Moderate embryonic delay of paternal mitochondrial elimination impairs mating and cognition and alters behaviors of adult animals

IF 11.7 1区综合性期刊 Q1 MULTIDISCIPLINARY SCIENCES

Science Advances Pub Date : 2024-10-04 DOI:10.1126/sciadv.adp8351

Hu Zhang, Yunan Zhu, Ding Xue

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Abstract

Rapid elimination of paternal mitochondria following fertilization is a conserved event in most animals, but its physiological significance remains unclear. We find that modest delay of paternal mitochondrial elimination (PME) in Caenorhabditis elegans embryos unexpectedly impairs mating and cognition of adult animals and alters their locomotion behaviors. Delayed PME causes decreased adenosine triphosphate (ATP) levels in early embryos, which lead to impaired physiological functions of adult animals through an energy-sensing pathway mediated by an adenosine monophosphate (AMP)–activated protein kinase, AAK-2, and a forkhead box class O (FOXO) transcription factor, DAF-16. Treatment of PME-delayed animals with MK-4, a subtype of vitamin K 2 that can improve mitochondrial ATP production, restores ATP levels in early embryos, and rescues physiological defects of adult animals. Our results suggest that moderate PME delay during embryo development adversely affects crucial physiological functions in adults, which could be evolutionarily disadvantageous. These observations provide mechanistic explanations for the need to swiftly remove paternal mitochondria early during embryo development.

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胚胎期父系线粒体消除的适度延迟会损害交配和认知能力，并改变成年动物的行为

父系线粒体在受精后迅速消亡是大多数动物的保守现象，但其生理意义仍不清楚。我们发现，秀丽隐杆线虫胚胎中父代线粒体消除（PME）的适度延迟会意外地损害成年动物的交配和认知能力，并改变它们的运动行为。PME延迟会导致早期胚胎中的三磷酸腺苷（ATP）水平下降，进而通过由单磷酸腺苷（AMP）激活的蛋白激酶AAK-2和叉头盒O类（FOXO）转录因子DAF-16介导的能量感应途径损害成年动物的生理功能。MK-4 是维生素 K 2 的一种亚型，能改善线粒体 ATP 的产生，它能恢复早期胚胎的 ATP 水平，并能挽救成年动物的生理缺陷。我们的研究结果表明，胚胎发育过程中适度的 PME 延迟会对成年动物的关键生理功能产生不利影响，这在进化过程中可能是不利的。这些观察结果从机理上解释了在胚胎发育早期迅速移除父系线粒体的必要性。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

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来源期刊

Science Advances 综合性期刊-综合性期刊

CiteScore

21.40

自引率

1.50%

发文量

1937

审稿时长

29 weeks

期刊介绍： Science Advances, an open-access journal by AAAS, publishes impactful research in diverse scientific areas. It aims for fair, fast, and expert peer review, providing freely accessible research to readers. Led by distinguished scientists, the journal supports AAAS's mission by extending Science magazine's capacity to identify and promote significant advances. Evolving digital publishing technologies play a crucial role in advancing AAAS's global mission for science communication and benefitting humankind.