Simultaneous cellular and molecular phenotyping of embryonic mutants using single-cell regulatory trajectories

Abmayr, 1998, Drosophila myogenesis and insights into the Role of nautilus, Curr. Top. Dev. Biol., 38, 35, 10.1016/S0070-2153(08)60244-6 Amini, 2014, Haplotype-resolved whole-genome sequencing by contiguity-preserving transposition and combinatorial indexing, Nat. Genet., 46, 1343, 10.1038/ng.3119 Argelaguet, 2019, Multi-omics profiling of mouse gastrulation at single-cell resolution, Nature, 576, 487, 10.1038/s41586-019-1825-8 Azpiazu, 1993, Tinman and bagpipe: two homeo box genes that determine cell fates in the dorsal mesoderm of Drosophila, Genes Dev, 7, 1325, 10.1101/gad.7.7b.1325 Azpiazu, 1996, Segmentation and specification of the Drosophila mesoderm, Genes Dev, 10, 3183, 10.1101/gad.10.24.3183 Bae, 2017, Comparative analysis of gene expression profiles for several migrating cell types identifies cell migration regulators, Mech. Dev., 148, 40, 10.1016/j.mod.2017.04.004 Bodmer, 1993, The gene tinman is required for specification of the heart and visceral muscles in Drosophila, Development, 118, 719, 10.1242/dev.118.3.719 Bolger, 2014, Trimmomatic: a flexible trimmer for Illumina sequence data, Bioinformatics, 30, 2114, 10.1093/bioinformatics/btu170 Bonn, 2012, Tissue-specific analysis of chromatin state identifies temporal signatures of enhancer activity during embryonic development, Nat. Genet., 44, 148, 10.1038/ng.1064 Bonn, 2012, Cell type-specific chromatin immunoprecipitation from multicellular complex samples using bits-chip, Nat. Protoc., 7, 978, 10.1038/nprot.2012.049 Bour, 1995, Drosophila MEF2, a transcription factor that is essential for myogenesis, Genes Dev, 9, 730, 10.1101/gad.9.6.730 Bravo González-Blas, 2019, cisTopic: cis-regulatory topic modeling on single-cell ATAC-seq data, Nat. Methods, 16, 397, 10.1038/s41592-019-0367-1 Briggs, 2018, The dynamics of gene expression in vertebrate embryogenesis at single-cell resolution, Science, 360, 10.1126/science.aar5780 Cannavò, 2017, Genetic variants regulating expression levels and isoform diversity during embryogenesis, Nature, 541, 402, 10.1038/nature20802 Chen, 2019, Assessment of computational methods for the analysis of single-cell ATAC-seq data, Genome Biol, 20, 241, 10.1186/s13059-019-1854-5 Ciglar, 2014, Coordinated repression and activation of two transcriptional programs stabilizes cell fate during myogenesis, Development, 141, 2633, 10.1242/dev.101956 Corces, 2017, An improved ATAC-seq protocol reduces background and enables interrogation of frozen tissues, Nat. Methods, 14, 959, 10.1038/nmeth.4396 Crittenden, 2018, Drosophila mef2 is essential for normal mushroom body and wing development, Biol. Open, 7 Cunha, 2010, Combinatorial binding leads to diverse regulatory responses: Lmd is a tissue-specific modulator of Mef2 activity, PLoS Genet, 6, 10.1371/journal.pgen.1001014 Cusanovich, 2018, A single-cell atlas of in vivo mammalian chromatin accessibility, Cell, 174, 1309, 10.1016/j.cell.2018.06.052 Cusanovich, 2018, The cis-regulatory dynamics of embryonic development at single-cell resolution, Nature, 555, 538, 10.1038/nature25981 Davidson, 2006, Gene regulatory networks and the evolution of animal body plans, Science, 311, 796, 10.1126/science.1113832 Davie, 2018, A single-cell transcriptome atlas of the aging Drosophila brain, Cell, 174, 982, 10.1016/j.cell.2018.05.057 Deng, 2017, Acting on identity: myoblast fusion and the formation of the syncytial muscle fiber, Semin. Cell Dev. Biol., 72, 45, 10.1016/j.semcdb.2017.10.033 Domcke, 2020, A human cell atlas of fetal chromatin accessibility, Science, 370, 10.1126/science.aba7612 Farley, 2015, Regulatory principles governing tissue specificity of developmental enhancers, Cold Spring Harb. Symp. Quant. Biol., 80, 27, 10.1101/sqb.2015.80.027227 Farrell, 2018, Single-cell reconstruction of developmental trajectories during zebrafish embryogenesis, Science, 360, 10.1126/science.aar3131 Furlong, 2018, Developmental enhancers and chromosome topology, Science, 361, 1341, 10.1126/science.aau0320 Ghavi-Helm, 2019, Highly rearranged chromosomes reveal uncoupling between genome topology and gene expression, Nat. Genet., 51, 1272, 10.1038/s41588-019-0462-3 Granja, 2021, ArchR is a scalable software package for integrative single-cell chromatin accessibility analysis, Nat. Genet., 53, 403, 10.1038/s41588-021-00790-6 Gratz, 2015, CRISPR-Cas9 genome editing in Drosophila, Curr. Protoc. Mol. Biol., 111, 31.2.1, 10.1002/0471142727.mb3102s111 Gratz, 2014, Highly specific and efficient CRISPR/Cas9-catalyzed homology-directed repair in Drosophila, Genetics, 196, 961, 10.1534/genetics.113.160713 Hanlon, 2016, Drosophila FoxL1 non-autonomously coordinates organ placement during embryonic development, Dev. Biol., 419, 273, 10.1016/j.ydbio.2016.09.007 Huang, 2019, Vireo: Bayesian demultiplexing of pooled single-cell RNA-seq data without genotype reference, Genome Biol, 20, 273, 10.1186/s13059-019-1865-2 Jakobsen, 2007, Temporal ChIP-on-chip reveals Biniou as a universal regulator of the visceral muscle transcriptional network, Genes Dev, 21, 2448, 10.1101/gad.437607 Junion, 2012, A transcription factor collective defines cardiac cell fate and reflects lineage history, Cell, 148, 473, 10.1016/j.cell.2012.01.030 Klapper, 2002, The formation of syncytia within the visceral musculature of the Drosophila midgut is dependent on duf, sns and mbc, Mech. Dev., 110, 85, 10.1016/S0925-4773(01)00567-6 Kögler, 2021, Extremely rapid and reversible optogenetic perturbation of nuclear proteins in living embryos, Dev. Cell, 56, 2348, 10.1016/j.devcel.2021.07.011 Korsunsky, 2019, Fast, sensitive and accurate integration of single-cell data with harmony, Nat. Methods, 16, 1289, 10.1038/s41592-019-0619-0 Kudron, 2018, The modern resource: genome-wide binding profiles for hundreds of Drosophila and Caenorhabditis elegans transcription factors, Genetics, 208, 937, 10.1534/genetics.117.300657 Kvon, 2014, Genome-scale functional characterization of Drosophila developmental enhancers in vivo, Nature, 512, 91, 10.1038/nature13395 Langmead, 2012, Fast gapped-read alignment with Bowtie 2, Nat. Methods, 9, 357, 10.1038/nmeth.1923 Lee, 2019, Drosophila myoblast fusion: invasion and resistance for the ultimate union, Annu. Rev. Genet., 53, 67, 10.1146/annurev-genet-120116-024603 Lee, 2006, Development of the larval visceral musculature, 62 Li, 2009, Fast and accurate short read alignment with Burrows-Wheeler transform, Bioinformatics, 25, 1754, 10.1093/bioinformatics/btp324 Li, 2009, The sequence alignment/map format and SAMtools, Bioinformatics, 25, 2078, 10.1093/bioinformatics/btp352 Lilly, 1995, Requirement of MADS domain transcription factor D-MEF2 for muscle formation in Drosophila, Science, 267, 688, 10.1126/science.7839146 Lin, 1997, PDP1, a novel Drosophila PAR domain bZIP transcription factor expressed in developing mesoderm, endoderm and ectoderm, is a transcriptional regulator of somatic muscle genes, Development, 124, 4685, 10.1242/dev.124.22.4685 Liu, 2009, A systematic analysis of Tinman function reveals Eya and JAK-STAT signaling as essential regulators of muscle development, Dev. Cell, 16, 280, 10.1016/j.devcel.2009.01.006 McKenna, 2010, The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data, Genome Res, 20, 1297, 10.1101/gr.107524.110 Meiler, 2021, AnnoMiner is a new web-tool to integrate epigenetics, transcription factor occupancy and transcriptomics data to predict transcriptional regulators, Sci. Rep., 11, 15463, 10.1038/s41598-021-94805-1 Miller, 2016, Third chromosome balancer inversions disrupt protein-coding genes and influence distal recombination events in Drosophila melanogaster, G3 (Bethesda), 6, 1959, 10.1534/g3.116.029330 Miller, 2018, The molecular and genetic characterization of second chromosome balancers in Drosophila melanogaster, G3 (Bethesda), 8, 1161, 10.1534/g3.118.200021 Minnoye, 2021, Chromatin accessibility profiling methods, Nat. Rev. Methods Prim., 1, 1 Özel, 2021, Neuronal diversity and convergence in a visual system developmental atlas, Nature, 589, 88, 10.1038/s41586-020-2879-3 Pijuan-Sala, 2019, A single-cell molecular map of mouse gastrulation and early organogenesis, Nature, 566, 490, 10.1038/s41586-019-0933-9 Pijuan-Sala, 2020, Single-cell chromatin accessibility maps reveal regulatory programs driving early mouse organogenesis, Nat. Cell Biol., 22, 487, 10.1038/s41556-020-0489-9 Plass, 2018, Cell type atlas and lineage tree of a whole complex animal by single-cell transcriptomics, Science, 360, 10.1126/science.aaq1723 Quinlan, 2010, BEDTools: a flexible suite of utilities for comparing genomic features, Bioinformatics, 26, 841, 10.1093/bioinformatics/btq033 Ramírez, 2016, deepTools2: a next generation web server for deep-sequencing data analysis, Nucleic Acids Res, 44, W160, 10.1093/nar/gkw257 Reddington, 2020, Lineage-resolved enhancer and promoter usage during a time course of embryogenesis, Dev. Cell, 55, 648, 10.1016/j.devcel.2020.10.009 Reim, 2010, Genetic and genomic dissection of cardiogenesis in the Drosophila model, Pediatr. Cardiol., 31, 325, 10.1007/s00246-009-9612-1 Reiter, 2017, Combinatorial function of transcription factors and cofactors, Curr. Opin. Genet. Dev., 43, 73, 10.1016/j.gde.2016.12.007 Riechmann, 1997, Control of cell fates and segmentation in the Drosophila mesoderm, Development, 124, 2915, 10.1242/dev.124.15.2915 Rivera, 2019, REDfly: the transcriptional regulatory element database for Drosophila, Nucleic Acids Res, 47, D828, 10.1093/nar/gky957 Rousseeuw, 1987, Silhouettes: a graphical aid to the interpretation and validation of cluster analysis, J. Comput. Appl. Math., 20, 53, 10.1016/0377-0427(87)90125-7 Rudolf, 2014, Distinct genetic programs guide Drosophila circular and longitudinal visceral myoblast fusion, BMC Cell Biol, 15, 27, 10.1186/1471-2121-15-27 San Martin, 2001, Hindgut visceral mesoderm requires an ectodermal template for normal development in Drosophila, Development, 128, 233, 10.1242/dev.128.2.233 Sandmann, 2007, A core transcriptional network for early mesoderm development in Drosophila melanogaster, Genes Dev, 21, 436, 10.1101/gad.1509007 Sandmann, 2007, ChIP-on-chip protocol for genome-wide analysis of transcription factor binding in Drosophila melanogaster embryos, Nat. Protoc., 1, 2839, 10.1038/nprot.2006.383 Sandmann, 2006, A temporal map of transcription factor activity: Mef2 directly regulates target genes at all stages of muscle development, Dev. Cell, 10, 797, 10.1016/j.devcel.2006.04.009 Satija, 2015, Spatial reconstruction of single-cell gene expression data, Nat. Biotechnol., 33, 495, 10.1038/nbt.3192 Satpathy, 2019, Massively parallel single-cell chromatin landscapes of human immune cell development and intratumoral T cell exhaustion, Nat. Biotechnol., 37, 925, 10.1038/s41587-019-0206-z Schaub, 2013, Org-1 is required for the diversification of circular visceral muscle founder cells and normal midgut morphogenesis, Dev. Biol., 376, 245, 10.1016/j.ydbio.2013.01.022 Schep, 2017, ChromVAR: inferring transcription-factor-associated accessibility from single-cell epigenomic data, Nat. Methods, 14, 975, 10.1038/nmeth.4401 Schindelin, 2012, Fiji: an open-source platform for biological-image analysis, Nat. Methods, 9, 676, 10.1038/nmeth.2019 Schor, 2018, Non-coding RNA expression, function, and variation during Drosophila embryogenesis, Curr. Biol., 28, 3547, 10.1016/j.cub.2018.09.026 Spitz, 2012, Transcription factors: from enhancer binding to developmental control, Nat. Rev. Genet., 13, 613, 10.1038/nrg3207 Stuart, 2021, Single-cell chromatin state analysis with Signac, Nat. Methods, 18, 1333, 10.1038/s41592-021-01282-5 Tao, 2007, Requirement of the LIM homeodomain transcription factor tailup for normal heart and hematopoietic organ formation in Drosophila melanogaster, Mol. Cell. Biol., 27, 3962, 10.1128/MCB.00093-07 Tomancak, 2002, Systematic determination of patterns of gene expression during Drosophila embryogenesis, Genome Biol, 3, 10.1186/gb-2002-3-12-research0088 Tyser, 2021, Characterization of a common progenitor pool of the epicardium and myocardium, Science, 371, 10.1126/science.abb2986 Wagner, 2018, Single-cell mapping of gene expression landscapes and lineage in the zebrafish embryo, Science, 360, 981, 10.1126/science.aar4362 Yin, 1998, Regulation and function of tinman during dorsal mesoderm induction and heart specification in Drosophila, Dev. Genet., 22, 187, 10.1002/(SICI)1520-6408(1998)22:3<187::AID-DVG2>3.0.CO;2-2 Zaffran, 2001, biniou (FoxF), a central component in a regulatory network controlling visceral mesoderm development and midgut morphogenesis in Drosophila, Genes Dev, 15, 2900, 10.1101/gad.917101 Zhang, 2008, Model-based analysis of ChIP-Seq (MACS), Genome Biol, 9, R137, 10.1186/gb-2008-9-9-r137 Zinzen, 2009, Combinatorial binding predicts spatio-temporal cis-regulatory activity, Nature, 462, 65, 10.1038/nature08531 Zmojdzian, 2013, Tailup plays multiple roles during cardiac outflow assembly in Drosophila, Cell Tissue Res, 354, 639, 10.1007/s00441-013-1644-4