Gene loss and compensatory evolution promotes the emergence of morphological novelties in budding yeast

Gene loss and compensatory evolution promotes the emergence of morphological novelties in budding yeast
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DOI:
10.1038/s41559-022-01730-1
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发表时间:
2022-04-28
影响因子:
16.8
通讯作者:
Papp, Balazs
Papp, Balazs
中科院分区:
生物学1区
文献类型:
--
作者:
Farkas, Zoltan;Kovacs, Karoly;Papp, Balazs

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补偿突变在表型进化中的作用尚不清楚。在这里,作者使用实验进化来表明,基因丢失后的补偿性进化有助于出芽酵母中新细胞和多细胞形态的快速出现。有害突变通常被认为与形态进化无关。然而,它们可以通过有条件的有益突变来补偿,从而提供新的适应性路径。在这里,我们使用实验室进化的芽殖酵母谱系的高维表型来证明新的细胞形态作为基因丢失和随后的补偿进化的副产品异常迅速地出现。出乎意料的是,侵入性生长、多细胞聚集和生物膜形成的能力也会因基因丢失而自发进化。这些多细胞表型可以通过不同的突变途径来实现,并且无需重新激活规范的调控途径。这些生态和临床相关特征源于补偿进化的多效性副作用,在实验室环境中没有明显的效用。进化谱系的形态多样性程度与具有不同遗传背景和生活方式的天然酵母分离物相当。最后,我们表明,最初的基因丢失和随后的补偿性突变都有助于新的形态,它们的协同效应是特定形态变化的基础。我们得出的结论是,补偿进化是形态多样性和表型新颖性的一个先前未被认识的来源。
The role of compensatory mutations in phenotypic evolution is unclear. Here the authors use experimental evolution to show that gene loss followed by compensatory evolution contributes to the rapid emergence of new cellular and multicellular morphologies in the budding yeast.Deleterious mutations are generally considered to be irrelevant for morphological evolution. However, they could be compensated by conditionally beneficial mutations, thereby providing access to new adaptive paths. Here we use high-dimensional phenotyping of laboratory-evolved budding yeast lineages to demonstrate that new cellular morphologies emerge exceptionally rapidly as a by-product of gene loss and subsequent compensatory evolution. Unexpectedly, the capacities for invasive growth, multicellular aggregation and biofilm formation also spontaneously evolve in response to gene loss. These multicellular phenotypes can be achieved by diverse mutational routes and without reactivating the canonical regulatory pathways. These ecologically and clinically relevant traits originate as pleiotropic side effects of compensatory evolution and have no obvious utility in the laboratory environment. The extent of morphological diversity in the evolved lineages is comparable to that of natural yeast isolates with diverse genetic backgrounds and lifestyles. Finally, we show that both the initial gene loss and subsequent compensatory mutations contribute to new morphologies, with their synergistic effects underlying specific morphological changes. We conclude that compensatory evolution is a previously unrecognized source of morphological diversity and phenotypic novelties.