/genetics , Selection, Genetic/genetics , Animals , Biological Evolution , Caenorhabditis elegans/genetics , DNA, Mitochondrial/genetics , Evolution, Molecular , Mitochondria/genetics , Mutation , Mutation Accumulation , Mutation Rate , Phylogeny , Phylogeography , Population Density , Sequence Analysis, DNA/methods
19.
Genome Res ; 26(10): 1441-1450, 2016 10.
Article in English | MEDLINE | ID: mdl-27531719

ABSTRACT

We generated detailed RNA-seq data for the nematode Caenorhabditis elegans with high temporal resolution in the embryo as well as representative samples from post-embryonic stages across the life cycle. The data reveal that early and late embryogenesis is accompanied by large numbers of genes changing expression, whereas fewer genes are changing in mid-embryogenesis. This lull in genes changing expression correlates with a period during which histone mRNAs produce almost 40% of the RNA-seq reads. We find evidence for many more splice junctions than are annotated in WormBase, with many of these suggesting alternative splice forms, often with differential usage over the life cycle. We annotated internal promoter usage in operons using SL1 and SL2 data. We also uncovered correlated transcriptional programs that span >80 kb. These data provide detailed annotation of the C. elegans transcriptome.


Subject(s)
Caenorhabditis elegans/genetics , Gene Expression Regulation, Developmental , Transcriptome , Animals , Caenorhabditis elegans/growth & development , Molecular Sequence Annotation
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