Asymmetric genome merging leads to gene expression novelty through nucleo-cytoplasmic disruptions and transcriptomic shock in Chlamydomonas triploids.

IF 9.4 1区 生物学 Q1 Agricultural and Biological Sciences
New Phytologist Pub Date : 2024-11-05 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
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Abstract

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.

不对称基因组合并通过衣藻三倍体中的核-细胞质破坏和转录组冲击导致基因表达的新颖性。
基因组合并是一种常见现象,会对表型、适应性和基因表达产生广泛影响,但人们对其更广泛的影响还不甚了解。基因组合并对基因表达的两种后果仍然知之甚少:剂量效应和表达进化。我们以莱茵衣藻(Chlamydomonas reinhardtii)为模型,通过将一个二倍体与一个单倍体株系杂交,产生一个新的三倍体株系,来研究不对称基因组合并的影响。在实验室自然选择实验中,由该三倍体品系衍生出的五个独立克隆品系经过了 425 个无性世代的进化。利用适配性测定、流式细胞仪和 RNA-Seq 技术,我们评估了基因组合并和后续进化的直接后果。我们的研究结果表明,基因组大小、基因表达、蛋白质平衡和细胞核比例发生了重大变化。基因表达表现出表达水平的优势和反向性(即表达水平高于或低于亲本)。从单倍体亲本中观察到持续的表达水平优势和 "功能优势 "模式。尽管基因组和核细胞质发生了严重破坏,三倍体株系的适应性仍然得到了提高。通过比较不同世代的基因表达,我们的研究结果表明,恢复蛋白稳态是红衣藻(可能也包括其他系统)基因组合并后快速适应的关键组成部分。
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来源期刊
New Phytologist
New Phytologist PLANT SCIENCES-
CiteScore
17.60
自引率
5.30%
发文量
728
审稿时长
1 months
期刊介绍: New Phytologist is a leading publication that showcases exceptional and groundbreaking research in plant science and its practical applications. With a focus on five distinct sections - Physiology & Development, Environment, Interaction, Evolution, and Transformative Plant Biotechnology - the journal covers a wide array of topics ranging from cellular processes to the impact of global environmental changes. We encourage the use of interdisciplinary approaches, and our content is structured to reflect this. Our journal acknowledges the diverse techniques employed in plant science, including molecular and cell biology, functional genomics, modeling, and system-based approaches, across various subfields.
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