Laboratory of Plant Development & Interactions, Department of Molecular & Cellular Biology, University of Guelph, 50 Stone Road, Guelph, ON N1G2W1, Canada.
J Exp Bot. 2024 Oct 30;75(20):6275-6294. doi: 10.1093/jxb/erae313.
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.
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。