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SCIENCE CHINA Life Sciences, Volume 62, Issue 4: 566-578(2019) https://doi.org/10.1007/s11427-019-9481-8

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

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  • ReceivedNov 2, 2018
  • AcceptedNov 28, 2018
  • PublishedMar 27, 2019

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.


Funded by

the National Natural Science Foundation of China(31372190)


Acknowledgment

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


Interest statement

The author(s) declare that they have no conflict of interest.


Supplement

SUPPORTING INFORMATION

File S1 The TLRs protein sequences

Table S1 TLR and relevant signal genes queries list

Table S2 TLRs annotation results

Table S3 TLR4 protein sequences identity matrix

Table S4 TLR relevant signal genes annotation results

Table S5 RLR genes queries list

Table S6 RLRs and signal relevant genes annotation results

Table S7 NLR genes queries list

Table S8 NLR annotation results

Table S9 CLR genes queries list

Table S10 CLR annotation results

Figure S1 Structure of TLR5 proteins.

Figure S2 TLR4 protein sequences alignment.

The supporting information is available online at http://life.scichina.com and https://link.springer.com. The supporting materials are published as submitted, without typesetting or editing. The responsibility for scientific accuracy and content remains entirely with the authors.


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  • Figure 1

    Phylogenetic relationship of TLR was constructed using maximum likelihood method with the most suitable substitution model LG+G. The tree was built by Phyml Version 3.0 (Guindon et al., 2010) with 1,000 bootstrap replications. Percent bootstrap support for major nodes are shown. Blue, beige, yellow, green, purple and red represent TLR1, TLR3, TLR4, TLR5, TLR7 and TLR11 subfamily, respectively. Gene name marked by corresponding branch color means NTR fishes.

  • Figure 2

    Summary of evolution of Toll-like receptors in vertebrates. Phylogenetic tree of species is mainly based on other research (Amemiya et al., 2013). The topological structure of the species tree only reflects the relationship between species. The gain and loss of different TLRs are marked in the node by green and red color, respectively. The counts of TLR subfamily members of each species are also shown in this figure. The counts of TLR subfamily members in sea squirts are not displayed because their TLRs do not cluster with TLRs in vertebrates.

  • Figure 3

    Functional domains were predicted by the SMART program (Schultz et al., 2000). LRR, LRRCT and TIR mean leucine-rich repeats, leucine-rich repeats C-terminal and Toll/IL-1R domain, respectively. Though alligator gar TLR4al owns TIR domain, it is a pseudogene due to too many stop codons. Spotted gar TLR4ba is not regarded as bona TLR4 because of TIR domain loss.

  • Figure 4

    Phylogenetic relationship of TLR was constructed using maximum likelihood method with the most suitable substitution model JTT+G+I+F. The tree was built by Phyml Version 3.0 (Guindon et al., 2010) with 1,000 bootstrap replications. Green, red, blue background represent DHX58 (LGP2), IFIH1 (MDA5) and DDX58 (RIG-I), respectively. The NTR fishes are marked in red. The accession numbers of reference sequences included are DHX58 (XP_003964848), IFIH1 (XP_011608567.1) in Fugu, DHX58 (NP_001015545), IFIH1 (XP_010800355), DDX58 (XP_002689526) in cow (Bos Taurus), DHX58 (XP_008108586), DDX58 (XP_008118557), IFIH1 (XP_003226281) in anole lizard (Anolis carolinensis).

  • Figure 5

    TLR and RLR signal pathway of inducing type I IFN. This figure shows how TLR7/8/9 and TLR3 rely on MyD88-dependent and TRIF-dependent pathway respectively, inducing the production of type I IFN. MyD88 recruits IRAKs and activates TRAF6 and the IκB kinase (IKK), then produces IFN after NF-κB is transferred to the nucleus (Li et al., 2017). Tripartite motif containing 25 (TRIM25) may trigger the ubiquitination of MAVS (Bruns and Horvath, 2012), which facilitates phosphorylation of ITN regulatory factor and initiates antiviral signaling. Green color indicates genes existing in the NTR fish. Light grey indicates genes absent partly in the five fish, and dark grey in the small circle indicates genes absent in the corresponding fish.

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