A whole-cell electron tomography model of vacuole biogenesis in Arabidopsis root cells

Cui, Yong; Cao, Wenhan; He, Yilin; Zhao, Qiong; Wakazaki, Mayumi; Zhuang, Xiaohong; Gao, Jiayi; Zeng, Yonglun; Gao, Caiji; Ding, Yu; Wong, Hiu Yan; Wong, Wing Shing; Lam, Ham Karen; Wang, Pengfei; Ueda, Takashi; Rojas-Pierce, Marcela; Toyooka, Kiminori; Kang, Byung-Ho; Jiang, Liwen

doi:10.1038/s41477-018-0328-1

Cited by 103 publications

(88 citation statements)

References 48 publications

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“…We examined vacuole morphology after ES17 treatment using the tonoplast marker protein YFP-VAMP711. ES17 induced the formation of rounded fragmented structures resembling the ab-errant vacuoles reported in mutants of PVC-tonoplast fusion (11,12,30,31) (Fig. 2B).…”

Section: Inhibition Of Late Compartment Fusion With the Tonoplast Altmentioning

confidence: 52%

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Interaction between VPS35 and RABG3f is necessary as a checkpoint to control fusion of late compartments with the vacuole

Rodríguez-Furlán

Domozych

Qian

et al. 2019

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

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Vacuoles are essential organelles in plants, playing crucial roles, such as cellular material degradation, ion and metabolite storage, and turgor maintenance. Vacuoles receive material via the endocytic, secretory, and autophagic pathways. Membrane fusion is the last step during which prevacuolar compartments (PVCs) and autophagosomes fuse with the vacuole membrane (tonoplast) to deliver cargoes. Protein components of the canonical intracellular fusion machinery that are conserved across organisms, including Arabidopsis thaliana, include complexes, such as soluble N-ethylmaleimide–sensitive factor attachment protein receptors (SNAREs), that catalyze membrane fusion, and homotypic fusion and vacuole protein sorting (HOPS), that serve as adaptors which tether cargo vesicles to target membranes for fusion under the regulation of RAB-GTPases. The mechanisms regulating the recruitment and assembly of tethering complexes are not well-understood, especially the role of RABs in this dynamic regulation. Here, we report the identification of the small synthetic molecule Endosidin17 (ES17), which interferes with synthetic, endocytic, and autophagic traffic by impairing the fusion of late endosome compartments with the tonoplast. Multiple independent target identification techniques revealed that ES17 targets the VPS35 subunit of the retromer tethering complex, preventing its normal interaction with the Arabidopsis RAB7 homolog RABG3f. ES17 interference with VPS35–RABG3f interaction prevents the retromer complex to endosome anchoring, resulting in retention of RABG3f. Using multiple approaches, we show that VPS35–RABG3f–GTP interaction is necessary to trigger downstream events like HOPS complex assembly and fusion of late compartments with the tonoplast. Overall, our results support a role for the interaction of RABG3f–VPS35 as a checkpoint in the control of traffic toward the vacuole.

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Section: Inhibition Of Late Compartment Fusion With the Tonoplast Altmentioning

confidence: 52%

“…Similar phenotypes are found in mutants interfering with fusion of PVC with the tonoplast. Examples include vps39, ccz1ab, sand1, amiRvps41, vps11, and vps33-2 (11,15,30). Based on similar cytosolic accumulations of YFP-VSR2 and Ara7-RFP during ES17 treatment ( Fig.…”

Section: Inhibition Of Late Compartment Fusion With the Tonoplast Altmentioning

confidence: 99%

Interaction between VPS35 and RABG3f is necessary as a checkpoint to control fusion of late compartments with the vacuole

Rodríguez-Furlán

Domozych

Qian

et al. 2019

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

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“…Recently, MVBs were discussed to be taken up into the vacuole by autophagy 66 . Additionally, studies in A. thaliana root cells have shown that central vacuoles were derived from MVB to small vacuole transition and subsequent fusions of small vacuoles 67 .…”

Section: Discussionmentioning

confidence: 99%

Protein sorting into protein bodies during barley endosperm development is putatively regulated by cytoskeleton members, MVBs and the HvSNF7s

Roustan

Hilscher

Weidinger

et al. 2020

Sci Rep

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cereal endosperm is a short-lived tissue adapted for nutrient storage, containing specialized organelles, such as protein bodies (pBs) and protein storage vacuoles (pSVs), for the accumulation of storage proteins. During development, protein trafficking and storage require an extensive reorganization of the endomembrane system. Consequently, endomembrane-modifying proteins will influence the final grain quality and yield. However, little is known about the molecular mechanism underlying endomembrane system remodeling during barley grain development. By using label-free quantitative proteomics profiling, we quantified 1,822 proteins across developing barley grains. Based on proteome annotation and a homology search, 94 proteins associated with the endomembrane system were identified that exhibited significant changes in abundance during grain development. Clustering analysis allowed characterization of three different development phases; notably, integration of proteomics data with in situ subcellular microscopic analyses showed a high abundance of cytoskeleton proteins associated with acidified PBs at the early development stages. Moreover, endosomal sorting complex required for transport (ESCRT)-related proteins and their transcripts are most abundant at early and mid-development. Specifically, multivesicular bodies (MVBs), and the ESCRT-III HvSNF7 proteins are associated with PBs during barley endosperm development. Together our data identified promising targets to be genetically engineered to modulate seed storage protein accumulation that have a growing role in health and nutritional issues. After differentiation, fully developed cereal endosperm makes up to 75% of the grain weight and covers four major cell types: aleurone, starchy endosperm, transfer cells, and the cells of the embryo surrounding region 1. The starchy endosperm thereby is characterized as a storage site, accumulating starch and seed storage proteins (SSPs) 2. The aleurone layer plays essential roles during seed germination and mobilizes starch and SSP reserves in the starchy endosperm by releasing hydrolytic enzymes that are responsible for the degradation of stored nutrients in the endosperm 2. Contrary to the persistent endosperm of cereals, the cellular endosperm of Arabidopsis thaliana (A. thaliana) supports the developing and growing embryo, resulting in a gradually depleted endosperm as the embryo grows. Finally, the massive A. thaliana embryo is only accompanied by a single peripheral layer, the aleurone layer, in mature seeds 2. Consequently, A. thaliana cannot to be used as a model system to study the endomembrane system in grain endosperm.

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“…The mechanism regulating vacuole morphology has been well characterized, although most studies have focused on developing cells, such as embryo and root epidermal cells (25,26,44,46,47). In this study, we investigated the dynamics of vacuole morphology in guard cells.…”

Section: Discussionmentioning

confidence: 99%

AP3M harbors actin filament binding activity that is crucial for vacuole morphology and stomatal closure in Arabidopsis

Zheng

Jiang

Wang

et al. 2019

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

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Stomatal movement is essential for plant growth. This process is precisely regulated by various cellular activities in guard cells. F-actin dynamics and vacuole morphology are both involved in stomatal movement. The sorting of cargoes by clathrin adaptor protein (AP) complexes from the Golgi to the vacuole is critical for establishing a normal vacuole morphology. In this study, we demonstrate that the medium subunit of the AP3 complex (AP3M) binds to and severs actin filaments in vitro and that it participates in the sorting of cargoes (such as the sucrose exporter SUC4) to the tonoplast, and thereby regulates stomatal closure in Arabidopsis thaliana. Defects in AP3 or SUC4 led to more rapid water loss and delayed stomatal closure, as well as hypersensitivity to drought stress. In ap3m mutants, the F-actin status was altered compared to the wild type, and the sorted cargoes failed to localize to the tonoplast. AP3M contains a previously unidentified F-actin binding domain that is conserved in AP3M homologs in both plants and animals. Mutations in the F-actin binding domain of AP3M abolished its F-actin binding activity in vitro, leading to an aberrant vacuole morphology and reduced levels of SUC4 on the tonoplast in guard cells. Our findings indicate that the F-actin binding activity of AP3M is required for the precise localization of AP3-dependent cargoes to the tonoplast and for the regulation of vacuole morphology in guard cells during stomatal closure.

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A whole-cell electron tomography model of vacuole biogenesis in Arabidopsis root cells

Cited by 103 publications

References 48 publications

Interaction between VPS35 and RABG3f is necessary as a checkpoint to control fusion of late compartments with the vacuole

Interaction between VPS35 and RABG3f is necessary as a checkpoint to control fusion of late compartments with the vacuole

Protein sorting into protein bodies during barley endosperm development is putatively regulated by cytoskeleton members, MVBs and the HvSNF7s

AP3M harbors actin filament binding activity that is crucial for vacuole morphology and stomatal closure in Arabidopsis

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