EXPO and Autophagosomes are Distinct Organelles in Plants

Lin, Youshun; Ding, Yu; Wang, Juan; Shen, Jinbo; Kung, Chun; Zhuang, Xiaohong; Cui, Yong; Yin, Zhao; Xia, Yiji; Lin, Hong‐Xuan; Robinson, David G.; Jiang, Liwen

doi:10.1104/pp.15.00953

Cited by 40 publications

(49 citation statements)

References 81 publications

(123 reference statements)

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“…To further examine the effect of ATG9 deficiency on the autophagic flux, we next treated the cells with BTH and concanamycin A (Conc A), a V-ATPase inhibitor, to prevent the degradation of autophagic bodies in the vacuole (10,13,20,21). Because FM4-64 is taken up into the plant cell from the plasma membrane via endocytosis to finally label the tonoplast and may be delivered into the vacuole together with the tonoplast membrane (22)(23)(24), to distinguish whether these abnormal structures reside within the vacuole, we performed an FM4-64 uptake study in both YFP-ATG8e and YFP-ATG8e/atg9-3 seedlings to label the tonoplast before BTH and Conc A treatments. As shown in Fig.…”

Section: Atg9 Malfunction Results In Accumulation Of Abnormal Autophamentioning

confidence: 99%

ATG9 regulates autophagosome progression from the endoplasmic reticulum in Arabidopsis

Zhuang

Chung

Cui

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Autophagy is a conserved pathway for bulk degradation of cytoplasmic material by a double-membrane structure named the autophagosome. The initiation of autophagosome formation requires the recruitment of autophagy-related protein 9 (ATG9) vesicles to the preautophagosomal structure. However, the functional relationship between ATG9 vesicles and the phagophore is controversial in different systems, and the molecular function of ATG9 remains unknown in plants. Here, we demonstrate that ATG9 is essential for endoplasmic reticulum (ER)-derived autophagosome formation in plants. Through a combination of genetic, in vivo imaging and electron tomography approaches, we show that Arabidopsis ATG9 deficiency leads to a drastic accumulation of autophagosome-related tubular structures in direct membrane continuity with the ER upon autophagic induction. Dynamic analyses demonstrate a transient membrane association between ATG9 vesicles and the autophagosomal membrane during autophagy. Furthermore, trafficking of ATG18a is compromised in atg9 mutants during autophagy by forming extended tubules in a phosphatidylinositol 3-phosphatedependent manner. Taken together, this study provides evidence for a pivotal role of ATG9 in regulating autophagosome progression from the ER membrane in Arabidopsis.O ne long-lasting question regarding autophagosome biogenesis is its membrane origin (1). The initiation site for autophagosomes is termed the preautophagosomal structure or phagophore assembly site (PAS). However, the source of the phagophore membrane remains controversial in different systems, and exactly how the phagophore is initiated from its membrane origin is still unclear. The core autophagy-related (ATG) machinery regulates phagophore assembly in a spatiotemporally coordinated manner whereas some of the ATG components will disassociate from the completed autophagosome and some are turned over together with the autophagosome (1-3).As the sole transmembrane protein, autophagy-related protein 9 (ATG9) has long been suggested to provide a lipid/membrane source for autophagosome formation because ATG9-deficient mutants in yeast or mammal fail to form autophagosomes (4, 5). Although ATG9 is conserved in all eukaryotes (6), it seems that ATG9 might perform its function divergently in different systems. In yeast, ATG9 participates in an early step by shuttling from a non-PAS site to the PAS site and supports an assembly model for yeast autophagosome biogenesis (4). In contrast, mammalian ATG9 is not stably incorporated into the isolation membrane or autophagosomes but is instead transiently associated with the omegasome, a phosphatidylinositol 3-phosphate (PI3P)-enriched endoplasmic reticulum (ER) subdomain (5). Cryomicroscopy studies have shown a close association between ATG9 vesicles and the omegasome structure (7), together with the presence of ATG9 on tubulovesicular membranes surrounding autophagosomes (5). A recent finding by livecell imaging indicates that autophagosome formation occurs where ATG9 vesicles coalesce with the ER ...

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Section: Atg9 Malfunction Results In Accumulation Of Abnormal Autophamentioning

confidence: 99%

ATG9 regulates autophagosome progression from the endoplasmic reticulum in Arabidopsis

Zhuang

Chung

Cui

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

213

162

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“…The exocyst-positive organelles, visualized mostly by ectopic expression, were shown to be cytoplasmic double membrane organelles that can fuse with the plasma membrane and secrete their contents to the apoplast in an exosome-like manner. It is not yet known whether other exocyst subunits also are localized to the same organelles and what might be the biological function of this putative compartment (Wang et al, 2010;Lin et al, 2015). In differentiating xylem cells, two coiled-coil proteins termed VESICLE TETHERING1 and VESICLE TETHERING2 recruit EXO70A1-positive puncta to microtubules via the GOLGI COMPLEX2 protein (Oda et al, 2015).…”

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confidence: 99%

Exocyst SEC3 and phosphoinositides define sites of exocytosis in pollen tube initiation and growth

et al. 2016

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“…Conserved autophagosome-related structures, including the phagophore and the completed double-membrane autophagosome, have been characterized at the ultrastructural level in plants (Isono et al, 2010; Zhuang et al, 2013; Le Bars et al, 2014; Gao et al, 2015; Lin et al, 2015; Spitzer et al, 2015). However, the underlying mechanism(s) of autophagosome biogenesis in plants remain largely unexplored.…”

Section: Introductionmentioning

confidence: 99%

Origin of the Autophagosomal Membrane in Plants

2016

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During autophagy, cargo molecules destined for degradation are sequestrated into a double-membrane structure called autophagosome, which subsequently fuses with the vacuole. An isolation membrane structure (also called the phagophore) initiates from the platform termed PAS (phagophore assembly site or preautophagosomal structure), which then elongates and expands to become the completed autophagosome. The origin of the membrane for autophagosome formation has been extensively investigated but remains an enigma in the field of autophagy. In yeast and mammalian cells multiple membrane sources have been suggested to contribute to autophagosome formation at different steps, from initiation through expansion and maturation. Recent studies in plants have provided a significant advance in our understanding of the conserved role of autophagy and the underlying mechanism for autophagosome formation. Here, we will discuss and evaluate these new findings on autophagosome formation in plants, with a particular focus on the origin of plant autophagosomal membranes.

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EXPO and Autophagosomes are Distinct Organelles in Plants

Cited by 40 publications

References 81 publications

ATG9 regulates autophagosome progression from the endoplasmic reticulum in Arabidopsis

ATG9 regulates autophagosome progression from the endoplasmic reticulum in Arabidopsis

Exocyst SEC3 and phosphoinositides define sites of exocytosis in pollen tube initiation and growth

Origin of the Autophagosomal Membrane in Plants

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