Gamete formation and subsequent offspring development often involve extended phases of suspended cellular development or even dormancy. How cells adapt to recover and resume growth remains poorly understood. Here, we visualized budding yeast cells undergoing meiosis by cryo-electron tomography (cryoET) and discovered elaborate filamentous assemblies decorating the nucleus, cytoplasm, and mitochondria. To determine filament composition, we developed a “filament identification” (FilamentID) workflow that combines multiscale cryoET/cryo-electron microscopy (cryoEM) analyses of partially lysed cells or organelles. FilamentID identified the mitochondrial filaments as being composed of the conserved aldehyde dehydrogenase Ald4^ALDH2 and the nucleoplasmic/cytoplasmic filaments as consisting of acetyl-coenzyme A (CoA) synthetase Acs1^ACSS2. Structural characterization further revealed the mechanism underlying polymerization and enabled us to genetically perturb filament formation. Acs1 polymerization facilitates the recovery of chronologically aged spores and, more generally, the cell cycle re-entry of starved cells. FilamentID is broadly applicable to characterize filaments of unknown identity in diverse cellular contexts.

配子形成和随后的后代发育通常涉及细胞发育暂停甚至休眠的延长阶段。细胞如何适应恢复和恢复生长仍知之甚少。在这里，我们通过冷冻电子断层扫描（cryoET）观察了正在经历减数分裂的出芽酵母细胞，并发现了装饰细胞核、细胞质和线粒体的精致丝状组件。为了确定细丝成分，我们开发了一种“细丝识别”(FilamentID) 工作流程，该工作流程结合了对部分裂解的细胞或细胞器的多尺度冷冻电子显微镜 (cryoET)/冷冻电子显微镜 (cryoEM) 分析。 FilamentID 鉴定线粒体丝由保守的乙醛脱氢酶 Ald4 ^ALDH2 组成，核质/细胞质丝由乙酰辅酶 A (CoA) 合成酶 Acs1 ^ACSS2 组成。结构表征进一步揭示了聚合的机制，并使我们能够从基因上干扰丝的形成。 Acs1 聚合促进了按时间顺序老化的孢子的恢复，更普遍的是，促进了饥饿细胞的细胞周期重新进入。 FilamentID 广泛适用于表征不同细胞环境中未知身份的细丝。