Strong selective effects of mitochondrial DNA on the nuclear genome

Strong selective effects of mitochondrial DNA on the nuclear genome
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DOI:
10.1073/pnas.1910141117
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发表时间:
2020-03-24
影响因子:
11.1
通讯作者:
Burton, Ronald S.
Burton, Ronald S.
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Healy, Timothy M.;Burton, Ronald S.

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氧化磷酸化是真核生物细胞能量的主要来源,需要在核和线粒体基因组中编码的基因产物。因此,基因组之间的功能整合对于三磷酸腺苷(ATP)的高效生成至关重要。尽管在种群内,这种整合可能是通过共同进化来维持的,但有丝核共同进化在物种形成和线粒体疾病等关键生物过程中的重要性一直受到质疑。在这项研究中,我们交叉了潮间带桡足动物加利福尼亚虎足的种群,以破坏互惠F-2杂交种中假定的共同进化的有核基因型。我们利用这些杂交种之间发育率的个体间差异作为适应度的代表来评估线粒体基因型对核基因组的选择强度。不同杂交个体的发育速率不同,高适合度杂交个体分离的线粒体体外ATP合成速率大约是低适合度个体分离的线粒体的两倍。然后,我们使用Pool-seq来比较高或低适合度杂交的核等位基因频率。在高适应度个体中,12条染色体中有5条染色体存在母体等位基因的显著偏倚,而在低适应度个体中,母体等位基因的偏倚基本不存在。因此,最适合的杂种是那些在这些染色体上具有与其线粒体基因型匹配的核等位基因的杂种,这表明有丝核效应是个体水平发育率差异的基础,基因组间相容性对高适合度至关重要。我们得出结论,有丝核相互作用可以对生理性能和核基因组的进化轨迹产生深远的影响。
Oxidative phosphorylation, the primary source of cellular energy in eukaryotes, requires gene products encoded in both the nuclear and mitochondrial genomes. As a result, functional integration between the genomes is essential for efficient adenosine triphosphate (ATP) generation. Although within populations this integration is presumably maintained by coevolution, the importance of mitonuclear coevolution in key biological processes such as speciation and mitochondrial disease has been questioned. In this study, we crossed populations of the intertidal copepod Tigriopus californicus to disrupt putatively coevolved mitonuclear genotypes in reciprocal F-2 hybrids. We utilized interindividual variation in developmental rate among these hybrids as a proxy for fitness to assess the strength of selection imposed on the nuclear genome by alternate mitochondrial genotypes. Developmental rate varied among hybrid individuals, and in vitro ATP synthesis rates of mitochondria isolated from high-fitness hybrids were approximately two-fold greater than those of mitochondria isolated from low-fitness individuals. We then used Pool-seq to compare nuclear allele frequencies for high- or low-fitness hybrids. Significant biases for maternal alleles were detected on 5 (of 12) chromosomes in high-fitness individuals of both reciprocal crosses, whereas maternal biases were largely absent in low-fitness individuals. Therefore, the most fit hybrids were those with nuclear alleles that matched their mitochondrial genotype on these chromosomes, suggesting that mitonuclear effects underlie individual-level variation in developmental rate and that intergenomic compatibility is critical for high fitness. We conclude that mitonuclear interactions can have profound impacts on both physiological performance and the evolutionary trajectory of the nuclear genome.