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Asymmetric genome merging leads to gene expression novelty through nucleo‐cytoplasmic disruptions and transcriptomic shock in Chlamydomonas triploids
New Phytologist ( IF 8.3 ) Pub Date : 2024-11-06 , DOI: 10.1111/nph.20249 Lucas Prost‐Boxoen, Quinten Bafort, Antoine Van de Vloet, Fabricio Almeida‐Silva, Yunn Thet Paing, Griet Casteleyn, Sofie D'hondt, Olivier De Clerck, Yves Van de Peer
New Phytologist ( IF 8.3 ) Pub Date : 2024-11-06 , DOI: 10.1111/nph.20249 Lucas Prost‐Boxoen, Quinten Bafort, Antoine Van de Vloet, Fabricio Almeida‐Silva, Yunn Thet Paing, Griet Casteleyn, Sofie D'hondt, Olivier De Clerck, Yves Van de Peer
Summary Genome merging is a common phenomenon causing a wide range of consequences on phenotype, adaptation, and gene expression, yet its broader implications are not well‐understood. Two consequences of genome merging on gene expression remain particularly poorly understood: dosage effects and evolution of expression. We employed Chlamydomonas reinhardtii as a model to investigate the effects of asymmetric genome merging by crossing a diploid with a haploid strain to create a novel triploid line. Five independent clonal lineages derived from this triploid line were evolved for 425 asexual generations in a laboratory natural selection experiment. Utilizing fitness assays, flow cytometry, and RNA‐Seq, we assessed the immediate consequences of genome merging and subsequent evolution. Our findings reveal substantial alterations in genome size, gene expression, protein homeostasis, and cytonuclear stoichiometry. Gene expression exhibited expression‐level dominance and transgressivity (i.e. expression level higher or lower than either parent). Ongoing expression‐level dominance and a pattern of ‘functional dominance’ from the haploid parent was observed. Despite major genomic and nucleo‐cytoplasmic disruptions, enhanced fitness was detected in the triploid strain. By comparing gene expression across generations, our results indicate that proteostasis restoration is a critical component of rapid adaptation following genome merging in Chlamydomonas reinhardtii and possibly other systems.
中文翻译:
不对称基因组合并通过三倍体衣藻的核-细胞质破坏和转录组休克导致基因表达新颖性
总结 基因组融合是一种常见现象,对表型、适应性和基因表达造成广泛的影响,但其更广泛的影响尚不清楚。基因组合并对基因表达的两个后果仍然知之甚少:剂量效应和表达进化。我们以莱茵衣藻为模型,通过将二倍体与单倍体菌株杂交来创建新的三倍体系,研究不对称基因组合并的影响。在实验室自然选择实验中,源自该三倍体系的 5 个独立克隆谱系进化了 425 代无性世代。利用适应性测定、流式细胞术和 RNA-Seq,我们评估了基因组合并和后续进化的直接后果。我们的研究结果揭示了基因组大小、基因表达、蛋白质稳态和细胞核化学计量的显着变化。基因表达表现出表达水平的显性和越界性 (即表达水平高于或低于任何亲本)。观察到持续的表达水平显性和来自单倍体亲本的“功能显性”模式。尽管基因组和核质破坏严重,但在三倍体菌株中检测到增强的适应性。通过比较各代的基因表达,我们的结果表明,在莱茵衣藻和可能的其他系统中,蛋白质稳态恢复是基因组合并后快速适应的关键组成部分。
更新日期:2024-11-06
中文翻译:
不对称基因组合并通过三倍体衣藻的核-细胞质破坏和转录组休克导致基因表达新颖性
总结 基因组融合是一种常见现象,对表型、适应性和基因表达造成广泛的影响,但其更广泛的影响尚不清楚。基因组合并对基因表达的两个后果仍然知之甚少:剂量效应和表达进化。我们以莱茵衣藻为模型,通过将二倍体与单倍体菌株杂交来创建新的三倍体系,研究不对称基因组合并的影响。在实验室自然选择实验中,源自该三倍体系的 5 个独立克隆谱系进化了 425 代无性世代。利用适应性测定、流式细胞术和 RNA-Seq,我们评估了基因组合并和后续进化的直接后果。我们的研究结果揭示了基因组大小、基因表达、蛋白质稳态和细胞核化学计量的显着变化。基因表达表现出表达水平的显性和越界性 (即表达水平高于或低于任何亲本)。观察到持续的表达水平显性和来自单倍体亲本的“功能显性”模式。尽管基因组和核质破坏严重,但在三倍体菌株中检测到增强的适应性。通过比较各代的基因表达,我们的结果表明,在莱茵衣藻和可能的其他系统中,蛋白质稳态恢复是基因组合并后快速适应的关键组成部分。