Genome-wide signatures of plastid-nuclear coevolution point to repeated perturbations of plastid proteostasis systems across angiosperms

Genome-wide signatures of plastid-nuclear coevolution point to repeated perturbations of plastid proteostasis systems across angiosperms
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DOI:
10.1093/plcell/koab021
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发表时间:
2021-01-28
期刊:
影响因子:
11.6
通讯作者:
Sloan, Daniel B.
Sloan, Daniel B.
中科院分区:
生物学1区
文献类型:
--
作者:
Forsythe, Evan S.;Williams, Alissa M.;Sloan, Daniel B.

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核和质体(叶绿体)基因组经历不同的突变率,选择水平和传输模式,但关键的细胞功能取决于它们的协调相互作用。功能相关的蛋白质通常显示出跨同源性序列进化速率的相关变化[进化速率共变(ERC)],提供了一种检测先前未识别的共进化和共功能基因的方法。我们在被子植物多样性中进行了ERC基因组分析,扫描了核基因组中显示ERC与质体基因的基因。正如预期的那样,最强的命中高度富集了编码质体靶向蛋白的基因,这提供了细胞核相互作用影响全基因组规模分子进化速率的证据。许多已鉴定的核基因在转录后调节和蛋白质稳态(蛋白质稳态)的维持中起作用,包括蛋白质翻译(在质体和胞质溶胶中)、输入、质量控制和周转。我们还确定了与质体基因组表现出强烈的共同进化特征的核基因,但它们编码的蛋白质缺乏细胞器靶向注释,使它们成为质体中先前未描述的角色的候选者。总之,我们的全基因组分析表明,质体核协同进化超出了叶绿体酶复合物内的亲密分子相互作用,可能是由负责维持被子植物质体蛋白质稳态的机制频繁重新布线驱动的。
Nuclear and plastid (chloroplast) genomes experience different mutation rates, levels of selection, and transmission modes, yet key cellular functions depend on their coordinated interactions. Functionally related proteins often show correlated changes in rates of sequence evolution across a phylogeny [evolutionary rate covariation (ERC)], offering a means to detect previously unidentified suites of coevolving and cofunctional genes. We performed phylogenomic analyses across angiosperm diversity, scanning the nuclear genome for genes that exhibit ERC with plastid genes. As expected, the strongest hits were highly enriched for genes encoding plastid-targeted proteins, providing evidence that cytonuclear interactions affect rates of molecular evolution at genome-wide scales. Many identified nuclear genes functioned in post-transcriptional regulation and the maintenance of protein homeostasis (proteostasis), including protein translation (in both the plastid and cytosol), import, quality control, and turnover. We also identified nuclear genes that exhibit strong signatures of coevolution with the plastid genome, but their encoded proteins lack organellar-targeting annotations, making them candidates for having previously undescribed roles in plastids. In sum, our genome-wide analyses reveal that plastid-nuclear coevolution extends beyond the intimate molecular interactions within chloroplast enzyme complexes and may be driven by frequent rewiring of the machinery responsible for maintenance of plastid proteostasis in angiosperms.