Fusome topology and inheritance during insect gametogenesis.

Fusome topology and inheritance during insect gametogenesis.
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DOI:
10.1371/journal.pcbi.1010875
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发表时间:
2023-02
影响因子:
4.3
通讯作者:
--
中科院分区:
生物学2区
文献类型:
--
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从昆虫到哺乳动物,卵母细胞和精子在由细胞间桥(ICBs)连接的细胞组成的生殖系囊肿中发育。在许多昆虫中,囊肿的形成伴随着丝体的生长,丝体是一种渗透在囊肿中的膜质细胞器。融合体的组成和功能在果蝇中得到了最好的理解:在卵子发生过程中,融合体决定了囊肿的拓扑和大小,并促进了卵母细胞的选择,而在精子发生过程中,融合体同步了囊肿对DNA损伤的反应。尽管它在昆虫配子发生过程中具有独特的性别特异性作用,但阐明雌性的融合体生长和遗传及其在雄性中的结构和连通性仍然具有挑战性。在这里,我们利用三维(3D)共聚焦显微镜和计算图像处理工具的进步来重建两性中融合体的拓扑结构,生长和分布。在女性中,我们的实验结果为融合体组装和遗传提供了理论模型,并表明卵母细胞的选择是通过“偏倚等效”机制进行的。在男性中,我们发现细胞分裂可能偏离在女性中观察到的最大分支模式,导致更大的拓扑变异性。我们的工作巩固了现有的脱节的实验观察,并为物种内和物种间配子体发生的定量研究提供了一种易于推广的计算方法。动物生殖系囊肿的普遍存在和显微镜技术的快速发展要求对其发育动力学进行定量和高度解决的研究。在这里,我们使用黑腹果蝇配子发生作为模型系统,并使用监督学习算法来研究精子和卵母细胞发育过程中出现的共享细胞器-融合体。丝体是一种高度特化的膜质细胞器,在两性中渗透于囊肿。我们的三维(3D)重建和在卵发生过程中囊发育的连续阶段的定量测量揭示了雌性种系囊肿内细胞命运不对称的进化,其中囊肿产生单个卵母细胞。在男性中,当囊肿的每个细胞继续形成精子时,fusome片段和表现出的拓扑结构与女性中发现的典型的最大分支拓扑结构不同。我们的发现可以在两性配子体发生的不同结果的背景下进行解释,并突出了定量测量在评估生物科学假设中的中心地位。
From insects to mammals, oocytes and sperm develop within germline cysts comprising cells connected by intercellular bridges (ICBs). In numerous insects, formation of the cyst is accompanied by growth of the fusome—a membranous organelle that permeates the cyst. Fusome composition and function are best understood in Drosophila melanogaster: during oogenesis, the fusome dictates cyst topology and size and facilitates oocyte selection, while during spermatogenesis, the fusome synchronizes the cyst’s response to DNA damage. Despite its distinct and sex-specific roles during insect gametogenesis, elucidating fusome growth and inheritance in females and its structure and connectivity in males has remained challenging. Here, we take advantage of advances in three-dimensional (3D) confocal microscopy and computational image processing tools to reconstruct the topology, growth, and distribution of the fusome in both sexes. In females, our experimental findings inform a theoretical model for fusome assembly and inheritance and suggest that oocyte selection proceeds through an ‘equivalency with a bias’ mechanism. In males, we find that cell divisions can deviate from the maximally branched pattern observed in females, leading to greater topological variability. Our work consolidates existing disjointed experimental observations and contributes a readily generalizable computational approach for quantitative studies of gametogenesis within and across species. The ubiquity of germline cysts across animals and accelerating advances in microscopy call for quantitative and highly resolved studies of their developmental dynamics. Here we use Drosophila melanogaster gametogenesis as a model system, alongside a supervised learning algorithm to study a shared organelle that arises during sperm and oocyte development—the fusome. The fusome is a highly specialized membranous organelle that permeates the cyst in both sexes. Our three-dimensional (3D) reconstructions of the fusome and quantitative measurements at successive stages of cyst development during oogenesis shed light on the evolution of cell fate asymmetry within the germline cyst in females, where the cyst gives rise to a single oocyte. In males, where each cell of the cyst goes on to form sperm, the fusome fragments and exhibits topologies that deviate from the stereotypic maximally branched topology found in females. Our findings can be interpreted in the context of the divergent outcomes of gametogenesis in both sexes and highlight the centrality of quantitative measurements in evaluating hypotheses in biological sciences.
DOI: 10.1038/s41567-021-01383-0
发表时间: 2021-12
期刊: Nature physics
影响因子: 19.6
作者:
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在表现出同步分化的细胞组中,细胞间桥的发生。
DOI: 10.1083/jcb.5.3.453
发表时间: 1959-05-25
期刊: The Journal of biophysical and biochemical cytology
影响因子: --
作者:
FAWCETT, D W;ITO, S;SLAUTTERBACK, D
通讯作者: SLAUTTERBACK, D
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影响因子: 4
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