Tissue folding at the organ-meristem boundary results in nuclear compression and chromatin compaction.

Tissue folding at the organ-meristem boundary results in nuclear compression and chromatin compaction.
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DOI:
10.1073/pnas.2017859118
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发表时间:
2021-02-23
影响因子:
11.1
通讯作者:
Hamant O
Hamant O
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Fal K;Korsbo N;Alonso-Serra J;Teles J;Liu M;Refahi Y;Chabouté ME;Jönsson H;Hamant O

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在发育过程中,生长使组织和器官变形。这在植物中的新花形成期间尤其如此,因为组织在幼花芽出现期间折叠。在这里,我们提供了进一步的证据,器官发生压缩细胞的边界,分离器官从干细胞龛,我们表明,这导致细胞核压缩和染色质的变化。虽然众所周知机械力会影响培养中哺乳动物细胞的核形状和染色质,但这表明这种效应也发生在发育中的生物体中,并表明力可能有助于通过大规模染色质效应来定义边界域。人工机械扰动影响培养中动物细胞的染色质。这是否也与活生物体中的组织生长有关仍然存在争议。在植物中,气生器官的出现是通过茎顶端分生组织周围的局部生长而发生的,茎顶端分生组织也包含干细胞生态位。有趣的是,已经提出器官生长在鞍形器官分生组织边界域中产生压缩。然而,这种生长诱导的机械应力是否会影响植物组织中的染色质还不清楚。在这里,通过成像的核包膜在体内随着时间的推移和量化核变形,我们证明了在该域中的活性核压缩的存在。我们开发了一种定量管道,可用于识别边界深处的非常变形的细胞核的子集,并且随着细胞横向收缩,细胞核逐渐变窄和变长。在这一领域,我们发现,染色质染色和标记所示的染色中心的数量减少,并诱导连接组蛋白H1.3的表达。作为力对染色质变化的作用的进一步证据,用MicroVice人工压缩可以诱导H1.3在分生组织的其余部分中的异位表达。此外,虽然染色质的甲基化状态与分生组织边界处的核变形相关,但这种相关性在h1.3突变体中丢失。总而言之,我们揭示了植物器官发生产生的压缩能够对单个细胞中的染色质产生全局影响。
During development, growth deforms tissues and organs. This is notably the case during the formation of new flowers in plants, as the tissue folds during young floral bud emergence. Here, we provide further evidence that organogenesis compresses the cells at the boundary, separating the organ from the stem cell niche, and we show that this leads to nucleus compression and chromatin changes. While mechanical forces are well known to affect nucleus shape and chromatin in mammalian cells in culture, this demonstrates that such an effect also occurs in a developing organism and suggests that forces may help to define boundary domains through large-scale chromatin effects. Artificial mechanical perturbations affect chromatin in animal cells in culture. Whether this is also relevant to growing tissues in living organisms remains debated. In plants, aerial organ emergence occurs through localized outgrowth at the periphery of the shoot apical meristem, which also contains a stem cell niche. Interestingly, organ outgrowth has been proposed to generate compression in the saddle-shaped organ–meristem boundary domain. Yet whether such growth-induced mechanical stress affects chromatin in plant tissues is unknown. Here, by imaging the nuclear envelope in vivo over time and quantifying nucleus deformation, we demonstrate the presence of active nuclear compression in that domain. We developed a quantitative pipeline amenable to identifying a subset of very deformed nuclei deep in the boundary and in which nuclei become gradually narrower and more elongated as the cell contracts transversely. In this domain, we find that the number of chromocenters is reduced, as shown by chromatin staining and labeling, and that the expression of linker histone H1.3 is induced. As further evidence of the role of forces on chromatin changes, artificial compression with a MicroVice could induce the ectopic expression of H1.3 in the rest of the meristem. Furthermore, while the methylation status of chromatin was correlated with nucleus deformation at the meristem boundary, such correlation was lost in the h1.3 mutant. Altogether, we reveal that organogenesis in plants generates compression that is able to have global effects on chromatin in individual cells.
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期刊: SCIENCE
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