Jiang Yaohan, Chen Xiao, Wang Chundi, Lyu Liping, Al-Farraj Saleh A, Stover Naomi A, Gao Feng
Key Laboratory of Evolution & Marine Biodiversity (Ministry of Education) and Institute of Evolution & Marine Biodiversity, Ocean University of China, Qingdao, 266003, China.
Marine College, Shandong University, Weihai, 264209, China.
Sci China Life Sci. 2025 Jan;68(1):232-248. doi: 10.1007/s11427-023-2605-9. Epub 2024 Sep 10.
Sexual reproduction first appeared in unicellular protists and has continued to be an essential biological process in almost all eukaryotes. Ciliated protists, which contain both germline and somatic genomes within a single cell, have evolved a special form of sexual reproduction called conjugation that involves mitosis, meiosis, fertilization, nuclear differentiation, genome rearrangement, and the development of unique cellular structures. The molecular basis and mechanisms of conjugation vary dramatically among ciliates, and many details of the process and its regulation are still largely unknown. In order to better comprehend these processes and mechanisms from an evolutionary perspective, this study provides the first comprehensive overview of the transcriptome and proteome profiles during the entire life cycle of the newly-established marine model ciliate Euplotes vannus. Transcriptome analyses from 14 life cycle stages (three vegetative stages and 11 sexual stages) revealed over 26,000 genes that are specifically expressed at different stages, many of which are related to DNA replication, transcription, translation, mitosis, meiosis, nuclear differentiation, and/or genome rearrangement. Quantitative proteomic analyses identified 338 proteins with homologs associated with conjugation and/or somatic nuclear development in other ciliates, including dicer-like proteins, Hsp90 proteins, RNA polymerase II and transcription elongation factors, ribosomal-associated proteins, and ubiquitin-related proteins. Four of these homologs belong to the PIWI family, each with different expression patterns identified and confirmed by RT-qPCR, which may function in small RNA-mediated genome rearrangement. Proteins involved in the nonhomologous end-joining pathway are induced early during meiosis and accumulate in the developing new somatic nucleus, where more than 80% of the germline sequences are eliminated from the somatic genome. A number of new candidate genes and proteins likely to play roles in conjugation and its related genome rearrangements have also been revealed. The gene expression profiles reported here will be valuable resources for further studies of the origin and evolution of sexual reproduction in this new model species.
有性生殖最早出现在单细胞原生生物中,并且一直是几乎所有真核生物中一个重要的生物学过程。纤毛原生生物在单个细胞内同时包含种系基因组和体细胞基因组,它们进化出了一种特殊的有性生殖形式,称为接合生殖,该过程涉及有丝分裂、减数分裂、受精、核分化、基因组重排以及独特细胞结构的发育。接合生殖的分子基础和机制在不同的纤毛虫之间差异极大,该过程及其调控的许多细节在很大程度上仍然未知。为了从进化的角度更好地理解这些过程和机制,本研究首次全面概述了新建立的海洋模式纤毛虫——扇形游仆虫在整个生命周期中的转录组和蛋白质组概况。对14个生命周期阶段(三个营养阶段和11个性阶段)的转录组分析揭示了超过26000个在不同阶段特异性表达的基因,其中许多基因与DNA复制、转录、翻译、有丝分裂、减数分裂、核分化和/或基因组重排有关。定量蛋白质组分析鉴定出338种蛋白质,它们在其他纤毛虫中具有与接合生殖和/或体细胞核发育相关的同源物,包括类Dicer蛋白、Hsp90蛋白、RNA聚合酶II和转录延伸因子、核糖体相关蛋白以及泛素相关蛋白。其中四个同源物属于PIWI家族,通过RT-qPCR鉴定并确认了它们各自不同的表达模式,它们可能在小RNA介导的基因组重排中发挥作用。参与非同源末端连接途径的蛋白质在减数分裂早期被诱导,并在发育中的新体细胞核中积累,在那里超过80%的种系序列从体细胞基因组中被消除。还揭示了一些可能在接合生殖及其相关基因组重排中发挥作用的新候选基因和蛋白质。本文报道的基因表达谱将为进一步研究这种新模型物种中有性生殖的起源和进化提供有价值的资源。