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Cellular-resolution gene expression mapping reveals organization in the head ganglia of the gastropod, Berghia stephanieae
Open accessPreprint — published as 10.1002/cne.25628 · Paper page
Abstract
Gastropod molluscs such as Aplysia , Lymnaea , and Tritonia have been important for determining fundamental rules of motor control, learning, and memory because of their large, individually identifiable neurons. Yet for the vast majority of gastropod neurons, as well as glia, there are no established molecular markers, limiting the ability to establish brain-wide structure-function relations. Here we combine high-throughput, single-cell RNA sequencing (scRNAseq) with in-situ hybridization chain reaction (HCR) in the nudibranch Berghia stephanieae to identify and visualize the expression of markers for cell types. Broad neuronal classes were characterized by genes associated with neurotransmitters, like acetylcholine, glutamate, serotonin, and GABA, as well as neuropeptides. These classes were subdivided by other genes including transcriptional regulators and unannotated genes. Marker genes expressed by neurons and glia formed discrete, previously unrecognized regions within and between ganglia. This study provides the foundation for understanding the fundamental cellular organization of gastropod nervous systems.
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Functional unknomics: Systematic screening of conserved genes of unknown function
Rocha, J. J., Jayaram, S. A., Stevens, T. J., Muschalik, N., Shah, R. D., Emran, S., Robles, C., Freeman, M., & Munro, S. (2023) · PLOS Biology · doi:10.1371/journal.pbio.3002222 · Cited by 70
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Research works printed but not linked: 121
- 10.1038/nature14668 · DOI
- Alquicira-Hernandez J , Powell JE . Nebulosa recovers single cell gene expression signals by kernel density estimation. Bioinformatics. 2021 Jan; . · DOI
- 10.1006/jmbi.1990.9999 · DOI · Paper page
- Arey LB . The multiple sensory activities of the so-called rhinophore of nudibranchs. American Journal of Physiology-Legacy Content. 1918; . · DOI
- 10.1242/dev.061879 · DOI
- 10.1016/S0925-4773(00)00271-9 · DOI
- 1995, Transient and restricted expression during mouse embryogenesis of Dll1, a murine gene closely related to Drosophila Delta, Development, 121, 2407, 10.1242/dev.121.8.2407 · DOI
- Blanco-Carmona E . Generating publication ready visualizations for Single Cell transcriptomics using SCpubr; 2022. · DOI
- 10.1093/bioinformatics/btu170 · DOI · Paper page
- 10.1038/nbt.3519 · DOI · Paper page
- Brunet Avalos C , Maier GL , Bruggmann R , Sprecher SG . Single cell transcriptome atlas of the Drosophila larval brain. Elife. 2019 Nov; 8. · DOI
- 10.1016/j.celrep.2016.12.063 · DOI
- 10.1038/s41592-021-01101-x · DOI · Paper page
- 2002, Formation of neuroblasts in the embryonic central nervous system of Drosophila melanogaster is controlled by SoxNeuro, Development, 129, 4193, 10.1242/dev.129.18.4193 · DOI · Paper page
- Camacho C , Coulouris G , Avagyan V , Ma N , Papadopoulos J , Bealer K , Madden TL . BLAST+: architecture and applications. BMC Bioinformatics. 2009 Dec; 10:421. · DOI · Paper page
- Chao MY , Larkins-Ford J , Tucey TM , Hart AC . lin-12 Notch functions in the adult nervous system of C. elegans. BMC Neurosci. 2005 Jul; 6:45. · DOI
- 10.1038/375761a0 · DOI
- Choi HMT , Schwarzkopf M , Fornace ME , Acharya A , Artavanis G , Stegmaier J , Cunha A , Pierce NA . Third-generation in situ hybridization chain reaction: multiplexed, quantitative, sensitive, versatile, robust. Development. 2018 Jun; 145(12). · DOI · Paper page
- 10.1002/dvdy.20463 · DOI
- 10.1002/dneu.20308 · DOI
- Croll RP . Identified neurons and cellular homologies. Nervous systems in invertebrates. 1987; . · DOI
- 10.1002/cne.1399 · DOI
- 2014, Olfaction in gastropods, Neuroecology and neuroethology in molluscs: The interface between behaviour and environment, 1, 45
- Dal Molin A , Baruzzo G , Di Camillo B . Single-Cell RNA-Sequencing: Assessment of Differential Expression Analysis Methods. Front Genet. 2017 May; 8:62. · DOI · Paper page
- 2019, Extensive conservation of the proneuropeptide and peptide prohormone complement in mollusks, Sci Rep, 9, 4846, 10.1038/s41598-019-40949-0 · DOI
- 10.1002/(SICI)1098-1136(199912)28:3<175::AID-GLIA1>3.0.CO;2-7 · DOI
- 2011, Immunohistochemical demonstration of cholinergic structures in central ganglia of the slug (Limax maximus, Limax valentianus). Neurochem Int, 58, 605, 10.1016/j.neuint.2011.02.002 · DOI
- 2021, Accelerated clearing and molecular labeling of biological tissues using magnetohydrodynamic force, Sci Rep, 11, 16462, 10.1038/s41598-021-95692-2 · DOI
- 2022, Optimization of Whole Mount RNA Multiplexed in situ Hybridization Chain Reaction With Immunohistochemistry, Clearing and Imaging to Visualize Octopus Embryonic Neurogenesis, Front Physiol, 13, 882413, 10.3389/fphys.2022.882413 · DOI
- 10.1007/s004410051240 · DOI
- 10.1016/S0165-5728(85)80063-1 · DOI
- 10.1023/A:1007677003387 · DOI
- 10.1186/s13059-015-0844-5 · DOI · Paper page
- 10.1093/nar/gkh885 · DOI
- 10.1093/nar/gkg563 · DOI
- Gavriouchkina D , Tan Y , Ziadi-Künzli F , Hasegawa Y , Piovani L , Zhang L , Sugimoto C , Luscombe N , Marlétaz F , Rokhsar DS . A single-cell atlas of bobtail squid visual and nervous system highlights molecular principles of convergent evolution; 2022. · DOI
- 10.1038/369061a0 · DOI
- 1980, Central pattern generator mediating swimming in Tritonia, I. Identification and synaptic interactions. J Neurophysiol, 44, 151
- 10.1007/BF00659144 · DOI
- 2014, Novel transcriptome assembly and improved annotation of the whiteleg shrimp (Litopenaeus vannamei), a dominant crustacean in global seafood mariculture, Sci Rep, 4, 7081, 10.1038/srep07081 · DOI
- Gold KS , Brand AH . Optix defines a neuroepithelial compartment in the optic lobe of the Drosophila brain. Neural Dev. 2014 Jul; 9:18. · DOI
- Goodheart JA , Rio RA , Taraporevala NF , Fiorenza RA , Barnes SR , Morrill K , Jacob MAC , Whitesel C , Masterson P , Batzel GO , Johnston HT , Desmond Ramirez M , Katz PS , Lyons DC . A chromosome-level genome for the nudibranch gastropod Berghia stephanieae helps parse clade-specific gene expression in novel and conserved phenotypes; 2023. · DOI
- 2011, Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol, 29, 644
- 2018, Detection and removal of barcode swapping in single-cell RNA-seq data, Nat Commun, 9, 2667, 10.1038/s41467-018-05083-x · DOI
- 2016, Comparative mapping of GABA-immunoreactive neurons in the buccal ganglia of Nudipleura molluscs, J Comp Neurol, 524, 1181, 10.1002/cne.23895 · DOI
- 10.1002/cne.23446 · DOI
- 1995, The homeobox gene repo is required for the differentiation and maintenance of glia function in the embryonic nervous system of Drosophila melanogaster, Development, 121, 317, 10.1242/dev.121.2.317 · DOI
- 2021, Integrated analysis of multimodal single-cell data. Cell, 184, 3573
- 2020, EnTAP: Bringing faster and smarter functional annotation to non-model eukaryotic transcriptomes, Mol Ecol Resour, 20, 591, 10.1111/1755-0998.13106 · DOI
- 1979, Cholinergic features of photoreceptor synapses in Hermissenda, J Neurophysiol, 42, 153
- 10.1038/375787a0 · DOI
- 10.1146/annurev-physiol-020911-153315 · DOI · Paper page
- 10.1016/j.conb.2018.12.006 · DOI · Paper page
- 10.1006/bbrc.1999.1247 · DOI
- 10.1074/jbc.M000032200 · DOI
- 10.1038/nn.3336 · DOI
- 10.1523/JNEUROSCI.04-05-01225.1984 · DOI
- 1999, Central pattern generator for escape swimming in the notaspid sea slug Pleurobranchaea californica, J Neurophysiol, 81, 654, 10.1152/jn.1999.81.2.654 · DOI
- 10.1093/molbev/mst010 · DOI · Paper page
- 10.1016/j.conb.2018.10.009 · DOI
- 10.1242/dev.024570 · DOI
- Kuehn E , Clausen DS , Null RW , Metzger BM , Willis AD , Özpolat BD . Segment number threshold determines juvenile onset of germline cluster expansion in Platynereis dumerilii. J Exp Zool B Mol Dev Evol. 2021 Nov; . · DOI
- Lacin H , Williamson WR , Card GM , Skeath JB , Truman JW . Unc-4 acts to promote neuronal identity and development of the take-off circuit in the Drosophila CNS. Elife. 2020 Mar; 9. · DOI
- 10.1073/pnas.1308758111 · DOI
- 10.1038/nature05453 · DOI · Paper page
- Leonard JL . Identifiable neurons in invertebrates: From invariant cells to dynamic systems. Verlag S. Karger; 2000. · DOI
- 10.1016/j.celrep.2022.110313 · DOI
- Lillvis JL , Gunaratne CA , Katz PS . Homology and homoplasy of swimming behaviors and neural circuits in the Nudipleura (Mollusca, Gastropoda, Opisthobranchia). Proceedings of the. 2012; .
- 10.1523/JNEUROSCI.4196-12.2013 · DOI
- 10.1002/(SICI)1098-1136(199708)20:4<275::AID-GLIA1>3.0.CO;2-5 · DOI
- 2018, The Oyster River Protocol: a multi-assembler and kmer approach for de novo transcriptome assembly, PeerJ, 6, e5428, 10.7717/peerj.5428 · DOI
- 10.1016/S0168-9525(01)02232-6 · DOI
- 10.1016/0304-3940(94)90052-3 · DOI
- 10.1016/S0076-6879(05)96040-0 · DOI
- 2020, Distribution and physiological effect of enterin neuropeptides in the olfactory centers of the terrestrial slug Limax, J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 206, 401, 10.1007/s00359-020-01400-2 · DOI
- 2009, Evidence that the swim afferent neurons of tritonia diomedea are glutamatergic, Biol Bull, 216, 103, 10.1086/BBLv216n2p103 · DOI
- 2021, Modular, efficient and constant-memory single-cell RNA-seq preprocessing, . Nat Biotechnol, 39, 813, 10.1038/s41587-021-00870-2 · DOI
- 10.1002/(SICI)1096-9861(19960415)367:4<607::AID-CNE10>3.0.CO;2-E · DOI
- 10.1073/pnas.051014098 · DOI
- 10.1002/cne.1270 · DOI
- 10.1002/cne.21111 · DOI
- 2012, Homology and homoplasy of swimming behaviors and neural circuits in the Nudipleura (Mollusca, Gastropoda, Opisthobranchia). Proceedings of the National Academy of Sciences, 109, 10669
- 10.1038/nrm757 · DOI · Paper page
- 10.1186/1741-7007-11-53 · DOI
- 1995, Six3, a murine homologue of the sine oculis gene, demarcates the most anterior border of the developing neural plate and is expressed during eye development, Development, 121, 4045, 10.1242/dev.121.12.4045 · DOI
- 10.1126/sciadv.aba0365 · DOI
- 10.1016/j.ceb.2014.12.009 · DOI
- Petersen KR , Streett DA , Gerritsen AT , Hunter SS , Settles ML . Super deduper, fast PCR duplicate detection in fastq files. In: Proceedings of the 6th ACM Conference on Bioinformatics, Computational Biology and Health Informatics BCB ’15, New York, NY, USA: Association for Computing Machinery; 2015. p. 491–492. · DOI
- 10.1242/dev.124.9.1699 · DOI
- 10.1371/journal.pone.0009490 · DOI · Paper page
- 10.1016/j.cub.2017.05.016 · DOI
- 2002, Distribution of glial cells in the central nervous system of the pulmonate snail Megalobulimus oblongus identified by means of a glial fibrillary acidic protein marker, Acta Zool, 83, 345, 10.1046/j.1463-6395.2002.00126.x · DOI
- 10.1016/S0361-9230(96)00325-5 · DOI
- 10.1093/bioinformatics/bts094 · DOI
- 10.1089/dna.1998.17.1017 · DOI
- 2000, The Drosophila homeobox gene optix is capable of inducing ectopic eyes by an eyeless-independent mechanism, Development, 127, 1879, 10.1242/dev.127.9.1879 · DOI
- 10.1016/S0925-4773(98)00028-8 · DOI
- 2018, A safer, urea-based in situ hybridization method improves detection of gene expression in diverse animal species, Dev Biol, 434, 15, 10.1016/j.ydbio.2017.11.015 · DOI
- 10.1101/gr.196469.115 · DOI
- 2022, Cell types and molecular architecture of the Octopus bimaculoides visual system, Curr Biol, 32, 5031, 10.1016/j.cub.2022.10.015 · DOI
- 10.1002/(SICI)1097-4695(19991115)41:3<399::AID-NEU8>3.0.CO;2-Z · DOI
- Storch V , Welsch U . Über Bau und Funktion der Nudibranchier-Rhinophoren. Cell Tissue Res. 1969; . · DOI
- 10.2144/00286ir01 · DOI
- 10.1016/S0925-4773(02)00043-6 · DOI
- 10.1038/s41467-022-35198-1 · DOI
- 10.1016/j.conb.2018.04.021 · DOI · Paper page
- 2021, Nemertean, Brachiopod, and Phoronid Neuropeptidomics Reveals Ancestral Spiralian Signaling Systems, Mol Biol Evol, 38, 4847, 10.1093/molbev/msab211 · DOI
- 10.1126/science.aar4237 · DOI · Paper page
- 10.1016/j.ygcen.2010.02.010 · DOI
- 10.1073/pnas.1610602114 · DOI
- Walters ET , Bodnarova M , Billy AJ , others. Somatotopic organization and functional properties of mechanosensory neurons expressing sensorin-A mRNA in Aplysia californica. Journal of. 2004; . · DOI
- Watkins KL . Chemosensory Receptors in Berghia stephanieae: Bioinformatics and Localization. PhD thesis, University of Massachusetts Amherst; 2022.
- Wertz A , Rössler W , Obermayer M , Bickmeyer U . Functional neuroanatomy of the rhinophore of Aplysia punctata. Front Zool. 2006 Apr; 3:6. · DOI
- Whitesel CA . Studying the Central and Peripheral Nervous Systems in larval and juvenile Berghia stephanieae. PhD thesis, UC San Diego; 2021.
- Williams EA , Verasztó C , Jasek S , Conzelmann M , Shahidi R , Bauknecht P , Mirabeau O , Jékely G . Synaptic and peptidergic connectome of a neurosecretory center in the annelid brain. Elife. 2017 Dec; 6. · DOI · Paper page
- 10.1093/bioinformatics/btu077 · DOI
- 10.1101/gad.8.8.981 · DOI
- 10.1152/jn.1994.72.3.1357 · DOI
- 10.1038/s41467-021-22751-7 · DOI
- Zappia L , Oshlack A . Clustering trees: a visualization for evaluating clusterings at multiple resolutions. Giga-science. 2018 Jul; 7(7). · DOI · Paper page
- 10.1101/lm.63903 · DOI
Metadata
- Authors
- Ramirez, M. D., Bui, T. N., & Katz, P. S.
- Affiliations
- University of Massachusetts Amherst (US)
- Corresponding author
- Ramirez, M. Desmond
- Venue
- The Journal of Comparative Neurology
- Publisher
- openRxiv
- Published
- 2023-06-26
- Volume
- 532
- Issue
- 6
- Pages
- e25628-e25628
- ISSN
- 0021-9967 (ISSN-L)
- PMC
- PMC11198006
- OpenAlex
- W4399473889
- Cited by
- 10
- References
- 1
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 4 · 2023: 1
- FWCI
- 1.23
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc
- Locations
- The Journal of Comparative Neurology (publishedVersion, cc-by-nc)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Science Foundation (1812017, 2227963)
- Harvard University
- National Institutes of Health (1u01ns123972-01)
- University of Massachusetts Amherst
- National Institute of Neurological Disorders and Stroke (U01NS108637, U01 NS123972, R01NS133654)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Keywords
- Berghia stephanieae, gastropod nervous system, neuronal cell types, single-cell RNA sequencing, neuropeptides, acetylcholine, glutamate, serotonin, GABA, glia, molecular markers, neuronal organization
- MeSH terms
- Animals, Head, Neurons, Gene Expression, Ganglia, Invertebrate, Gastropoda
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