Immunogenetic losses co-occurred with seahorse male pregnancy and mutation in tlx1 accompanied functional asplenia

Liu, Yali; Qu, Meng; Jiang, Han; Schneider, Ralf; Qin, Geng; Luo, Wei; Yu, Haiyan; Zhang, Bo; Wang, Xin; Zhang, Yanhong; Zhang, Huixian; Zhang, Zhixin; Wu, Yongli; Yin, Jingdong; Zhang, Si; Venkatesh, Byrappa; Roth, Olivia; Meyer, Axel; Lin, Qiang

doi:10.1038/s41467-022-35338-7

Cited by 16 publications

(14 citation statements)

References 73 publications

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“…It is noteworthy that amino acid indels occur less frequently compared to substitutions, indicating that indels are less likely to occur during evolution than substitutions ( Chen et al 2009 ). As expected, a Hippocampus -specific amino acid substitution in tlx1 has been identified (see case results in the website), which probably contributes to the loss of spleen in seahorses ( Liu et al 2022 ).…”

Section: Case Study 2: Hippocampus -Specific Amino...supporting

confidence: 73%

“…The monophyly of syngnathids has been supported in recent phylogenomic studies ( Hamilton et al 2017 , Longo et al 2017 , Santaquiteria et al 2021 , Stiller et al 2022 ). Sequencing of syngnathid genomes has prompted the investigation of the genetic basis underlying the phenotypic evolution, such as the male brooding pouch ( Lin et al 2016 , Small et al 2016 , Zhang et al 2020 ), leaf-like appendages ( Qu et al 2021 , Small et al 2022 ), and loss of teeth and spleen ( Liu et al 2022 ).…”

Section: Case Study 2: Hippocampus -Specific Amino...mentioning

confidence: 99%

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WGCCRR: a web-based tool for genome-wide screening of convergent indels and substitutions of amino acids

Dong,

Wang,

2024

Bioinformatics Advances

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Genome-wide analyses of protein-coding gene sequences are being employed to examine the genetic basis of adaptive evolution in many organismal groups. Previous studies have revealed that convergent/parallel adaptive evolution may be caused by convergent/parallel amino acid changes. Similarly, detailed analysis of lineage-specific amino acid changes has shown correlations with certain lineage-specific traits. However, experimental validation remains the ultimate measure of causality. With the increasing availability of genomic data, a streamlined tool for such analyses would facilitate and expedite the screening of genetic loci that hold potential for adaptive evolution, while alleviating the bioinformatic burden for experimental biologists. In this study, we present a user-friendly web-based tool called WGCCRR (Whole Genome Comparative Coding Region Read) designed to screen both convergent/parallel and lineage-specific amino acid changes on a genome-wide scale. Our tool allows users to replicate previous analyses with just a few clicks, and the exported results are straightforward to interpret. In addition, we have also included amino acid indels that are usually neglected in previous work. Our website provides an efficient platform for screening candidate loci for downstream experimental tests. It is available at: https://fishevo.xmu.edu.cn/.

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Section: Case Study 2: Hippocampus -Specific Amino...supporting

confidence: 73%

Section: Case Study 2: Hippocampus -Specific Amino...mentioning

confidence: 99%

WGCCRR: a web-based tool for genome-wide screening of convergent indels and substitutions of amino acids

Dong,

Wang,

2024

Bioinformatics Advances

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“…Given the qualitative and quantitative differences between foxn1driven and foxn4-driven thymopoietic environments, we set out to determine the status of these genes in deep-sea anglerfishes. We also included the tlx1 gene in our survey, which encodes a transcription factor that is specifically required for the development of the spleen in mammals [33][34][35] and teleosts [36,37]. The spleen is an important lymphoid organ that orchestrates both innate and adaptive immune reactions [38] and is therefore expected to be present in all species of deep-sea anglerfishes, even in those that lack canonical adaptive immunity.…”

Section: Distinct Immunogenomes Of Deep-sea Anglerfishesmentioning

confidence: 99%

Foxn1 is not essential for T‐cell development in teleosts

Schorpp,

Swann,

Hess

et al. 2023

Eur J Immunol

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In mammals, T cell development depends on the activity of the Foxn1 transcription factor in the thymic epithelium; mutations in the vertebrate‐specific Foxn1 gene are associated with profound T cell lymphopenia and fatal immunodeficiency. Here, we examined the extent of T cell development in teleosts lacking a functional foxn1 gene. In zebrafish carrying a deleterious internal deletion of foxn1, reduced but robust lymphopoietic activity is maintained in the mutant thymus. Moreover, pseudogenization or loss of foxn1 in the genomes of deep‐sea anglerfishes is independent of the presence or absence of the canonical signatures of the T cell lineage. Thus, in contrast to the situation in mammals, the teleost thymus can support foxn1‐independent lymphopoiesis, most likely through the activity of the Foxn4, an ancient metazoan paralog of Foxn1. Our results imply that during early stages of vertebrate evolution, genetic control of thymopoiesis was functionally redundant and thus robust; in mammals, the genetic network was reorganized to become uniquely dependent on the FOXN1 transcription factor.This article is protected by copyright. All rights reserved

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“…The Syngnathidae family comprises seahorses, pipefish, and sea dragons, which are well known for their unique male pregnancy ( 5 , 6 ). Males of most syngnathid species have evolved a brood pouch that function similarly to the mammalian uterus ( 7 , 8 ).…”

Section: Introductionmentioning

confidence: 99%

Gene loss and co-option of toll-like receptors facilitate paternal immunological adaptation in the brood pouch of pregnant male seahorses

Zhang,

Xiao,

Qin

et al. 2023

Front. Immunol.

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Male pregnancy in syngnathids (seahorses, pipefishes, and sea dragons) is an evolutionary innovation in the animal kingdom. Paternal immune resistance to the fetus is a critical challenge, particularly in seahorses with fully enclosed brood pouches and sophisticated placentas. In this study, comparative genomic analysis revealed that all syngnathid species lost three vertebrate-conserved Toll-like receptors (TLR1, TLR2, and TLR9), of which all play essential roles in immune protection and immune tolerance in the uterus and placenta. Quantitative real-time PCR (qRT-PCR) analysis showed that the TLR paralog genes including TLR18, TLR25, and TLR21 were highly expressed in the placenta inside the seahorse brood pouch and changed dynamically during the breeding cycle, suggesting the potentially important role of the TLRs during male pregnancy. Furthermore, the immune challenge test in vitro showed a remarkable expression response from all three TLR genes to specific pathogenic antigens, confirming their immune function in seahorse brood pouches. Notably, the altered antigen recognition spectrum of these genes appeared to functionally compensate in part for the lost TLRs, in contrast to that observed in other species. Therefore, we suggest that gene loss and co-option of TLRs may be a typical evolutionary strategy for facilitating paternal immunological adaptation during male pregnancy.

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Immunogenetic losses co-occurred with seahorse male pregnancy and mutation in tlx1 accompanied functional asplenia

Cited by 16 publications

References 73 publications

WGCCRR: a web-based tool for genome-wide screening of convergent indels and substitutions of amino acids

WGCCRR: a web-based tool for genome-wide screening of convergent indels and substitutions of amino acids

Foxn1 is not essential for T‐cell development in teleosts

Gene loss and co-option of toll-like receptors facilitate paternal immunological adaptation in the brood pouch of pregnant male seahorses

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