Activation of the Rab7 GTPase by the MON1-CCZ1 Complex Is Essential for PVC-to-Vacuole Trafficking and Plant Growth in <i>Arabidopsis</i>

Cui, Yong; Zhao, Qiong; Gao, Caiji; Ding, Yu; Zeng, Yonglun; Ueda, Takashi; Nakano, Akihiko; Jiang, Liwen

doi:10.1105/tpc.114.123141

Cited by 176 publications

(160 citation statements)

References 87 publications

(120 reference statements)

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“…During seed germination proteases, such as aleurain, will be synthesized in the endoplasmic reticulum (ER) and transported to vacuoles where they attain a mature form, allowing them to degrade the storage proteins to provide energy for seed germination and amino acids for early stages of seedling growth (19,20). Here, we detected a strong accumulation of the precursor form of aleurain in DEX::RNAi-FREE1 seedlings germinated in the presence of DEX (Fig.…”

Section: Resultsmentioning

confidence: 66%

“…S1) (5). To further investigate the possible roles of FREE1 in regulating PVC-mediated vacuolar protein transport and vacuole biogenesis, we crossed the free1 +/− mutant with a plant expressing the protein storage vacuole (PSV) marker GFP-CT24, which consists of a signal peptide and GFP followed by the C-terminal 24 amino acids of the α′ subunit of β-conglycinin under the control of a seed-specific promoter that is sufficient for sorting to PSVs in Arabidopsis seeds (18,19). Interestingly, large numbers of green seeds under UV light were found in the progenies derived from the self-pollinated free1 +/− mutant plants expressing GFP-CT24 (Fig.…”

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confidence: 99%

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Dual roles of an Arabidopsis ESCRT component FREE1 in regulating vacuolar protein transport and autophagic degradation

Gao

Zhuang

Cui

et al. 2015

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

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170

165

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Protein turnover can be achieved via the lysosome/vacuole and the autophagic degradation pathways. Evidence has accumulated revealing that efficient autophagic degradation requires functional endosomal sorting complex required for transport (ESCRT) machinery. However, the interplay between the ESCRT machinery and the autophagy regulator remains unclear. Here, we show that FYVE domain protein required for endosomal sorting 1 (FREE1), a recently identified plant-specific ESCRT component essential for multivesicular body (MVB) biogenesis and plant growth, plays roles both in vacuolar protein transport and autophagic degradation. FREE1 also regulates vacuole biogenesis in both seeds and vegetative cells of Arabidopsis. Additionally, FREE1 interacts directly with a unique plant autophagy regulator SH3 DOMAIN-CONTAINING PROTEIN2 and associates with the PI3K complex, to regulate the autophagic degradation in plants. Thus, FREE1 plays multiple functional roles in vacuolar protein trafficking and organelle biogenesis as well as in autophagic degradation via a previously unidentified regulatory mechanism of cross-talk between the ESCRT machinery and autophagy process. T he endosomal-lysosomal/vacuolar pathway is the primary catabolic system of eukaryotic cells that degrades extracellular and intracellular materials. Membrane proteins destined for degradation, such as misfolded proteins or endocytosed receptors, become tagged by ubiquitin for further sorting to the endosomal-lysosomal/vacuolar system for degradation (1). During this process, an evolutionarily conserved machinery called endosomal sorting complex required for transport (ESCRT), is responsible for sorting these ubiquitinated cargos into the intraluminal vesicles (ILVs) of prevacuolar compartments/multivesicular bodies (PVCs/MVBs), which subsequently fuse with vacuoles/lysosomes to deliver their contents into the lumen for proteolytic degradation (2, 3). Malfunction of the assembly or dissociation of the ESCRT machinery disrupts MVB formation and thus results in the accumulation of ubiquitinated membrane cargos (4, 5).Macroautophagy (hereafter as autophagy) is another highly conserved catabolic process, which converges on the endosomallysosomal/vacuolar pathway to deliver aberrant organelles, longlived proteins, and protein aggregates to the lysosome/vacuole via a unique structure termed the "autophagosome" (6). Morphologically different from MVBs, autophagosomes are characterized by a double membrane structure, which is initiated from the phagophore assembly site/preautophagosome site (PAS) (7). The proteins or organelles to be degraded are encapsulated by autophagosomes that fuse either directly with the vacuole/lysosome or with endosomes like MVBs for expansion/maturation to form amphisomes, which then fuse with vacuole/lysosome for degradation. A number of conserved autophagy-related gene (ATG) proteins have been identified as participating in the autophagy pathway in eukaryotic cells (8).Even though it is generally accepted that at least one population of...

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Section: Resultsmentioning

confidence: 66%

mentioning

confidence: 99%

Dual roles of an Arabidopsis ESCRT component FREE1 in regulating vacuolar protein transport and autophagic degradation

Gao

Zhuang

Cui

et al. 2015

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

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170

165

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“…In yeast cells, the HOPS complex is recruited by the active form of RAB GTPase Ypt7/RAB7 to mediate fusion between the prevacuolar compartment membrane and vacuole/lysosome membrane with the assistance of SNARE proteins (16)(17)(18). In Arabidopsis, RAB7/RABG GTPases and a Rab5 homolog Rha1/RABF2a were also involved in vacuolar trafficking of cargo proteins (24)(25)(26). To test whether recruitment of AtVPS41 to PVCs/tonoplast is also mediated by interaction between AtVPS41 and the RAB GTPases and SNARE proteins, we performed split-ubiquitin yeast two-hybrid assays (27, 28) using AtVPS41 as a bait protein and RABF2a, RABG3c, and VAMP711 as prey proteins.…”

Section: Atvps41 Is Localized Mainly In the Late Endosomes/pvcs And Tmentioning

confidence: 99%

AtVPS41-mediated endocytic pathway is essential for pollen tube–stigma interaction in Arabidopsis

Hao

Liu

Zhong

et al. 2016

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

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In flowering plants, extensive male–female interactions are required for successful fertilization in which various signaling cascades are involved. Prevacuolar compartments (PVC) and vacuoles are two types of subcellular compartments that terminate signal transduction by sequestrating signaling molecules in yeast and mammalian cells; however, the manner in which they might be involved in male–female interactions in plants is unknown. In this study, we identified Arabidopsisthaliana vacuolar protein sorting 41 (AtVPS41), encoded by a single-copy gene with sequence similarity to yeast Vps41p, as a new factor controlling pollen tube–stigma interaction. Loss of AtVPS41 function disrupted penetration of pollen tubes into the transmitting tissue and thus led to failed male transmission. In the pollen tubes, AtVPS41 protein is associated with PVCs and the tonoplast. We demonstrate that AtVPS41 is required for the late stage of the endocytic pathway (i.e., endomembrane trafficking from PVCs to vacuoles) because internalization of cell-surface molecules was normal in the vps41-deficient pollen tubes, whereas PVC-to-vacuole trafficking was impaired. We further show that the CHCR domain is required for subcellular localization and biological functioning of AtVPS41. These results indicate that the AtVPS41-mediated late stage of the endocytic pathway is essential for pollen tube–stigma interaction in Arabidopsis.

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“…Recently, a complex consisting of SAND/MONENSIN SENSITIVITY1 and CALCIUM CAFFEINE ZINC SENSITIVITY1 (CCZ1) was demonstrated to act as an effector of canonical plant RAB5s (Cui et al, 2014;Ebine et al, 2014;Singh et al, 2014). The SAND-CCZ1 complex interacts with GTP-bound RAB5s and serves as a GEF for RAB7, which leads to RAB5-to-RAB7 conversion on the endosome.…”

Section: Introductionmentioning

confidence: 99%

ENDOSOMAL RAB EFFECTOR WITH PX-DOMAIN, an Interacting Partner of RAB5 GTPases, Regulates Membrane Trafficking to Protein Storage Vacuoles in Arabidopsis

et al. 2016

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ORCID ID: 0000-0001-7441-0203 (H.T.S.)RAB5 GTPases act as molecular switches that regulate various endosomal functions in animal cells, including homotypic fusion of early endosomes, endosomal motility, endosomal signaling, and subcompartmentalization of the endosomal membrane. RAB5 proteins fulfill these diverse functions through interactions with downstream effector molecules. Two canonical RAB5 members, ARA7 and RAB HOMOLOG1 (RHA1), are encoded in the Arabidopsis thaliana genome. ARA7 and RHA1 play crucial roles in endocytic and vacuolar trafficking pathways. Plant RAB5 GTPases function via interactions with effector molecules, whose identities and functions are currently unclear. In this study, we searched for canonical RAB5 effector molecules of Arabidopsis and identified a candidate, which we called ENDOSOMAL RAB EFFECTOR WITH PX-DOMAIN (EREX). The intimate genetic interaction between EREX and RAB5 members, the results from subcellular colocalization experiments, and the direct interaction observed in an in vitro pull-down assay strongly suggest that EREX is a genuine effector of canonical RAB5s in Arabidopsis. We further found that close homologs of EREX play partially redundant functions with EREX in the transport of seed storage proteins. Our results indicate that canonical plant RAB5s acquired distinct effector molecules from those of non-plant systems to fulfill their functions.

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Activation of the Rab7 GTPase by the MON1-CCZ1 Complex Is Essential for PVC-to-Vacuole Trafficking and Plant Growth in Arabidopsis

Cited by 176 publications

References 87 publications

Dual roles of an Arabidopsis ESCRT component FREE1 in regulating vacuolar protein transport and autophagic degradation

Dual roles of an Arabidopsis ESCRT component FREE1 in regulating vacuolar protein transport and autophagic degradation

AtVPS41-mediated endocytic pathway is essential for pollen tube–stigma interaction in Arabidopsis

ENDOSOMAL RAB EFFECTOR WITH PX-DOMAIN, an Interacting Partner of RAB5 GTPases, Regulates Membrane Trafficking to Protein Storage Vacuoles in Arabidopsis

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