Single-cell RNA sequencing illuminates the ontogeny, conservation and diversification of cartilaginous and bony fish lymphocytes.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
03 Sep 2024
Historique:
received: 13 12 2023
accepted: 16 08 2024
medline: 4 9 2024
pubmed: 4 9 2024
entrez: 3 9 2024
Statut: epublish

Résumé

Elucidating cellular architecture and cell-type evolution across species is central to understanding immune system function and susceptibility to disease. Adaptive immunity is a shared trait of the common ancestor of cartilaginous and bony fishes. However, evolutionary features of lymphocytes in these two jawed vertebrates remain unclear. Here, we present a single-cell RNA sequencing atlas of immune cells from cartilaginous (white-spotted bamboo shark) and bony (zebrafish and Chinese tongue sole) fishes. Cross-species comparisons show that the same cell types across different species exhibit similar transcriptional profiles. In the bamboo shark, we identify a phagocytic B cell population expressing several pattern recognition receptors, as well as a T cell sub-cluster co-expressing both T and B cell markers. In contrast to a division by function in the bony fishes, we show close linkage and poor functional specialization among lymphocytes in the cartilaginous fish. Our cross-species single-cell comparison presents a resource for uncovering the origin and evolution of the gnathostome immune system.

Identifiants

pubmed: 39227568
doi: 10.1038/s41467-024-51761-4
pii: 10.1038/s41467-024-51761-4
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

7627

Informations de copyright

© 2024. The Author(s).

Références

Arendt, D. et al. The origin and evolution of cell types. Nat. Rev. Genet 17, 744–757 (2016).
pubmed: 27818507 doi: 10.1038/nrg.2016.127
Network, B. I. C. C. A multimodal cell census and atlas of the mammalian primary motor cortex. Nature 598, 86–102 (2021).
doi: 10.1038/s41586-021-03950-0
Hodge, R. D. et al. Conserved cell types with divergent features in human versus mouse cortex. Nature 573, 61–68 (2019).
pubmed: 31435019 pmcid: 6919571 doi: 10.1038/s41586-019-1506-7
Shami, A. N. et al. Single-cell RNA sequencing of human, macaque, and mouse testes uncovers conserved and divergent features of mammalian spermatogenesis. Dev. Cell 54, 529–547.e512 (2020).
pubmed: 32504559 pmcid: 7879256 doi: 10.1016/j.devcel.2020.05.010
Flajnik, M. F. A cold-blooded view of adaptive immunity. Nat. Rev. Immunol. 18, 438–453 (2018).
pubmed: 29556016 pmcid: 6084782 doi: 10.1038/s41577-018-0003-9
Flajnik, M. F. & Kasahara, M. Origin and evolution of the adaptive immune system: genetic events and selective pressures. Nat. Rev. Genet 11, 47–59 (2010).
pubmed: 19997068 doi: 10.1038/nrg2703
Boehm, T. Evolution of vertebrate immunity. Curr. Biol. 22, R722–732, (2012).
pubmed: 22975003 doi: 10.1016/j.cub.2012.07.003
Shimeld, S. M. & Holland, P. W. Vertebrate innovations. Proc. Natl Acad. Sci. USA 97, 4449–4452 (2000).
pubmed: 10781042 pmcid: 34320 doi: 10.1073/pnas.97.9.4449
Dornburg, A. & Yoder, J. A. On the relationship between extant innate immune receptors and the evolutionary origins of jawed vertebrate adaptive immunity. Immunogenetics 74, 111–128 (2022).
pubmed: 34981186 doi: 10.1007/s00251-021-01232-7
Li, J. et al. B lymphocytes from early vertebrates have potent phagocytic and microbicidal abilities. Nat. Immunol. 7, 1116–1124 (2006).
pubmed: 16980980 doi: 10.1038/ni1389
Tan, M. et al. The whale shark genome reveals patterns of vertebrate gene family evolution. Elife 10, https://doi.org/10.7554/eLife.65394 (2021).
Venkatesh, B. et al. Elephant shark genome provides unique insights into gnathostome evolution. Nature 505, 174–179 (2014).
pubmed: 24402279 pmcid: 3964593 doi: 10.1038/nature12826
Zhang, Y. et al. The white-spotted bamboo shark genome reveals chromosome rearrangements and fast-evolving immune genes of cartilaginous fish. iScience 23, 101754 (2020).
pubmed: 33251490 pmcid: 7677710 doi: 10.1016/j.isci.2020.101754
Litman, G. W., Anderson, M. K. & Rast, J. P. Evolution of antigen binding receptors. Annu Rev. Immunol. 17, 109–147 (1999).
pubmed: 10358755 doi: 10.1146/annurev.immunol.17.1.109
Matz, H., Munir, D., Logue, J. & Dooley, H. The immunoglobulins of cartilaginous fishes. Dev. Comp. Immunol. 115, 103873 (2021).
pubmed: 32979434 doi: 10.1016/j.dci.2020.103873
Greenberg, A. S. et al. A new antigen receptor gene family that undergoes rearrangement and extensive somatic diversification in sharks. Nature 374, 168–173 (1995).
pubmed: 7877689 doi: 10.1038/374168a0
Wu, L. et al. Recent advances on phagocytic B cells in teleost fish. Front Immunol. 11, 824 (2020).
pubmed: 32536909 pmcid: 7267004 doi: 10.3389/fimmu.2020.00824
Rast, J. P. et al. alpha, beta, gamma, and delta T cell antigen receptor genes arose early in vertebrate phylogeny. Immunity 6, 1–11 (1997).
pubmed: 9052832 doi: 10.1016/S1074-7613(00)80237-X
Flajnik, M. F., Ohta, Y., Namikawa-Yamada, C. & Nonaka, M. Insight into the primordial MHC from studies in ectothermic vertebrates. Immunol. Rev. 167, 59–67 (1999).
pubmed: 10319251 doi: 10.1111/j.1600-065X.1999.tb01382.x
Kulski, J. K., Shiina, T., Anzai, T., Kohara, S. & Inoko, H. Comparative genomic analysis of the MHC: the evolution of class I duplication blocks, diversity and complexity from shark to man. Immunol. Rev. 190, 95–122 (2002).
pubmed: 12493009 doi: 10.1034/j.1600-065X.2002.19008.x
Takizawa, F. et al. CD4 and LAG-3 from sharks to humans: related molecules with motifs for opposing functions. Front. Immunol. 14, 1267743 (2023).
pubmed: 38187381 pmcid: 10768021 doi: 10.3389/fimmu.2023.1267743
Deiss, T. C. et al. Ancient use of Ig variable domains contributes significantly to the TCRδ repertoire. J. Immunol. 203, 1265–1275 (2019).
pubmed: 31341077 doi: 10.4049/jimmunol.1900369
Stanfield, R. L., Dooley, H., Flajnik, M. F. & Wilson, I. A. Crystal structure of a shark single-domain antibody V region in complex with lysozyme. Science 305, 1770–1773 (2004).
pubmed: 15319492 doi: 10.1126/science.1101148
Horton, R. et al. Gene map of the extended human MHC. Nat. Rev. Genet 5, 889–899 (2004).
pubmed: 15573121 doi: 10.1038/nrg1489
Li, L. et al. Nuclear adaptor Ldb1 regulates a transcriptional program essential for the maintenance of hematopoietic stem cells. Nat. Immunol. 12, 129–136 (2011).
pubmed: 21186366 doi: 10.1038/ni.1978
Shay, T. et al. Conservation and divergence in the transcriptional programs of the human and mouse immune systems. Proc. Natl Acad. Sci. USA 110, 2946–2951 (2013).
pubmed: 23382184 pmcid: 3581886 doi: 10.1073/pnas.1222738110
Hagai, T. et al. Gene expression variability across cells and species shapes innate immunity. Nature 563, 197–202 (2018).
pubmed: 30356220 pmcid: 6347972 doi: 10.1038/s41586-018-0657-2
Iwasaki, H. & Akashi, K. Myeloid lineage commitment from the hematopoietic stem cell. Immunity 26, 726–740 (2007).
pubmed: 17582345 doi: 10.1016/j.immuni.2007.06.004
Levy, S. et al. A stony coral cell atlas illuminates the molecular and cellular basis of coral symbiosis, calcification, and immunity. Cell 184, 2973–2987.e2918 (2021).
pubmed: 33945788 pmcid: 8162421 doi: 10.1016/j.cell.2021.04.005
Gu, Z., Gu, L., Eils, R., Schlesner, M. & Brors, B. Circlize implements and enhances circular visualization in R. Bioinformatics 30, 2811–2812 (2014).
pubmed: 24930139 doi: 10.1093/bioinformatics/btu393
Ashburner, M. et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet 25, 25–29 (2000).
pubmed: 10802651 pmcid: 3037419 doi: 10.1038/75556
Hsieh, T. et al. JunB is critical for survival of T helper cells. Front. Immunol. 13, 901030 (2022).
pubmed: 35837408 pmcid: 9273772 doi: 10.3389/fimmu.2022.901030
Powell, M. D., Read, K. A., Sreekumar, B. K. & Oestreich, K. J. Ikaros zinc finger transcription factors: regulators of cytokine signaling pathways and CD4+ T helper cell differentiation. Front. Immunol. 10, 462704 (2019).
doi: 10.3389/fimmu.2019.01299
Zhao, Z. et al. IL-12Rβ2 promotes the development of CD4+ CD25+ regulatory T cells. J. Immunol. 181, 3870–3876 (2008).
pubmed: 18768841 doi: 10.4049/jimmunol.181.6.3870
McCausland, M. M. et al. SAP regulation of follicular helper CD4 T cell development and humoral immunity is independent of SLAM and Fyn kinase. J. Immunol. 178, 817–828 (2007).
pubmed: 17202343 doi: 10.4049/jimmunol.178.2.817
Kasheta, M. et al. Identification and characterization of T reg–like cells in zebrafish. J. Exp. Med. 214, 3519–3530 (2017).
pubmed: 29066577 pmcid: 5716030 doi: 10.1084/jem.20162084
Wan, F. et al. Characterization of γδ T cells from zebrafish provides insights into their important role in adaptive humoral immunity. Front. Immunol. 7, 675 (2017).
pubmed: 28119690 pmcid: 5220103 doi: 10.3389/fimmu.2016.00675
Dee, C. T. et al. CD4-transgenic zebrafish reveal tissue-resident Th2-and regulatory T cell–like populations and diverse mononuclear phagocytes. J. Immunol. 197, 3520–3530 (2016).
pubmed: 27694495 pmcid: 5073357 doi: 10.4049/jimmunol.1600959
Luckheeram, R. V., Zhou, R., Verma, A. D. & Xia, B. CD4+ T cells: differentiation and functions. Clin. developmental Immunol. 2012, 925135 (2012).
doi: 10.1155/2012/925135
Onishi, R. M. & Gaffen, S. L. Interleukin‐17 and its target genes: mechanisms of interleukin‐17 function in disease. Immunology 129, 311–321 (2010).
pubmed: 20409152 pmcid: 2826676 doi: 10.1111/j.1365-2567.2009.03240.x
Wang, L. et al. The zinc finger transcription factor Zbtb7b represses CD8-lineage gene expression in peripheral CD4+ T cells. Immunity 29, 876–887 (2008).
pubmed: 19062319 pmcid: 3392968 doi: 10.1016/j.immuni.2008.09.019
Matz, H. et al. Organized B cell sites in cartilaginous fishes reveal the evolutionary foundation of germinal centers. Cell Rep. 42, 112664 (2023).
pubmed: 37342909 pmcid: 10529500 doi: 10.1016/j.celrep.2023.112664
Huang, Y. et al. Discovery of an unconventional lamprey lymphocyte lineage highlights divergent features in vertebrate adaptive immune system evolution. https://doi.org/10.1038/s41467-024-51763-2 . NCOMMS-23-60270C.
Busslinger, M. Transcriptional control of early B cell development. Annu Rev. Immunol. 22, 55–79 (2004).
pubmed: 15032574 doi: 10.1146/annurev.immunol.22.012703.104807
Rabinovitch, A., Suarez-Pinzon, W. L., Lapchak, P. H., Meager, A. & Power, R. F. Tumor necrosis factor mediates the protective effect of Freund’s adjuvant against autoimmune diabetes in BB rats. J. Autoimmun. 8, 357–366 (1995).
pubmed: 7575997 doi: 10.1006/jaut.1995.0028
Desjardins, M., Houde, M. & Gagnon, E. Phagocytosis: the convoluted way from nutrition to adaptive immunity. Immunol. Rev. 207, 158–165 (2005).
pubmed: 16181334 doi: 10.1111/j.0105-2896.2005.00319.x
Stuart, L. M. & Ezekowitz, R. A. Phagocytosis: elegant complexity. Immunity 22, 539–550 (2005).
pubmed: 15894272 doi: 10.1016/j.immuni.2005.05.002
Bauer, S. R., Holmes, K. L., Morse, H. C. 3rd & Potter, M. Clonal relationship of the lymphoblastic cell line P388 to the macrophage cell line P388D1 as evidenced by immunoglobulin gene rearrangements and expression of cell surface antigens. J. Immunol. 136, 4695–4699 (1986).
pubmed: 3086440 doi: 10.4049/jimmunol.136.12.4695
Hanecak, R., Zovich, D. C., Pattengale, P. K. & Fan, H. Differentiation in vitro of a leukemia virus-induced B-cell lymphoma into macrophages. Mol. Cell Biol. 9, 2264–2268 (1989).
pubmed: 2546061 pmcid: 363027
Star, B. et al. The genome sequence of Atlantic cod reveals a unique immune system. Nature 477, 207–210 (2011).
pubmed: 21832995 pmcid: 3537168 doi: 10.1038/nature10342
Swann, J. B., Holland, S. J., Petersen, M., Pietsch, T. W. & Boehm, T. The immunogenetics of sexual parasitism. Science 369, 1608–1615 (2020).
pubmed: 32732279 doi: 10.1126/science.aaz9445
Klein, J. & Figueroa, F. Evolution of the major histocompatibility complex. Crit. Rev. Immunol. 6, 295–386 (1986).
pubmed: 3536303
Rowe, R. G., Mandelbaum, J., Zon, L. I. & Daley, G. Q. Engineering hematopoietic stem cells: lessons from development. Cell Stem Cell 18, 707–720 (2016).
pubmed: 27257760 pmcid: 4911194 doi: 10.1016/j.stem.2016.05.016
Haas, S., Trumpp, A. & Milsom, M. D. Causes and consequences of hematopoietic stem cell heterogeneity. Cell Stem Cell 22, 627–638 (2018).
pubmed: 29727678 doi: 10.1016/j.stem.2018.04.003
Kang, J. & Malhotra, N. Transcription factor networks directing the development, function, and evolution of innate lymphoid effectors. Annu Rev. Immunol. 33, 505–538 (2015).
pubmed: 25650177 pmcid: 4674156 doi: 10.1146/annurev-immunol-032414-112025
Vivier, E., van de Pavert, S. A., Cooper, M. D. & Belz, G. T. The evolution of innate lymphoid cells. Nat. Immunol. 17, 790–794 (2016).
pubmed: 27328009 pmcid: 5287353 doi: 10.1038/ni.3459
Dai, H. et al. PIRs mediate innate myeloid cell memory to nonself MHC molecules. Science 368, 1122–1127 (2020).
pubmed: 32381589 pmcid: 7379379 doi: 10.1126/science.aax4040
Huang, Y. et al. Single-cell transcriptome landscape of zebrafish liver reveals hepatocytes and immune cell interactions in understanding nonalcoholic fatty liver disease. Fish Shellfish Immunol 146, 109428 (2024).
Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).
pubmed: 23104886 doi: 10.1093/bioinformatics/bts635
Tarasov, A., Vilella, A. J., Cuppen, E., Nijman, I. J. & Prins, P. Sambamba: fast processing of NGS alignment formats. Bioinformatics 31, 2032–2034 (2015).
pubmed: 25697820 pmcid: 4765878 doi: 10.1093/bioinformatics/btv098
Satija, R., Farrell, J. A., Gennert, D., Schier, A. F. & Regev, A. Spatial reconstruction of single-cell gene expression data. Nat. Biotechnol. 33, 495–502 (2015).
pubmed: 25867923 pmcid: 4430369 doi: 10.1038/nbt.3192
McGinnis, C. S., Murrow, L. M. & Gartner, Z. J. DoubletFinder: doublet detection in single-cell RNA sequencing data using artificial nearest neighbors. Cell Syst. 8, 329–337.e324 (2019).
pubmed: 30954475 pmcid: 6853612 doi: 10.1016/j.cels.2019.03.003
Linderman, G. C., Rachh, M., Hoskins, J. G., Steinerberger, S. & Kluger, Y. Fast interpolation-based t-SNE for improved visualization of single-cell RNA-seq data. Nat. methods 16, 243–245 (2019).
pubmed: 30742040 pmcid: 6402590 doi: 10.1038/s41592-018-0308-4
Emms, D. M. & Kelly, S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 20, 1–14 (2019).
doi: 10.1186/s13059-019-1832-y
Crow, M., Paul, A., Ballouz, S., Huang, Z. J. & Gillis, J. Characterizing the replicability of cell types defined by single cell RNA-sequencing data using MetaNeighbor. Nat. Commun. 9, 1–12 (2018).
doi: 10.1038/s41467-018-03282-0
Kanehisa, M. & Goto, S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28, 27–30 (2000).
pubmed: 10592173 pmcid: 102409 doi: 10.1093/nar/28.1.27
Larkin, M. A. et al. Clustal W and clustal X version 2.0. Bioinformatics 23, 2947–2948 (2007).
pubmed: 17846036 doi: 10.1093/bioinformatics/btm404
Robert, X. & Gouet, P. Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res 42, W320–324 (2014).
pubmed: 24753421 pmcid: 4086106 doi: 10.1093/nar/gku316
Arrigucci, R. et al. FISH-Flow, a protocol for the concurrent detection of mRNA and protein in single cells using fluorescence in situ hybridization and flow cytometry. Nat. Protoc. 12, 1245–1260 (2017).
pubmed: 28518171 pmcid: 5548662 doi: 10.1038/nprot.2017.039
Chen, T. et al. The genome sequence archive family: toward explosive data growth and diverse data types. Genomics Proteom. Bioinforma. 19, 578–583 (2021).
doi: 10.1016/j.gpb.2021.08.001
Database Resources of the National Genomics Data Center, China National Center for Bioinformation in 2022. Nucleic Acids Res 50, D27-d38, https://doi.org/10.1093/nar/gkab951 (2022).

Auteurs

Hong-Yan Wang (HY)

State Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, Shandong, 266071, China.
Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Qingdao, Shandong, 266237, China.

Jian-Yang Chen (JY)

BGI Research, Qingdao, 266555, China.
Qingdao Key Laboratory of Marine Genomics, BGI Research, Qingdao, 266555, Shandong, China.

Yanan Li (Y)

State Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, Shandong, 266071, China.
Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Qingdao, Shandong, 266237, China.
College of Fisheries and Life Science, Shanghai Ocean University, Shanghai, 201306, China.

Xianghui Zhang (X)

State Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, Shandong, 266071, China.
Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Qingdao, Shandong, 266237, China.

Xiang Liu (X)

State Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, Shandong, 266071, China.
Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Qingdao, Shandong, 266237, China.
Qingdao-Europe Advanced Institute for Life Sciences, BGI Research, Qingdao, 266555, China.

Yifang Lu (Y)

State Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, Shandong, 266071, China.
Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Qingdao, Shandong, 266237, China.

Hang He (H)

BGI Research, Qingdao, 266555, China.
Qingdao Key Laboratory of Marine Genomics, BGI Research, Qingdao, 266555, Shandong, China.

Yubang Li (Y)

State Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, Shandong, 266071, China.
Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Qingdao, Shandong, 266237, China.

Hongxi Chen (H)

BGI Research, Qingdao, 266555, China.
Qingdao Key Laboratory of Marine Genomics, BGI Research, Qingdao, 266555, Shandong, China.

Qun Liu (Q)

BGI Research, Qingdao, 266555, China.
Qingdao Key Laboratory of Marine Genomics, BGI Research, Qingdao, 266555, Shandong, China.

Yingyi Huang (Y)

State Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, Shandong, 266071, China.
Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Qingdao, Shandong, 266237, China.

Zhao Jia (Z)

Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai, 201306, China.

Shuo Li (S)

State Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, Shandong, 266071, China.
Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Qingdao, Shandong, 266237, China.

Yangqing Zhang (Y)

State Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, Shandong, 266071, China.
Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Qingdao, Shandong, 266237, China.

Shenglei Han (S)

State Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, Shandong, 266071, China.
Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Qingdao, Shandong, 266237, China.

Shuhong Jiang (S)

State Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, Shandong, 266071, China.
Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Qingdao, Shandong, 266237, China.

Mingming Yang (M)

BGI Research, Qingdao, 266555, China.
Qingdao Key Laboratory of Marine Genomics, BGI Research, Qingdao, 266555, Shandong, China.

Yingying Zhang (Y)

BGI Research, Qingdao, 266555, China.
Qingdao Key Laboratory of Marine Genomics, BGI Research, Qingdao, 266555, Shandong, China.

Li Zhou (L)

BGI Research, Qingdao, 266555, China.
Qingdao Key Laboratory of Marine Genomics, BGI Research, Qingdao, 266555, Shandong, China.

Fujian Tan (F)

BGI Research, Qingdao, 266555, China.
Qingdao Key Laboratory of Marine Genomics, BGI Research, Qingdao, 266555, Shandong, China.

Qianyue Ji (Q)

MGI Tech, Shenzhen, 518083, China.

Liang Meng (L)

BGI Research, Qingdao, 266555, China.
Qingdao Key Laboratory of Marine Genomics, BGI Research, Qingdao, 266555, Shandong, China.

Rui Wang (R)

State Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, Shandong, 266071, China.
Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Qingdao, Shandong, 266237, China.

Yuyan Liu (Y)

State Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, Shandong, 266071, China.
Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Qingdao, Shandong, 266237, China.

Kaiqiang Liu (K)

State Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, Shandong, 266071, China.
Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Qingdao, Shandong, 266237, China.

Qian Wang (Q)

State Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, Shandong, 266071, China.
Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Qingdao, Shandong, 266237, China.

Inge Seim (I)

Integrative Biology Laboratory, College of Life Sciences, Nanjing Normal University, Nanjing, 210023, China.
School of Biology and Environmental Science, Queensland University of Technology, Brisbane, 4000, Australia.

Jun Zou (J)

Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai, 201306, China.

Guangyi Fan (G)

BGI Research, Qingdao, 266555, China.
Qingdao Key Laboratory of Marine Genomics, BGI Research, Qingdao, 266555, Shandong, China.
BGI Research, Shenzhen, 518083, China.

Shanshan Liu (S)

MGI Tech, Shenzhen, 518083, China. liushanshan@mgi-tech.com.

Changwei Shao (C)

State Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, Shandong, 266071, China. shaocw@ysfri.ac.cn.
Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Qingdao, Shandong, 266237, China. shaocw@ysfri.ac.cn.

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