Skip to main content
SpringerLink
Log in

Comparative study on pattern recognition receptors in non-teleost ray-finned fishes and their evolutionary significance in primitive vertebrates

  • Research Paper
  • Published:
Science China Life Sciences Aims and scope Submit manuscript

Abstract

Pattern recognition receptors (PRRs) play important roles in innate immunity system and trigger the specific pathogen recognition by detecting the pathogen-associated molecular patterns. The main four PRRs components including Toll-like receptors (TLRs), RIG-I-like receptors (RLRs), NOD-like receptors (NLRs) and C-type lectin receptors (CLRs) were surveyed in the five genomes of non-teleost ray-finned fishes (NTR) including bichir (Polypterus senegalus), American paddlefish (Polyodon spathula), alligator gar (Atractosteus spatula), spotted gar (Lepisosteus oculatus) and bowfin (Amia calva), representing all the four major basal groups of ray-finned fishes. The result indicates that all the four PRRs components have been well established in these NTR fishes. In the RLR-MAVS signal pathway, which detects intracellular RNA ligands to induce production of type I interferons (IFNs), the MAVS was lost in bichir particularly. Also, the essential genes of recognition of Lipopolysaccharide (LPS) commonly in mammals like MD2, LY96 and LBP could not be identified in NTR fishes. It is speculated that TLR4 in NTR fishes may act as a cooperator with other PRRs and has a different pathway of recognizing LPS compared with that in mammals. In addition, we provide a survey of NLR and CLR in NTR fishes. The CLRs results suggest that Group V receptors are absent in fishes and Group II and VI receptors are well established in the early vertebrate evolution. Our comprehensive research of PRRs involving NTR fishes provides a new insight into PRR evolution in primitive vertebrate.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Amemiya, C.T., Alföldi, J., Lee, A.P., Fan, S., Philippe, H., Maccallum, I., Braasch, I., Manousaki, T., Schneider, I., Rohner, N., et al. (2013). The african coelacanth genome provides insights into tetrapod evolution. Nature 496, 311–316.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berczi, I., Bertók, L., and Bereznai, T. (1966). Comparative studies on the toxicity of Escherichia coli lipopolysaccharide endotoxin in various animal species. Can J Microbiol 12, 1070–1071.

    Article  CAS  PubMed  Google Scholar 

  • Bilodeau, A.L., and Waldbieser, G.C. (2005). Activation of TLR3 and TLR5 in channel catfish exposed to virulent Edwardsiella ictaluri. Dev Comp Immunol 29, 713–721.

    Article  CAS  PubMed  Google Scholar 

  • Birney, E., Clamp, M., and Durbin, R. (2004). Genewise and genomewise. Genome Res 14, 988–995.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boudinot, P., Zou, J., Ota, T., Buonocore, F., Scapigliati, G., Canapa, A., Cannon, J., Litman, G., and Hansen, J.D. (2014). A tetrapod-like repertoire of innate immune receptors and effectors for coelacanths. J Exp Zool (Mol Dev Evol) 322, 415–437.

    Article  CAS  Google Scholar 

  • Brown, G.D., Willment, J.A., and Whitehead, L. (2018). C-type lectins in immunity and homeostasis. Nat Rev Immunol 18, 374–389.

    Article  CAS  PubMed  Google Scholar 

  • Brownlie, R., and Allan, B. (2011). Avian toll-like receptors. Cell Tissue Res 343, 121–130.

    Article  CAS  PubMed  Google Scholar 

  • Bruns, A.M., and Horvath, C.M. (2012). Activation of RIG-I-like receptor signal transduction. Crit Rev Biochem Mol Biol 47, 194–206.

    Article  CAS  PubMed  Google Scholar 

  • Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., and Madden, T.L. (2009). Blast+: Architecture and applications. BMC BioInf 10, 421.

    Article  CAS  Google Scholar 

  • Chen, S.N., Zou, P.F., and Nie, P. (2017). Retinoic acid-inducible gene I (RIG-I)-like receptors (RLRs) in fish: Current knowledge and future perspectives. Immunology 151, 16–25.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen, W.Q., Hu, Y.W., Zou, P.F., Ren, S.S., Nie, P., and Chang, M.X. (2015). MAVS splicing variants contribute to the induction of interferon and interferon-stimulated genes mediated by RIG-I-like receptors. Dev Comp Immunol 49, 19–30.

    Article  CAS  PubMed  Google Scholar 

  • Dambuza, I.M., and Brown, G.D. (2015). C-type lectins in immunity: Recent developments. Curr Opin Immunol 32, 21–27.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drickamer, K., and Taylor, M.E. (2015). Recent insights into structures and functions of C-type lectins in the immune system. Curr Opin Struct Biol 34, 26–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edgar, R.C. (2004). Muscle: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32, 1792–1797.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feng, X., Zhang, Y., Yang, C., Liao, L., Wang, Y., and Su, J. (2015). Functional characterizations of IPS-1 in cik cells: Potential roles in regulating IFN-I response dependent on IFN-7 but not irf3. Dev Comp Immunol 53, 23–32.

    Article  CAS  PubMed  Google Scholar 

  • Gao, D., Wu, J., Wu, Y.T., Du, F., Aroh, C., Yan, N., Sun, L., and Chen, Z.J. (2013). Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses. Science 341, 903–906.

    Article  CAS  PubMed  Google Scholar 

  • Geijtenbeek, T.B.H., and Gringhuis, S.I. (2016). C-type lectin receptors in the control of T helper cell differentiation. Nat Rev Immunol 16, 433–448.

    Article  CAS  PubMed  Google Scholar 

  • Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W., and Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of phyml 3.0. Systatic Biol 59, 307–321.

    Article  CAS  Google Scholar 

  • Hall, T.A. (1999). Bioedit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Series 41, 95–98.

    CAS  Google Scholar 

  • Hibino, T., Loza-Coll, M., Messier, C., Majeske, A.J., Cohen, A.H., Terwilliger, D.P., Buckley, K.M., Brockton, V., Nair, S.V., Berney, K., et al. (2006). The immune gene repertoire encoded in the purple sea urchin genome. Dev Biol 300, 349–365.

    Article  CAS  PubMed  Google Scholar 

  • Howe, K., Schiffer, P.H., Zielinski, J., Wiehe, T., Laird, G.K., Marioni, J.C., Soylemez, O., Kondrashov, F., and Leptin, M. (2016). Structure and evolutionary history of a large family of NLR proteins in the zebrafish. Open Biol 6, 160009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang, R., Dong, F., Jang, S., Liao, L., Zhu, Z., and Wang, Y. (2012). Isolation and analysis of a novel grass carp toll-like receptor 4 (TLR4) gene cluster involved in the response to grass carp reovirus. Dev Comp Immunol 38, 383–388.

    Article  CAS  PubMed  Google Scholar 

  • Huang, S., Yuan, S., Guo, L., Yu, Y., Li, J., Wu, T., Liu, T., Yang, M., Wu, K., Liu, H., et al. (2008). Genomic analysis of the immune gene repertoire of amphioxus reveals extraordinary innate complexity and diversity. Genome Res 18, 1112–1126.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hwang, S.D., Asahi, T., Kondo, H., Hirono, I., and Aoki, T. (2010). Molecular cloning and expression study on toll-like receptor 5 paralogs in Japanese flounder, Paralichthys olivaceus. Fish Shellfish Immunol 29, 630–638.

    Article  CAS  PubMed  Google Scholar 

  • Iliev, D.B., Roach, J.C., Mackenzie, S., Planas, J.V., and Goetz, F.W. (2005). Endotoxin recognition: In fish or not in fish? FEBS Lett 579, 6519–6528.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ishii, A., Kawasaki, M., Matsumoto, M., Tochinai, S., and Seya, T. (2007a). Phylogenetic and expression analysis of amphibian xenopus toll-like receptors. Immunogenetics 59, 281–293.

    Article  CAS  PubMed  Google Scholar 

  • Ishii, A., Matsuo, A., Sawa, H., Tsujita, T., Shida, K., Matsumoto, M., and Seya, T. (2007b). Lamprey TLRs with properties distinct from those of the variable lymphocyte receptors. J Immunol 178, 397–406.

    Article  CAS  PubMed  Google Scholar 

  • Jault, C., Pichon, L., and Chluba, J. (2004). Toll-like receptor gene family and TIR-domain adapters in Danio rerio. Mol Immunol 40, 759–771.

    Article  CAS  PubMed  Google Scholar 

  • Jia, P., Jin, Y., Chen, L., Zhang, J., Jia, K., and Yi, M. (2016). Molecular characterization and expression analysis of mitochondrial antiviral signaling protein gene in sea perch, lateolabrax japonicus. Dev Comp Immunol 55, 188–193.

    Article  CAS  PubMed  Google Scholar 

  • Kasamatsu, J., Oshiumi, H., Matsumoto, M., Kasahara, M., and Seya, T. (2010). Phylogenetic and expression analysis of lamprey toll-like receptors. Dev Comp Immunol 34, 855–865.

    Article  CAS  PubMed  Google Scholar 

  • Kawai, T., and Akira, S. (2011). Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34, 637–650.

    Article  CAS  PubMed  Google Scholar 

  • Kufer, T.A., and Sansonetti, P.J. (2011). NLR functions beyond pathogen recognition. Nat Immunol 12, 121–128.

    Article  CAS  PubMed  Google Scholar 

  • Laing, K.J., Purcell, M.K., Winton, J.R., and Hansen, J.D. (2008). A genomic view of the nod-like receptor family in teleost fish: Identification of a novel NLR subfamily in zebrafish. BMC Evol Biol 8, 42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Le, S.Q., and Gascuel, O. (2008). An improved general amino acid replacement matrix. Mol Biol Evol 25, 1307–1320.

    Article  CAS  PubMed  Google Scholar 

  • Lefort, V., Longueville, J.E., and Gascuel, O. (2017). SMS: Smart model selection in PhyML. Mol Biol Evol 34, 2422–2424.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, J., Chu, Q., and Xu, T. (2016). A genome-wide survey of expansive NLR-C subfamily in miiuy croaker and characterization of the NLRB30.2 genes. Dev Comp Immunol 61, 116–125.

    Article  CAS  PubMed  Google Scholar 

  • Li, Y., Li, Y., Cao, X., Jin, X., and Jin, T. (2017). Pattern recognition receptors in zebrafish provide functional and evolutionary insight into innate immune signaling pathways. Cell Mol Immunol 14, 80–89.

    Article  CAS  PubMed  Google Scholar 

  • Loo, Y.M., and Gale Jr., M. (2011). Immune signaling by RIG-I-like receptors. Immunity 34, 680–692.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meijer, A.H., Gabby Krens, S.F., Medina Rodriguez, I.A., He, S., Bitter, W., Ewa Snaar-Jagalska, B., and Spaink, H.P. (2004). Expression analysis of the Toll-like receptor and TIR domain adaptor families of zebrafish. Mol Immunol 40, 773–783.

    Article  CAS  PubMed  Google Scholar 

  • Meunier, E., and Broz, P. (2017). Evolutionary convergence and divergence in NLR function and structure. Trends Immunol 38, 744–757.

    Article  CAS  PubMed  Google Scholar 

  • Mukherjee, K., Korithoski, B., and Kolaczkowski, B. (2014). Ancient origins of vertebrate-specific innate antiviral immunity. Mol Biol Evol 31, 140–153.

    Article  CAS  PubMed  Google Scholar 

  • Onoguchi, K., Yoneyama, M., and Fujita, T. (2011). Retinoic acid-inducible gene-I-like receptors. J Interf Cytok Res 31, 27–31.

    Article  CAS  Google Scholar 

  • Oshiumi, H., Tsujita, T., Shida, K., Matsumoto, M., Ikeo, K., and Seya, T. (2003). Prediction of the prototype of the human toll-like receptor gene family from the pufferfish, Fugu rubripes, genome. Immunogenetics 54, 791–800.

    CAS  PubMed  Google Scholar 

  • Palti, Y. (2011). Toll-like receptors in bony fish: From genomics to function. Dev Comp Immunol 35, 1263–1272.

    Article  CAS  PubMed  Google Scholar 

  • Panagos, P.G., Dobrinski, K.P., Chen, X., Grant, A.W., Traver, D., Djeu, J. Y., Wei, S., and Yoder, J.A. (2006). Immune-related, lectin-like receptors are differentially expressed in the myeloid and lymphoid lineages of zebrafish. Immunogenetics 58, 31–40.

    Article  CAS  PubMed  Google Scholar 

  • Petersen, T.N., Brunak, S., von Heijne, G., and Nielsen, H. (2011). Signalp 4.0: Discriminating signal peptides from transmembrane regions. Nat Methods 8, 785–786.

    Article  CAS  PubMed  Google Scholar 

  • Pietretti, D., Scheer, M., Fink, I.R., Taverne, N., Savelkoul, H.F.J., Spaink, H.P., Forlenza, M., and Wiegertjes, G.F. (2014). Identification and functional characterization of nonmammalian Toll-like receptor 20. Immunogenetics 66, 123–141.

    Article  CAS  PubMed  Google Scholar 

  • Pietretti, D., and Wiegertjes, G.F. (2014). Ligand specificities of toll-like receptors in fish: Indications from infection studies. Dev Comp Immunol 43, 205–222.

    Article  CAS  PubMed  Google Scholar 

  • Quiniou, S.M.A., Boudinot, P., and Bengtén, E. (2013). Comprehensive survey and genomic characterization of toll-like receptors (TLRs) in channel catfish, Ictalurus punctatus: Identification of novel fish TLRs. Immunogenetics 65, 511–530.

    Article  CAS  PubMed  Google Scholar 

  • Raetz, C.R.H., and Whitfield, C. (2002). Lipopolysaccharide endotoxins. Annu Rev Biochem 71, 635–700.

    Article  CAS  PubMed  Google Scholar 

  • Rajendran, K.V., Zhang, J., Liu, S., Kucuktas, H., Wang, X., Liu, H., Sha, Z., Terhune, J., Peatman, E., and Liu, Z. (2012). Pathogen recognition receptors in channel catfish: I. Identification, phylogeny and expression of NOD-like receptors. Dev Comp Immunol 37, 77–86.

    Article  CAS  PubMed  Google Scholar 

  • Rauta, P.R., Samanta, M., Dash, H.R., Nayak, B., and Das, S. (2014). Toll-like receptors (TLRs) in aquatic animals: Signaling pathways, expressions and immune responses. Immunol Lett 158, 14–24.

    Article  CAS  PubMed  Google Scholar 

  • Reikine, S., Nguyen, J.B., and Modis, Y. (2014). Pattern recognition and signaling mechanisms of RIG-I and MDA5. Front Immunol 5.

    Google Scholar 

  • Roach, J.C., Glusman, G., Rowen, L., Kaur, A., Purcell, M.K., Smith, K.D., Hood, L.E., and Aderem, A. (2005). The evolution of vertebrate Toll-like receptors. Proc Natl Acad Sci USA 102, 9577–9582.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sattler, S., Ghadially, H., and Hofer, E. (2012). Evolution of the C-type lectin-like receptor genes of the Dectin-1 cluster in the NK gene complex. Sci World J 2012(13), 1–11.

    Article  CAS  Google Scholar 

  • Schroder, K., and Tschopp, J. (2010). The inflammasomes. Cell 140, 821–832.

    Article  CAS  PubMed  Google Scholar 

  • Schultz, J., Copley, R.R., Doerks, T., Ponting, C.P., and Bork, P. (2000). Smart: A web-based tool for the study of genetically mobile domains. Nucleic Acids Res 28, 231–234.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sepulcre, M.P., Alcaraz-Perez, F., Lopez-Munoz, A., Roca, F.J., Meseguer, J., Cayuela, M.L., and Mulero, V. (2009). Evolution of lipopolysaccharide (LPS) recognition and signaling: Fish TLR4 does not recognize LPS and negatively regulates NF-kB activation. J Immunol 182, 1836–1845.

    Article  CAS  PubMed  Google Scholar 

  • Seth, R.B., Sun, L., Ea, C.K., and Chen, Z.J. (2005). Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-κB and IRF3. Cell 122, 669–682.

    Article  CAS  PubMed  Google Scholar 

  • Shen, B., Hu, Y., Zhang, S., Zheng, J., Zeng, L., Zhang, J., Zhu, A., and Wu, C. (2016). Molecular characterization and expression analyses of three RIG-I-like receptor signaling pathway genes (MDA5, LGP2 and MAVS) in Larimichthys crocea. Fish Shellfish Immunol 55, 535–549.

    Article  CAS  PubMed  Google Scholar 

  • Shimazu, R., Akashi, S., Ogata, H., Nagai, Y., Fukudome, K., Miyake, K., and Kimoto, M. (1999). Md-2, a molecule that confers lipopolysaccharide responsiveness on Toll-like receptor 4. J Exp Med 189, 1777–1782.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith, J.J., Kuraku, S., Holt, C., Sauka-Spengler, T., Jiang, N., Campbell, M.S., Yandell, M.D., Manousaki, T., Meyer, A., Bloom, O.E., et al. (2013). Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution. Nat Genet 45, 415–421.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stein, C., Caccamo, M., Laird, G., and Leptin, M. (2007). Conservation and divergence of gene families encoding components of innate immune response systems in zebrafish. Genome Biol 8, R251.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Su, J., Yang, C., Xiong, F., Wang, Y., and Zhu, Z. (2009). Toll-like receptor 4 signaling pathway can be triggered by grass carp reovirus and Aeromonas hydrophila infection in rare minnow Gobiocypris rarus. Fish Shellfish Immunol 27, 33–39.

    Article  CAS  PubMed  Google Scholar 

  • Sullivan, C., Charette, J., Catchen, J., Lage, C.R., Giasson, G., Postlethwait, J.H., Millard, P.J., and Kim, C.H. (2009). The gene history of zebrafish TLR4a and TLR4b is predictive of their divergent functions. J Immunol 183, 5896–5908.

    Article  CAS  PubMed  Google Scholar 

  • Tahoun, A., Jensen, K., Corripio-Miyar, Y., McAteer, S., Smith, D.G.E., McNeilly, T.N., Gally, D.L., and Glass, E.J. (2017). Host species adaptation of TLR5 signalling and flagellin recognition. Scientific Reports 7.

    Google Scholar 

  • Takeuchi, O., and Akira, S. (2010). Pattern recognition receptors and inflammation. Cell 140, 805–820.

    Article  CAS  PubMed  Google Scholar 

  • Tsoi, S., Park, K.C., Kay, H.H., O’Brien, T.J., Podor, E., Sun, G., Douglas, S.E., Brown, L.L., and Johnson, S.C. (2006). Identification of a transcript encoding a soluble form of toll-like receptor 5 (TLR5) in atlantic salmon during Aeromonas salmonicida infection. Vet Immunol Immunopathol 109, 183–187.

    Article  CAS  PubMed  Google Scholar 

  • Tsujita, T., Tsukada, H., Nakao, M., Oshiumi, H., Matsumoto, M., and Seya, T. (2004). Sensing bacterial flagellin by membrane and soluble orthologs of Toll-like receptor 5 in rainbow trout (Onchorhynchus mikiss). J Biol Chem 279, 48588–48597.

    Article  CAS  PubMed  Google Scholar 

  • Tsukada, H., Fukui, A., Tsujita, T., Matsumoto, M., Iida, T., and Seya, T. (2005). Fish soluble toll-like receptor 5 (TLR5s) is an acute-phase protein with integral flagellin-recognition activity. Int J Mol Med 15, 519–525.

    CAS  PubMed  Google Scholar 

  • Wang, J., Chai, J., and Wang, H. (2016). Structure of the mouse Toll-like receptor 13 ectodomain in complex with a conserved sequence from bacterial 23S ribosomal RNA. FEBS J 283, 1631–1635.

    Article  CAS  PubMed  Google Scholar 

  • Wang, J., Zhang, Z., Liu, J., Li, F., Chang, F., Fu, H., Zhao, J., and Yin, D. (2015). Structural characterization and evolutionary analysis of fish-specific TLR27. Fish Shellfish Immunol 45, 940–945.

    Article  CAS  PubMed  Google Scholar 

  • Wright, S.D., Ramos, R.A., Tobias, P.S., Ulevitch, R.J., and Mathison, J.C. (1990). CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science 249, 1431–1433.

    Article  CAS  PubMed  Google Scholar 

  • Yuen, B., Bayes, J.M., and Degnan, S.M. (2014). The characterization of sponge NLRs provides insight into the origin and evolution of this innate immune gene family in animals. Mol Biol Evol 31, 106–120.

    Article  CAS  PubMed  Google Scholar 

  • Zelensky, A.N., and Gready, J.E. (2005). The C-type lectin-like domain superfamily. FEBS J 272, 6179–6217.

    Article  CAS  PubMed  Google Scholar 

  • Zelensky, A.N., and Gready, J.E. (2004). C-type lectin-like domains in Fugu rubripes. BMC Genomics 5, 51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, J., Kong, X., Zhou, C., Li, L., Nie, G., and Li, X. (2014). Toll-like receptor recognition of bacteria in fish: Ligand specificity and signal pathways. Fish Shellfish Immunol 41, 380–388.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, J., Liu, S., Rajendran, K.V., Sun, L., Zhang, Y., Sun, F., Kucuktas, H., Liu, H., and Liu, Z. (2013). Pathogen recognition receptors in channel catfish: III phylogeny and expression analysis of Toll-like receptors. Dev Comp Immunol 40, 185–194.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, L., Gao, Z., Yu, L., Zhang, B., Wang, J., and Zhou, J. (2018). Nucleotide-binding and oligomerization domain (NOD)-like receptors in teleost fish: Current knowledge and future perspectives. J Fish Dis 41, 1317–1330.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, Z., Yuan, B., Bao, M., Lu, N., Kim, T., and Liu, Y.J. (2011). The helicase DDX41 senses intracellular DNA mediated by the adaptor STING in dendritic cells. Nat Immunol 12, 959–965.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31372190).

Author information

Authors and Affiliations

  1. BGI Education Center, University of Chinese Academy of Sciences, Shenzhen, 518083, China

    Yuming He

  2. China National Genebank, BGI-Shenzhen, Shenzhen, 518083, China

    Yuming He, Hailin Pan & Guojie Zhang

  3. State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, 650223, China

    Hailin Pan & Guojie Zhang

  4. Centre for Social Evolution, Department of Biology, Universitetsparken 15, University of Copenhagen, DK-2100, Copenhagen, Denmark

    Hailin Pan & Guojie Zhang

  5. Key Laboratory of Aquatic Biodiversity and Conservation of the Chinese Academy of Sciences, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, China

    Shunping He

Authors
  1. Yuming He
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hailin Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guojie Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shunping He
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Guojie Zhang or Shunping He.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

He, Y., Pan, H., Zhang, G. et al. Comparative study on pattern recognition receptors in non-teleost ray-finned fishes and their evolutionary significance in primitive vertebrates. Sci. China Life Sci. 62, 566–578 (2019). https://doi.org/10.1007/s11427-019-9481-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11427-019-9481-8

Keywords

Search

Navigation