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串联的质体-内质网动态促进了由亲缘关系驱动的质体-核关系。

Proximity driven plastid-nucleus relationships are facilitated by tandem plastid-ER dynamics.

机构信息

Laboratory of Plant Development & Interactions, Department of Molecular & Cellular Biology, University of Guelph, 50 Stone Road, Guelph, ON N1G2W1, Canada.

出版信息

J Exp Bot. 2024 Oct 30;75(20):6275-6294. doi: 10.1093/jxb/erae313.

DOI:10.1093/jxb/erae313
PMID:39034638
原文链接:https://pmc.ncbi.nlm.nih.gov/articles/PMC11523032/
Abstract

Peri-nuclear clustering (PNC) of chloroplasts has largely been described in senescent and pathogen- or reactive oxygen species-stressed cells. Stromules, tubular plastid extensions, are also observed under similar conditions. Coincident observations of PNC and stromules associate the two phenomena in facilitating retrograde signaling between chloroplasts and the nucleus. However, PNC incidence in non-stressed cells under normal growth and developmental conditions, when stromules are usually not observed, remains unclear. Using transgenic Arabidopsis expressing different organelle-targeted fluorescent proteins, we show that PNC is a dynamic subcellular phenomenon that continues in the absence of light and is not dependent on stromule formation. PNC is facilitated by tandem plastid-endoplasmic reticulum (ER) dynamics created through membrane contact sites between the two organelles. While PNC increases upon ER membrane expansion, some plastids may remain in the peri-nuclear region due to their localization in ER-lined nuclear indentions. Moreover, some PNC plastids may sporadically extend stromules into ER-lined nuclear grooves. Our findings strongly indicate that PNC is not an exclusive response to stress caused by pathogens, high light, or exogenous H2O2 treatment, and does not require stromule formation. However, morphological and behavioral alterations in ER and concomitant changes in tandem, plastid-ER dynamics play a major role in facilitating the phenomenon.

摘要

核周聚簇(PNC)主要在衰老细胞、病原体或活性氧物质应激细胞中被描述。在类似条件下,也观察到了管状质体延伸结构——质体丝状体。PNC 和质体丝状体的同时观察将这两种现象联系起来,有助于叶绿体和细胞核之间的逆行信号转导。然而,在正常生长和发育条件下,非应激细胞中 PNC 的发生率尚不清楚,此时通常观察不到质体丝状体。使用表达不同细胞器靶向荧光蛋白的转基因拟南芥,我们表明 PNC 是一种动态的亚细胞现象,即使在没有光照的情况下也会继续发生,并且不依赖于质体丝状体的形成。PNC 是通过两个细胞器之间的膜接触位点形成的串联质体-内质网(ER)动态来促进的。虽然 PNC 随着 ER 膜的扩展而增加,但由于某些质体定位于 ER 衬里的核凹陷中,它们可能仍留在核周区域。此外,一些 PNC 质体可能会偶尔将质体丝状体延伸到 ER 衬里的核槽中。我们的研究结果强烈表明,PNC 不是对病原体、高光或外源 H2O2 处理引起的应激的特有反应,也不需要质体丝状体的形成。然而,ER 的形态和行为改变以及串联的、质体-ER 动态的变化在促进这一现象中起着重要作用。

https://cdn.ncbi.nlm.nih.gov/pmc/blobs/ac89/11523032/44dbeb4c8e3b/erae313_fig7.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/ac89/11523032/eeded1d6d67d/erae313_fig1.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/ac89/11523032/0301a138c7ff/erae313_fig2.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/ac89/11523032/a1faf05d13cd/erae313_fig3.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/ac89/11523032/c2d9c9b9405a/erae313_fig4.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/ac89/11523032/b5b40a53faeb/erae313_fig5.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/ac89/11523032/0b20cf7372f7/erae313_fig6.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/ac89/11523032/44dbeb4c8e3b/erae313_fig7.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/ac89/11523032/eeded1d6d67d/erae313_fig1.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/ac89/11523032/0301a138c7ff/erae313_fig2.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/ac89/11523032/a1faf05d13cd/erae313_fig3.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/ac89/11523032/c2d9c9b9405a/erae313_fig4.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/ac89/11523032/b5b40a53faeb/erae313_fig5.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/ac89/11523032/0b20cf7372f7/erae313_fig6.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/ac89/11523032/44dbeb4c8e3b/erae313_fig7.jpg

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本文引用的文献

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Talk to your neighbors in an emergency: Stromule-mediated chloroplast-nucleus communication in plant immunity.在紧急情况下与邻居交谈:植物免疫中的 Stromule 介导线粒体-核通讯。
Curr Opin Plant Biol. 2024 Jun;79:102529. doi: 10.1016/j.pbi.2024.102529. Epub 2024 Apr 11.
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Membrane contacts with the endoplasmic reticulum modulate plastid morphology and behaviour.与内质网的膜接触调节质体形态和行为。
Front Plant Sci. 2023 Dec 4;14:1293906. doi: 10.3389/fpls.2023.1293906. eCollection 2023.
3
Calponin homology domain containing kinesin, KIS1, regulates chloroplast stromule formation and immunity.
肌球蛋白轻链激酶 KIS1 通过卷曲螺旋结构域同源蛋白调控叶绿体丝状体的形成和免疫
Sci Adv. 2023 Oct 27;9(43):eadi7407. doi: 10.1126/sciadv.adi7407. Epub 2023 Oct 25.
4
Hydrogen peroxide sensor HyPer7 illuminates tissue-specific plastid redox dynamics.过氧化氢传感器 HyPer7 可照亮组织特异性质体氧化还原动力学。
Plant Physiol. 2023 Aug 31;193(1):217-228. doi: 10.1093/plphys/kiad307.
5
Pepper mild mottle virus coat protein interacts with pepper chloroplast outer envelope membrane protein OMP24 to inhibit antiviral immunity in plants.辣椒轻斑驳病毒外壳蛋白与辣椒叶绿体外膜蛋白OMP24相互作用,以抑制植物的抗病毒免疫。
Hortic Res. 2023 Mar 15;10(5):uhad046. doi: 10.1093/hr/uhad046. eCollection 2023 May.
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A tell tail sign: a conserved C-terminal tail-anchor domain targets a subset of pathogen effectors to the plant endoplasmic reticulum.一个明显的标志:保守的 C 端尾部锚定域将病原体效应物的一个子集靶向植物内质网。
J Exp Bot. 2023 May 19;74(10):3188-3202. doi: 10.1093/jxb/erad075.
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Plant Physiol. 2023 Jan 2;191(1):161-176. doi: 10.1093/plphys/kiac481.
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J Exp Bot. 2022 Nov 19;73(21):7105-7125. doi: 10.1093/jxb/erac344.
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J Exp Bot. 2022 Nov 19;73(21):7155-7164. doi: 10.1093/jxb/erac334.
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J Microsc. 2023 Jul;291(1):105-118. doi: 10.1111/jmi.13139. Epub 2022 Aug 30.