ER assembly of SNARE complexes mediating formation of partitioning membrane in Arabidopsis cytokinesis

Karnahl, Matthias; Park, Misoon; Mayer, Ulríke; Hiller, Ulrike; Jürgens, Gerd

doi:10.7554/elife.25327

Cited by 25 publications

(27 citation statements)

References 23 publications

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“…S7 ) and depicted GFP signals seem to be retained in the vesicle compartments. To confirm these results, we next generated fusion protein of well-known vesicle marker involved in the secretory pathway at plant system; VAMP721 protein was selected (Karnahl et al, 2017). We first determined the subcellular localization of VAMP721 protein subjected to mock or Exo1 treatment in N. benthamiana leaves.…”

Section: Resultsmentioning

confidence: 94%

Glucosylhydroxyceramides Modulate Secretion Machinery of a Subset of Plasmodesmata Proteins and a Change in the Callose Accumulation

Iswanto

Shon

et al. 2020

Preprint

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The plasma membranes encapsulated in the plasmodesmata (PDs) with symplasmic nano-channels contain abundant lipid rafts, which are enriched by sphingolipids and sterols. The attenuation of sterol compositions has demonstrated the role played by lipid raft integrity in the intercellular trafficking of glycosylphosphatidylinositol (GPI)-anchored PD proteins, particularly affecting in the callose enhancement. The presence of callose at PD is tightly attributed to the callose metabolic enzymes, callose synthases (CalSs) and β-1,3-glucanases (BGs) in regulating callose accumulation and callose degradation, respectively. Sphingolipids have been implicated in signaling and membrane protein trafficking, however the underlying processes linking sphingolipid compositions to the control of symplasmic apertures remain unknown. A wide variety of sphingolipids in plants prompts us to investigate which sphingolipid molecules are important in regulating symplasmic apertures. Here, we demonstrate that perturbations of sphingolipid metabolism by introducing several potential sphingolipid (SL) pathway inhibitors and genetically modifying SL contents from two independent SL pathway mutants are able to modulate callose deposition to control symplasmic connectivity. Our data from pharmacological and genetic approaches show that the alteration in glucosylhydroxyceramides (GlcHCers) particularly disturb the secretory machinery for GPI-anchored PdBG2 protein, resulting in an over accumulated callose. Moreover, our results reveal that SL-enriched lipid rafts link symplasmic channeling to PD callose homeostasis by controlling the targeting of GPI-anchored PdBG2. This study elevates our understanding of the molecular linkage underlying intracellular trafficking and precise targeting to specific destination of GPI-anchored PD proteins incorporated with GlcHCers contents.

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Section: Resultsmentioning

confidence: 94%

Glucosylhydroxyceramides Modulate Secretion Machinery of a Subset of Plasmodesmata Proteins and a Change in the Callose Accumulation

Iswanto

Shon

et al. 2020

Preprint

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“…A physical interaction between Sec6 and Sec1/munc18 (SM) family protein KEULE was proposed to be an important regulatory step in cytokinetic vesicle fusion in Arabidopsis (Wu et al, 2013). KEULE contributes to fusion by preventing the important cytokinetic SNARE-component KNOLLE from refolding into its closed, non-fusion-competent conformation, thereby allowing the formation of fusogenic trans-SNARE complexes among vesicles delivered to the cell plate (Park et al, 2012; Karnahl et al, 2017; Jürgens et al, 2015). Whether the Sec6 interaction regulates this specific activity is presently unknown.…”

Section: Resultsmentioning

confidence: 99%

Exocyst subunit Sec6 is positioned by microtubule overlaps in the moss phragmoplast prior to the arrival of cell plate membrane

Tang

Overdijk

et al. 2018

Preprint

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MAP65 24 25 Summary statement: We performed a time-resolved localization screen of multiple 26 subunits of the exocyst complex throughout moss cytokinesis and show that each subunit 27 has a unique spatiotemporal recruitment pattern. 28 29 2 Abstract 30 31 During plant cytokinesis a radially expanding membrane-enclosed cell plate is formed 32 from fusing vesicles that compartmentalizes the cell in two. How fusion is spatially 33 restricted to the site of cell plate formation is unknown. Aggregation of cell-plate 34 membrane starts near regions of microtubule overlap within the bipolar phragmoplast 35 apparatus of the moss Physcomitrella patens. Since vesicle fusion generally requires 36 coordination of vesicle tethering and subsequent fusion activity we analysed the 37 subcellular localization of several subunits of the exocyst, a tethering complex active 38 during plant cytokinesis. We found that Sec6, but neither Sec3 or Sec5 subunits localized 39 to microtubule overlap regions in advance of cell plate construction started in moss. 40 Moreover, Sec6 exhibited a conserved physical interaction with an orthologue of the 41 Sec1/Munc18 protein KEULE, an important regulator for cell-plate membrane vesicle 42 fusion in Arabidopsis. Recruitment of PpKEULE and vesicles to the early cell plate was 43 delayed upon Sec6 gene silencing. Our findings thus suggest that vesicle-vesicle fusion is 44 in part enabled by a pool of exocyst subunits at microtubule overlaps that is recruited 45 independent of the delivery of vesicles. 46 47 56 2014; Boruc and Van Damme, 2015). Adaptations of canonical trafficking mechanisms 57 are however required because there is no pre-existing target membrane at the site of cell 58 3 division to which vesicles can fuse. Instead, membrane deposition is thought to be 59 initiated by 'homotypic' fusion of vesicles (Smertenko et al., 2017). This raises the 60 question of how vesicle fusion is spatially restricted to the site of cell division and not 61 spuriously throughout the cell when vesicles meet. It is thought that vesicles are 62 transported along polarized microtubules to the centre of the phragmoplast, a 63 cytoskeletal apparatus that supports cell plate assembly. Although locally concentrating 64 vesicles may enhance the fusion rates of fusion-competent vesicles, it is unclear whether 65 a transport-based mechanism alone can provide the spatial accuracy required to build a 66 straight and flat cell plate. Recently we identified short stretches of antiparallel 67 microtubule overlap at the midzone of phragmoplasts in the moss Physcomitrella patens 68 as sites where membrane build up is initiated (de Keijzer et al., 2017). It remained 69 however unclear whether there are molecules at overlaps that trigger vesicle fusion 70 locally. 71 In eukaryotic cells the fusion of transport vesicles with endomembrane compartments 72 and the plasma membrane relies on the combined action of fusion and tethering 73 complexes. The force driving the fusion of a vesicle and its destination membrane is 74 almost...

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“…SNARE complexes occur in two different states; a trans-SNARE complex between the v-SNARE on the vesicle and the t-SNAREs on the target membrane, and a cis-SNARE complex where both v-and t-SNAREs are present on the same membrane until they are disassembled by the ATPase NSF and SNAPs (Südhof and Rothman, 2009). It was recently shown that, also before vesicle fusion, SNAREs involved in cytokinesis are transported to their site of action as cis-SNARE complexes, which may apply to other secretory SNAREs as well (Karnahl et al, 2017). The actual vesicle fusion event involving trans-SNARE complexes is short-lived compared to the lifetime of cis-SNARE complexes.…”

Section: Discussionmentioning

confidence: 99%

SNARE Complexity in Arbuscular Mycorrhizal Symbiosis

et al. 2020

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How cells control the proper delivery of vesicles and their associated cargo to specific plasma membrane (PM) domains upon internal or external cues is a major question in plant cell biology. A widely held hypothesis is that expansion of plant exocytotic machinery components, such as SNARE proteins, has led to a diversification of exocytotic membrane trafficking pathways to function in specific biological processes. A key biological process that involves the creation of a specialized PM domain is the formation of a host-microbe interface (the peri-arbuscular membrane) in the symbiosis with arbuscular mycorrhizal fungi. We have previously shown that the ability to intracellularly host AM fungi correlates with the evolutionary expansion of both v-(VAMP721d/e) and t-SNARE (SYP132α) proteins, that are essential for arbuscule formation in Medicago truncatula. Here we studied to what extent the symbiotic SNAREs are different from their non-symbiotic family members and whether symbiotic SNAREs define a distinct symbiotic membrane trafficking pathway. We show that all tested SYP1 family proteins, and most of the non-symbiotic VAMP72 members, are able to complement the defect in arbuscule formation upon knock-down/-out of their symbiotic counterparts when expressed at sufficient levels. This functional redundancy is in line with the ability of all tested v-and t-SNARE combinations to form SNARE complexes. Interestingly, the symbiotic t-SNARE SYP132α appeared to occur less in complex with v-SNAREs compared to the non-symbiotic syntaxins in arbuscule-containing cells. This correlated with a preferential localization of SYP132α to functional branches of partially collapsing arbuscules, while non-symbiotic syntaxins accumulate at the degrading parts. Overexpression of VAMP721e caused a shift in SYP132α localization toward the degrading parts, suggesting an influence on its endocytic turnover. These data indicate that the symbiotic SNAREs do not selectively interact to define a symbiotic vesicle trafficking pathway, but that symbiotic SNARE complexes are more rapidly disassembled resulting in a preferential localization of SYP132α at functional arbuscule branches.

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ER assembly of SNARE complexes mediating formation of partitioning membrane in Arabidopsis cytokinesis

Cited by 25 publications

References 23 publications

Glucosylhydroxyceramides Modulate Secretion Machinery of a Subset of Plasmodesmata Proteins and a Change in the Callose Accumulation

Glucosylhydroxyceramides Modulate Secretion Machinery of a Subset of Plasmodesmata Proteins and a Change in the Callose Accumulation

Exocyst subunit Sec6 is positioned by microtubule overlaps in the moss phragmoplast prior to the arrival of cell plate membrane

SNARE Complexity in Arbuscular Mycorrhizal Symbiosis

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