Autophagy in Plants – What's New on the Menu?

Michaeli, Simon; Galili, Gad; Genschik, Pascal; Fernie, Alisdair R.; Avin‐Wittenberg, Tamar

doi:10.1016/j.tplants.2015.10.008

Cited by 214 publications

(172 citation statements)

References 91 publications

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“…Autophagy is a conserved biological process that maintains cellular homeostasis in either a housekeeping capacity or in response to environmental stress (Michaeli et al, 2016). Upon induction, autophagy occurs via phagophore (isolation membrane) initiation, nucleation, expansion, and maturation, leading to the formation of autophagosomes, which subsequently fuse with the vacuole and deliver the engulfed materials for degradation (Yang and Klionsky, 2010;Liu and Bassham, 2012;Li and Vierstra, 2012).…”

Section: Discussionmentioning

confidence: 99%

“…Upon induction, autophagy occurs via phagophore (isolation membrane) initiation, nucleation, expansion, and maturation, leading to the formation of autophagosomes, which subsequently fuse with the vacuole and deliver the engulfed materials for degradation (Yang and Klionsky, 2010;Liu and Bassham, 2012;Li and Vierstra, 2012). To date, several ATGs and their regulatory factors have been shown to function in autophagy in plants (Michaeli et al, 2016). Among these, ATG6 is a key component of the nucleation complex that functions during autophagy by interacting with the phosphatidylinositol-3-kinases PI3K and VPS15.…”

Section: Discussionmentioning

confidence: 99%

“…Macroautophagy (hereafter referred to as autophagy, or "selfeating") is a conserved pathway in all eukaryotic cells that is used to recycle nutrients via double-membrane vesicles termed autophagosomes, which target cytoplasmic contents and organelles to the lysosome or vacuole for degradation by resident hydrolases (He and Klionsky, 2009;Liu and Bassham, 2012;Li and Vierstra, 2012;Zhuang et al, 2015;Michaeli et al, 2016). The outer membrane of the autophagosome fuses with the tonoplast and releases an intravacuolar vesicle (autophagic body) containing the inner membrane of the autophagosome and the engulfed components (Liu and Bassham, 2012;Li and Vierstra, 2012).…”

Section: Introductionmentioning

confidence: 99%

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TRAF Family Proteins Regulate Autophagy Dynamics by Modulating AUTOPHAGY PROTEIN6 Stability in Arabidopsis

et al. 2017

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Eukaryotic cells use autophagy to recycle cellular components. During autophagy, autophagosomes deliver cytoplasmic contents to the vacuole or lysosome for breakdown. Mammalian cells regulate the dynamics of autophagy via ubiquitinmediated proteolysis of autophagy proteins. Here, we show that the Arabidopsis thaliana Tumor necrosis factor ReceptorAssociated Factor (TRAF) family proteins TRAF1a and TRAF1b (previously named MUSE14 and MUSE13, respectively) help regulate autophagy via ubiquitination. Upon starvation, cytoplasmic TRAF1a and TRAF1b translocated to autophagosomes. Knockout traf1a/b lines showed reduced tolerance to nutrient deficiency, increased salicylic acid and reactive oxygen species levels, and constitutive cell death in rosettes, resembling the phenotypes of autophagy-defective mutants. Starvation-activated autophagosome accumulation decreased in traf1a/b root cells, indicating that TRAF1a and TRAF1b function redundantly in regulating autophagosome formation. TRAF1a and TRAF1b interacted in planta with ATG6 and the RING finger E3 ligases SINAT1, SINAT2, and SINAT6 (with a truncated RING-finger domain). SINAT1 and SINAT2 require the presence of TRAF1a and TRAF1b to ubiquitinate and destabilize AUTOPHAGY PROTEIN6 (ATG6) in vivo. Conversely, starvation-induced SINAT6 reduced SINAT1-and SINAT2-mediated ubiquitination and degradation of ATG6. Consistently, SINAT1/SINAT2 and SINAT6 knockout mutants exhibited increased tolerance and sensitivity, respectively, to nutrient starvation. Therefore, TRAF1a and TRAF1b function as molecular adaptors that help regulate autophagy by modulating ATG6 stability in Arabidopsis.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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TRAF Family Proteins Regulate Autophagy Dynamics by Modulating AUTOPHAGY PROTEIN6 Stability in Arabidopsis

et al. 2017

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“…Autophagy functions in the degradation and recycling of macromolecules and cytoplasmic organelles, often in response to stress conditions (Yang and Bassham, 2015). There is also recent evidence for selective autophagy in plants, whereby specific proteins or organelles are recognized by receptor proteins and degraded, although many details remain to be elucidated (Michaeli et al, 2016). A subset of these receptors contain a ubiquitin-binding domain and an ATG8-interacting motif (AIM), allowing them to recruit ubiquitinated cargo to ATG8-labeled autophagosomes (Floyd et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

Selective Autophagy of BES1 Mediated by DSK2 Balances Plant Growth and Survival

et al. 2017

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SUMMARY Plants encounter a variety of stresses and must fine-tune their growth and stress-response programs to best suit their environment. BES1 functions as a master regulator in the brassinosteroid (BR) pathway that promotes plant growth. Here, we show that BES1 interacts with the ubiquitin receptor protein DSK2 and is targeted to the autophagy pathway during stress via the interaction of DSK2 with ATG8, a ubiquitin-like protein directing autophagosome formation and cargo recruitment. Additionally, DSK2 is phosphorylated by the GSK3-like kinase BIN2, a negative regulator in the BR pathway. BIN2 phosphorylation of DSK2 flanking its ATG8 interacting motifs (AIMs) promotes DSK2-ATG8 interaction, thereby targeting BES1 for degradation. Accordingly, loss-of-function dsk2 mutants accumulate BES1, have altered global gene expression profiles, and have compromised stress responses. Our results thus reveal that plants coordinate growth and stress responses by integrating BR and autophagy pathways and identify the molecular basis of this crosstalk.

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“…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)(2)(3).…”

mentioning

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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Autophagy in Plants – What's New on the Menu?

Cited by 214 publications

References 91 publications

TRAF Family Proteins Regulate Autophagy Dynamics by Modulating AUTOPHAGY PROTEIN6 Stability in Arabidopsis

TRAF Family Proteins Regulate Autophagy Dynamics by Modulating AUTOPHAGY PROTEIN6 Stability in Arabidopsis

Selective Autophagy of BES1 Mediated by DSK2 Balances Plant Growth and Survival

ATG9 regulates autophagosome progression from the endoplasmic reticulum in Arabidopsis

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