The Deubiquitinating Enzyme AMSH3 Is Required for Intracellular Trafficking and Vacuole Biogenesis in<i>Arabidopsis thaliana</i>

Isono, Erika; Katsiarimpa, Anthi; Müller, Isabel; Anzenberger, Franziska; Stierhof, York‐Dieter; Geldner, Niko; Chory, Joanne; Schwechheimer, Claus

doi:10.1105/tpc.110.075952

Cited by 119 publications

(138 citation statements)

References 72 publications

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“…AMSH3, an Arabidopsis deubiquitinating enzyme processing both polyubiquitin K48-and K63-linked chains, was recently shown to be essential for vacuole biogenesis and its mutation leads to the accumulation of autophagosomes (31). AGO1 protein amount was at least fourfold enriched in this mutant, suggesting that its degradation in a nonviral context depends on AMSH3 function (Fig.…”

Section: Resultsmentioning

confidence: 90%

Degradation of the antiviral component ARGONAUTE1 by the autophagy pathway

Derrien

Baumberger

Schepetilnikov

et al. 2012

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

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255

288

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Posttranscriptional gene silencing (PTGS) mediated by siRNAs is an evolutionarily conserved antiviral defense mechanism in higher plants and invertebrates. In this mechanism, viral-derived siRNAs are incorporated into the RNA-induced silencing complex (RISC) to guide degradation of the corresponding viral RNAs. In Arabidopsis, a key component of RISC is ARGONAUTE1 (AGO1), which not only binds to siRNAs but also carries the RNA slicer activity. At present little is known about posttranslational mechanisms regulating AGO1 turnover. Here we report that the viral suppressor of RNA silencing protein P0 triggers AGO1 degradation by the autophagy pathway. Using a P0-inducible transgenic line, we observed that AGO1 degradation is blocked by inhibition of autophagy. The engineering of a functional AGO1 fluorescent reporter protein further indicated that AGO1 colocalizes with autophagy-related (ATG) protein 8a (ATG8a) positive bodies when degradation is impaired. Moreover, this pathway also degrades AGO1 in a nonviral context, especially when the production of miRNAs is impaired. Our results demonstrate that a selective process such as ubiquitylation can lead to the degradation of a key regulatory protein such as AGO1 by a degradation process generally believed to be unspecific. We anticipate that this mechanism will not only lead to degradation of AGO1 but also of its associated proteins and eventually small RNAs.

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Section: Resultsmentioning

confidence: 90%

Degradation of the antiviral component ARGONAUTE1 by the autophagy pathway

Derrien

Baumberger

Schepetilnikov

et al. 2012

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

Self Cite

255

288

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“…A number of recent reports connected light and growth regulator signaling to vacuolar sorting of PIN proteins (25,33,34), substantiating a scenario in which multiple pathways impinge on PIN protein degradation to orchestrate auxin distribution in a multifaceted developmental context. Variations in PIN polyubiquitylation might function as a common transmitter of such a diverse range of signals, but versatility and molecular constituents of this pathway remain to be determined (35,36).…”

Section: Discussionmentioning

confidence: 99%

Lysine ⁶³ -linked ubiquitylation of PIN2 auxin carrier protein governs hormonally controlled adaptation of Arabidopsis root growth

Leitner

Petrášek²,

Tomanov³

et al. 2012

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

184

220

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Cross-talk between plant cells and their surroundings requires tight regulation of information exchange at the plasma membrane (PM), which involves dynamic adjustments of PM protein localization and turnover to modulate signal perception and solute transport at the interface between cells and their surroundings. In animals and fungi, turnover of PM proteins is controlled by reversible ubiquitylation, which signals endocytosis and delivery to the cell's lytic compartment, and there is emerging evidence for related mechanisms in plants. Here, we describe the fate of Arabidopsis PIN2 protein, required for directional cellular efflux of the phytohormone auxin, and identify cis-and trans-acting mediators of PIN2 ubiquitylation. We demonstrate that ubiquitin acts as a principal signal for PM protein endocytosis in plants and reveal dynamic adjustments in PIN2 ubiquitylation coinciding with variations in vacuolar targeting and proteolytic turnover. We show that control of PIN2 proteolytic turnover via its ubiquitylation status is of significant importance for auxin distribution in root meristems and for environmentally controlled adaptations of root growth. Moreover, we provide experimental evidence indicating that PIN2 vacuolar sorting depends on modification specifically by lysine 63 -linked ubiquitin chains. Collectively, our results establish lysine 63 -linked PM cargo ubiquitylation as a regulator of polar auxin transport and adaptive growth responses in higher plants.P lants have evolved a repertoire of mechanisms for continuously adapting vital parameters in response to fluctuating environmental conditions. Sensing and responding to such variations depend to a large extent on the activity of plasma membrane (PM)-associated proteins that function in stimulus perception and solute transport. Specifically, adjustments in subcellular distribution of PM proteins are an efficient means to modulate their activity and involve continuous protein cycling between PM and endosomes as well as irreversible targeting for degradation in the lytic vacuole/lysosome (1).An evolutionary conserved machinery controls PM protein sorting for degradation, and, specifically in animals and fungi, it was demonstrated that PM protein fate is decisively influenced by their reversible ubiquitylation, triggering cargo endocytosis and delivery to the lytic compartment (2-4). Related mechanisms appear to be operative in plants (5-9) because, recently, ubiquitylation has been described for some plant PM proteins, linking nutrient transport and stimulus perception to endocytic protein turnover (6-9). Strikingly, different patterns of protein ubiquitylation have been observed, with mono-, di-, as well as polyubiquitylation implicated in regulating endocytic trafficking and degradation of distinct proteins (5). This resembles the situation in nonplant organisms, in which mono-and polyubiquitylation have been associated with cargo endocytosis (10).Vacuolar sorting was also demonstrated for PIN1-type auxin carrier proteins, which are instrumental for ...

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“…In the vacuoleless1 mutant, the biogenesis of LVs in the embryo is blocked and large numbers of autophagosomes accumulate instead (Rojo et al, 2001). Similarly, in the amsh3 mutant, in which the deubiquitinating enzyme AMSH3 is inactivated, the cells are also incapable of forming large central LVs and also accumulate increased numbers of autophagosomes (Isono et al, 2010).…”

Section: Cryofixation and Freeze-substitution Methods Are Important Fmentioning

confidence: 99%

Protein Storage Vacuoles Are Transformed into Lytic Vacuoles in Root Meristematic Cells of Germinating Seedlings by Multiple, Cell Type-Specific Mechanisms

Zheng

Staehelin

2011

Plant Physiology

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We have investigated the structural events associated with vacuole biogenesis in root tip cells of tobacco (Nicotiana tabacum) seedlings preserved by high-pressure freezing and freeze-substitution techniques. Our micrographs demonstrate that the lytic vacuoles (LVs) of root tip cells are derived from protein storage vacuoles (PSVs) by cell type-specific sets of transformation events. Analysis of the vacuole transformation pathways has been aided by the phytin-dependent black osmium staining of PSV luminal contents. In epidermal and outer cortex cells, the central LVs are formed by a process involving PSV fusion, storage protein degradation, and the gradual replacement of the PSV marker protein a-tonoplast intrinsic protein (TIP) with the LV marker protein g-TIP. In contrast, in the inner cortex and vascular cylinder cells, the transformation events are more complex. During mobilization of the stored molecules, the PSV membranes collapse osmotically upon themselves, thereby squeezing the vacuolar contents into the remaining bulging vacuolar regions. The collapsed PSV membranes then differentiate into two domains: (1) vacuole "reinflation" domains that produce pre-LVs, and (2) multilamellar autophagosomal domains that are later engulfed by the pre-LVs. The multilamellar autophagosomal domains appear to originate from concentric sheets of PSV membranes that create compartments within which the cytoplasm begins to break down. Engulfment of the multilamellar autophagic vacuoles by the pre-LVs gives rise to the mature LVs. During pre-LV formation, the PSV marker a-TIP disappears and is replaced by the LV marker g-TIP. These findings demonstrate that the central LVs of root cells arise from PSVs via cell type-specific transformation pathways.

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The Deubiquitinating Enzyme AMSH3 Is Required for Intracellular Trafficking and Vacuole Biogenesis inArabidopsis thaliana

Cited by 119 publications

References 72 publications

Degradation of the antiviral component ARGONAUTE1 by the autophagy pathway

Degradation of the antiviral component ARGONAUTE1 by the autophagy pathway

Lysine ⁶³ -linked ubiquitylation of PIN2 auxin carrier protein governs hormonally controlled adaptation of Arabidopsis root growth

Protein Storage Vacuoles Are Transformed into Lytic Vacuoles in Root Meristematic Cells of Germinating Seedlings by Multiple, Cell Type-Specific Mechanisms

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The Deubiquitinating Enzyme AMSH3 Is Required for Intracellular Trafficking and Vacuole Biogenesis inArabidopsis thaliana

Cited by 119 publications

References 72 publications

Degradation of the antiviral component ARGONAUTE1 by the autophagy pathway

Degradation of the antiviral component ARGONAUTE1 by the autophagy pathway

Lysine 63 -linked ubiquitylation of PIN2 auxin carrier protein governs hormonally controlled adaptation of Arabidopsis root growth

Protein Storage Vacuoles Are Transformed into Lytic Vacuoles in Root Meristematic Cells of Germinating Seedlings by Multiple, Cell Type-Specific Mechanisms

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Lysine ⁶³ -linked ubiquitylation of PIN2 auxin carrier protein governs hormonally controlled adaptation of Arabidopsis root growth