A comparative transcriptomic analysis provides new insights into the ecological adaptations in Ichthyophis bannanicus

Background Banna caecilian (Ichthyophis bannanicus) is the only species of Gymnophiona in China, with unique lifestyles and characteristics. Although there have been some studies on distribution and morphological characteristics in I. bannanicus, little research focused on the molecular level. A comprehensive analysis of gene expression profiling across tissues can provide necessary information for an in-depth understanding of their biological functions. Result To provide new insights into molecular mechanisms of ecological adaptation in I. bannanicus, we performed gene expression analysis across 10 tissues including skin, blood, spleen, liver, kidney, lung, heart, stomach, testis and ovary. By integrating 27 newly generated RNA-seq datasets with 21 publicly available transcriptomes, we performed a systematic gene expression analysis across tissues representing 19 major organ systems, thereby generating a comprehensive and high-resolution transcriptomic atlas for I. bannanicus. We identified 5,092 housekeeping genes (HKGs) and 2,169 tissue-specific genes (TSGs), and conducted weighted gene co-expression network analysis to determine the modules most relevant to each tissue. Functional enrichment indicated that HKGs support basic cellular activities, while TSGs and the module genes are associated with tissue differentiation and specific physiological processes. Our comparative genomic analysis of I. bannanicus and Xenopus tropicalis revealed genes potentially lost in I. bannanicus, including RCVRN.1, GNAT2, SAG, GRK7, SMURF1, NOG, and MAPK14, which may be associated with degeneration of its visual system and limb structures. Notably, cross-species comparison of HKGs, TSGs, and co-expression modules highlighted an enhanced and unique immune capacity in I. bannanicus. Conclusion Our findings demonstrate that HKGs, TSGs, and co-expression module genes offer valuable perspectives on tissue specialization and evolutionary divergence. The comparative transcriptomic analysis across multiple species and diverse tissue types provides valuable clues into the molecular features that may contribute to ecological adaptation in I. bannanicus. Overall design: We conducted transcriptomic analysis on ten tissues (liver, kidney, lung, blood, heart, ovary, skin, spleen, stomach, and testis) of Ichthyophis bannanicus.

背景 版纳鱼螈（Ichthyophis bannanicus）是中国境内唯一的无足目（Gymnophiona）物种，具有独特的生活方式与生物学特征。尽管目前已有针对版纳鱼螈分布与形态特征的相关研究，但针对其分子层面的探究仍较为匮乏。结果 为深入解析版纳鱼螈生态适应的分子机制，本研究对其10种组织（皮肤、血液、脾脏、肝脏、肾脏、肺脏、心脏、胃脏、睾丸与卵巢）开展基因表达谱分析。本研究整合27条新生成的RNA测序（RNA-seq）数据集与21条公开转录组数据，对覆盖19个主要器官系统的组织开展系统性基因表达分析，进而构建了版纳鱼螈的全面且高分辨率转录组图谱。本研究共鉴定出5092个持家基因（housekeeping genes, HKGs）与2169个组织特异性基因（tissue-specific genes, TSGs），并通过加权基因共表达网络分析，确定了与各组织最相关的基因模块。功能富集分析结果显示，持家基因参与维持细胞基础生命活动，而组织特异性基因及共表达模块基因则与组织分化及特定生理过程密切相关。本研究对版纳鱼螈与热带爪蟾（Xenopus tropicalis）开展比较基因组分析，鉴定出版纳鱼螈中可能发生丢失的基因，包括RCVRN.1、GNAT2、SAG、GRK7、SMURF1、NOG及MAPK14，这些基因的丢失或与其视觉系统与肢体结构的退化相关。值得注意的是，跨物种比较持家基因、组织特异性基因及共表达模块后发现，版纳鱼螈具有增强且独特的免疫能力。结论 本研究结果表明，持家基因、组织特异性基因及共表达模块基因可为解析组织特化与演化分化提供重要视角。跨物种、多组织类型的比较转录组分析，可为揭示版纳鱼螈生态适应相关的分子特征提供关键线索。总体实验设计：本研究对版纳鱼螈的10种组织（肝脏、肾脏、肺脏、血液、心脏、卵巢、皮肤、脾脏、胃脏与睾丸）开展转录组分析。