<i>Arabidopsis</i>ATG8-INTERACTING PROTEIN1 Is Involved in Autophagy-Dependent Vesicular Trafficking of Plastid Proteins to the Vacuole

Michaeli, Simon; Honig, Arik; Levanony, Hanna; Peled-Zehavi, Hadas; Galili, Gad

doi:10.1105/tpc.114.129999

Cited by 186 publications

(194 citation statements)

References 61 publications

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“…The autophagosome formation process is conserved, and ATG8 has been used as an autophagosomal marker in Arabidopsis (10)(11)(12)(13)(14). In Significance One fundamental question in the autophagy field is the membrane origin of the autophagosome.…”

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.

221

162

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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.

221

162

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“…The abundance of the thylakoid proteins D1/PsbA and PHOTOSYSTEM I SUBUNIT F (PSAF) relative to cytoplasmic and nuclear proteins used as internal controls was unchanged (Figures 2I and 2K; Supplemental Table 1). This distinction might reflect the fact that the several pathways participate in the degradation of plastid proteins (Ling et al, 2012;Lee et al, 2013;Michaeli et al, 2014). Whereas stromal components are thought to be degraded in the vacuole and envelope proteins by the proteasome (Ling et al, 2012;Jarvis and López-Juez, 2013) and the vacuole (Michaeli et al, 2014), D1/PSBA is removed internally by stroma-localized proteases (Haussühl et al, 2001).…”

Section: The Chmp1 Mutant Accumulates Stromal and Plastid Envelope Prmentioning

confidence: 99%

“…Recently, a novel autophagic structure devoid of Rubisco and decorated with ATG8-Interacting Protein 1 (AT1-PS bodies) has been postulated to mediate the vacuolar degradation of some stroma, envelope, and thylakoid proteins (Michaeli et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

The Endosomal Protein CHARGED MULTIVESICULAR BODY PROTEIN1 Regulates the Autophagic Turnover of Plastids in Arabidopsis

et al. 2015

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Endosomal Sorting Complex Required for Transport (ESCRT)-III proteins mediate membrane remodeling and the release of endosomal intraluminal vesicles into multivesicular bodies. Here, we show that the ESCRT-III subunit paralogs CHARGED MULTIVESICULAR BODY PROTEIN1 (CHMP1A) and CHMP1B are required for autophagic degradation of plastid proteins in Arabidopsis thaliana. Similar to autophagy mutants, chmp1a chmp1b (chmp1) plants hyperaccumulated plastid components, including proteins involved in plastid division. The autophagy machinery directed the release of bodies containing plastid material into the cytoplasm, whereas CHMP1A and B were required for delivery of these bodies to the vacuole. Autophagy was upregulated in chmp1 as indicated by an increase in vacuolar green fluorescent protein (GFP) cleavage from the autophagic reporter GFP-ATG8. However, autophagic degradation of the stromal cargo RECA-GFP was drastically reduced in the chmp1 plants upon starvation, suggesting that CHMP1 mediates the efficient delivery of autophagic plastid cargo to the vacuole. Consistent with the compromised degradation of plastid proteins, chmp1 plastids show severe morphological defects and aberrant division. We propose that CHMP1 plays a direct role in the autophagic turnover of plastid constituents.

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“…22,23 However, recent evidence indicates a specific function for ATG8 isoforms. 19,24 Human GABARAP sequence is more similar to GABARAPL2 than LC3. Overexpression of LC3 fails to rescue the autophagy defect in GABARAP or GABARAPL2 knockdown cells, and vice versa.…”

Section: Introductionmentioning

confidence: 99%

Comparative analyses of ubiquitin-like ATG8 and cysteine protease ATG4 autophagy genes in the plant lineage and cross-kingdom processing of ATG8 by ATG4

et al. 2016

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Autophagy is important for degradation and recycling of intracellular components. In a diversity of genera and species, orthologs and paralogs of the yeast Atg4 and Atg8 proteins are crucial in the biogenesis of double-membrane autophagosomes that carry the cellular cargoes to vacuoles and lysosomes. Although many plant genome sequences are available, the ATG4 and ATG8 sequence analysis is limited to some model plants. We identified 28 ATG4 and 116 ATG8 genes from the available 18 different plant genome sequences. Gene structures and protein domain sequences of ATG4 and ATG8 are conserved in plant lineages. Phylogenetic analyses classified ATG8s into 3 subgroups suggesting divergence from the common ancestor. The ATG8 expansion in plants might be attributed to whole genome duplication, segmental and dispersed duplication, and purifying selection. Our results revealed that the yeast Atg4 processes Arabidopsis ATG8 but not human LC3A (HsLC3A). In contrast, HsATG4B can process yeast and plant ATG8s in vitro but yeast and plant ATG4s cannot process HsLC3A. Interestingly, in Nicotiana benthamiana plants the yeast Atg8 is processed compared to HsLC3A. However, HsLC3A is processed when coexpressed with HsATG4B in plants. Molecular modeling indicates that lack of processing of HsLC3A by plant and yeast ATG4 is not due to lack of interaction with HsLC3A. Our in-depth analyses of ATG4 and ATG8 in the plant lineage combined with results of cross-kingdom ATG8 processing by ATG4 further support the evolutionarily conserved maturation of ATG8. Broad ATG8 processing by HsATG4B and lack of processing of HsLC3A by yeast and plant ATG4s suggest that the cross-kingdom ATG8 processing is determined by ATG8 sequence rather than ATG4.

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ArabidopsisATG8-INTERACTING PROTEIN1 Is Involved in Autophagy-Dependent Vesicular Trafficking of Plastid Proteins to the Vacuole

Cited by 186 publications

References 61 publications

ATG9 regulates autophagosome progression from the endoplasmic reticulum in Arabidopsis

ATG9 regulates autophagosome progression from the endoplasmic reticulum in Arabidopsis

The Endosomal Protein CHARGED MULTIVESICULAR BODY PROTEIN1 Regulates the Autophagic Turnover of Plastids in Arabidopsis

Comparative analyses of ubiquitin-like ATG8 and cysteine protease ATG4 autophagy genes in the plant lineage and cross-kingdom processing of ATG8 by ATG4

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