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

文献类型： 外文期刊

作者： Zhang, Bo 1 ; Xiao, Wanghong 3 ; Qin, Geng 3 ; Chen, Zelin 3 ; Qiu, Lihua 1 ; Wang, Xin 3 ; Lin, Qiang 3 ;

作者机构： 1.Chinese Acad Fishery Sci, South China Sea Fisheries Res Inst, Key Lab South China Sea Fishery Resources Exploita, Minist Agr & Rural Affairs, Guangzhou, Peoples R China

2.Chinese Acad Fishery Sci, South China Sea Fisheries Res Inst, Key Lab Aquat Prod Proc, Minist Agr & Rural Affairs, Guangzhou, Peoples R China

3.Chinese Acad Sci, South China Sea Inst Oceanol, CAS Key Lab Trop Marine Bioresources & Ecol, Guangzhou, Peoples R China

4.Chinese Acad Sci, South China Sea Inst Oceanol, Southern Marine Sci & Engn Guangdong Lab Guangzhou, Guangzhou, Peoples R China

5.Sanya Inst Ocean Ecoenvironm Engn, Sanya, Peoples R China

关键词： seahorse; pregnancy; immune tolerance; host resistance; toll-like receptor

期刊名称：FRONTIERS IN IMMUNOLOGY （ 影响因子：7.3； 五年影响因子：8.0 ）

ISSN： 1664-3224

年卷期： 2023 年 14 卷

页码：

收录情况： SCI

摘要： 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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