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自噬总是意味着死亡吗?韧皮部形成过程中高度选择性细胞质降解的案例研究。

Is autophagy always a death sentence? A case study of highly selective cytoplasmic degradation during phloemogenesis.

作者信息

Michalak Kornel M, Wojciechowska Natalia, Kułak Karolina, Minicka Julia, Jagodziński Andrzej M, Bagniewska-Zadworna Agnieszka

机构信息

Department of General Botany, Institute of Experimental Biology, Faculty of Biology, Adam Mickiewicz University in Poznań, Uniwersytetu Poznańskiego 6, Poznań 61-614, Poland.

Department of Virology and Bacteriology, Institute of Plant Protection in Poznań, Węgorka 20, Poznań 60-318, Poland.

出版信息

Ann Bot. 2025 Mar 13;135(4):681-696. doi: 10.1093/aob/mcae195.

DOI:10.1093/aob/mcae195
PMID:39497527
原文链接:https://pmc.ncbi.nlm.nih.gov/articles/PMC11904893/
Abstract

BACKGROUND AND AIMS

The transformation of sieve elements from meristematic cells, equipped with a full complement of organelles, to specialized transport tubes devoid of a nucleus has long been enigmatic. We hypothesized a strong involvement of various degradation pathways, particularly macroautophagy in this context, emphasizing the importance of autophagic selectivity in the remaining viability of these cells.

METHODS

Experiments were performed on pioneer roots of Populus trichocarpa cultivated in rhizotrons under field conditions. Through anatomical, ultrastructural and molecular analyses, we delineate the stages of phloemogenesis and the concurrent alterations in the cytoplasmic composition of SEs.

KEY RESULTS

Notably, we observed not only macroautophagic structures, but also the formation of autophagic plastids, the selective degradation of specific organelles, vacuole disruption and the release of vacuolar contents. These events initially lead to localized reductions in cytoplasm density, but the organelle-rich cytoplasmic phase is safeguarded from extensive damage by a membrane system derived from the endoplasmic reticulum. The sieve element ultimately develops into a conduit containing electron-translucent cytoplasm. Eventually, the mature sieve element is a tube filled only by translucent cytoplasm, with sparse organelles tethered to the cell wall.

CONCLUSIONS

Although the activation of programmed cell death pathways was postulated, the persistence of sieve elements indicates that protoplast depletion is meticulously regulated by hitherto unidentified mechanisms. This research elucidates the sequential processes occurring in these cells during phloemogenesis and unveils novel insights into the mechanisms of selective autophagy.

摘要

背景与目的

筛管分子从具有全套细胞器的分生细胞转变为没有细胞核的特殊运输管道,这一过程长期以来一直是个谜。我们推测各种降解途径,特别是在这种情况下的巨自噬,起着重要作用,并强调自噬选择性对这些细胞剩余活力的重要性。

方法

在田间条件下,对种植在根箱中的毛果杨初生根进行实验。通过解剖学、超微结构和分子分析,我们描绘了韧皮部形成的阶段以及筛管分子细胞质组成的同步变化。

主要结果

值得注意的是,我们不仅观察到巨自噬结构,还观察到自噬质体的形成、特定细胞器的选择性降解、液泡破裂以及液泡内容物的释放。这些事件最初导致细胞质密度局部降低,但富含细胞器的细胞质阶段通过源自内质网的膜系统免受广泛损伤。筛管分子最终发育成一个含有电子透明细胞质的管道。最终,成熟的筛管分子是一个仅由透明细胞质填充的管道,稀疏的细胞器附着在细胞壁上。

结论

尽管推测了程序性细胞死亡途径的激活,但筛管分子的持续存在表明原生质体的消耗受到迄今尚未明确的机制的精细调控。这项研究阐明了韧皮部形成过程中这些细胞发生的连续过程,并揭示了选择性自噬机制的新见解。

https://cdn.ncbi.nlm.nih.gov/pmc/blobs/67f4/11904893/7afd6c2277ee/mcae195_fig5.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/67f4/11904893/2dde28c75656/mcae195_fig1.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/67f4/11904893/4fdb8ba77f76/mcae195_fig2.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/67f4/11904893/d93b04d49a47/mcae195_fig3.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/67f4/11904893/20188ccbf815/mcae195_fig4.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/67f4/11904893/7afd6c2277ee/mcae195_fig5.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/67f4/11904893/2dde28c75656/mcae195_fig1.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/67f4/11904893/4fdb8ba77f76/mcae195_fig2.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/67f4/11904893/d93b04d49a47/mcae195_fig3.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/67f4/11904893/20188ccbf815/mcae195_fig4.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/67f4/11904893/7afd6c2277ee/mcae195_fig5.jpg

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本文引用的文献

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NBR1: The archetypal selective autophagy receptor.NBR1:典型的选择性自噬受体。
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Functions of autophagy in chloroplast protein degradation and homeostasis.自噬在叶绿体蛋白质降解和稳态中的作用。
Front Plant Sci. 2022 Sep 29;13:993215. doi: 10.3389/fpls.2022.993215. eCollection 2022.
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Combining Clearing and Fluorescence Microscopy for Visualising Changes in Gene Expression and Physiological Responses to Plasmodiophora brassicae.结合透明化和荧光显微镜观察基因表达变化和对芸薹根肿菌的生理响应。
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Cell. 2022 Mar 17;185(6):1101-1102. doi: 10.1016/j.cell.2022.03.002.
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The Role of Autophagy in Lamellar Body Formation and Surfactant Production in Type 2 Alveolar Epithelial Cells.自噬在 II 型肺泡上皮细胞中板层小体形成和表面活性物质产生中的作用。
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