Synaptotagmins Maintain Diacylglycerol Homeostasis at Endoplasmic Reticulum-Plasma Membrane Contact Sites during Abiotic Stress

Ruiz-López, Noemı́; Pérez-Sancho, Jessica; Valle, Alicia Esteban del; Haslam, Richard P.; Vanneste, Steffen; Catalá, Ramón; Perea-Resa, Carlos; Damme, Daniël Van; García-Hernández, Selene; Albert, Armando; Vallarino, José G.; Lin, Jun; Friml, Jiřı́; Macho, Alberto P.; Salinas, Julio; Rosado, Abel; Napier, J. A.; Amorim‐Silva, Vítor; Botella, Miguel A.

doi:10.1101/2020.07.28.222919

Cited by 13 publications

(38 citation statements)

References 89 publications

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“…Some plasma membrane microdomains are tethered to the underlying cortical ER at so‐called ER‐plasma membrane contact sites (EPCSs) through synaptotagmins (SYT1 and SYT3) (Ruiz‐Lopez et al, 2020 ). SYT1/3 are ER proteins that bind (via C2‐domains) to phosphatidylinositolphosphate (PIP)‐containing microdomains of the plasma membrane (Figure 4 ).…”

Section: Sensing Mechanisms Of Moderate To Severe Heat Stressmentioning

confidence: 99%

Hot topic: Thermosensing in plants

Hayes

Schachtschabel

Mishkind

et al. 2021

Plant Cell & Environment

123

108

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Plants alter their morphology and cellular homeostasis to promote resilience under a variety of heat regimes. Molecular processes that underlie these responses have been intensively studied and found to encompass diverse mechanisms operating across a broad range of cellular components, timescales and temperatures. This review explores recent progress throughout this landscape with a particular focus on thermosensing in the model plant Arabidopsis. Direct temperature sensors include the photosensors phytochrome B and phototropin, the clock component ELF3 and an RNA switch. In addition, there are heat‐regulated processes mediated by ion channels, lipids and lipid‐modifying enzymes, taking place at the plasma membrane and the chloroplast. In some cases, the mechanism of temperature perception is well understood but in others, this remains an open question. Potential novel thermosensing mechanisms are based on lipid and liquid–liquid phase separation. Finally, future research directions of high temperature perception and signalling pathways are discussed.

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Section: Sensing Mechanisms Of Moderate To Severe Heat Stressmentioning

confidence: 99%

Hot topic: Thermosensing in plants

Hayes

Schachtschabel

Mishkind

et al. 2021

Plant Cell & Environment

123

108

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“…Ca 2+ is also known to regulate many actors of endomembrane trafficking including regulators of the cytoskeleton, TPLATE complex, ANNEXINs and SYNAPTOTAGMINs (Bürstenbinder et al, 2013, 2017; Carroll et al, 1998; Hepler, 2016; Schapire et al, 2008; Van Damme et al, 2006). For instance, the ER-Plasma membrane tethers protein SYT1 contains C2 domains that bind Ca 2+ and phosphoinositides (Giordano et al, 2013; Idevall-Hagren et al, 2015; Lee et al, 2019; Pérez-Sancho et al, 2015; Ruiz-Lopez et al, 2020; Yamazaki et al, 2008). As previously mentioned, the PI4Kα1 complex could be localized at ER-Plasma membrane contact sites and participate in the Ca 2+ signalling at this junction through calmodulin binding.…”

Section: Discussionmentioning

confidence: 99%

A nanodomain anchored-scaffolding complex is required for PI4Kα function and localization in plants

Noack

Bayle

Armengot

et al. 2020

Preprint

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Phosphoinositides are low-abundant lipids that participate in the acquisition of membrane identity through their spatiotemporal enrichment in specific compartments. PI4P accumulates at the plant plasma membrane driving its high electrostatic potential, and thereby facilitating interactions with polybasic regions of proteins. PI4Kα1 has been suggested to produce PI4P at the plasma membrane, but how it is recruited to this compartment is unknown. Here, we pin-point the mechanism that tethers PI4Kα1 to the plasma membrane via a nanodomain-anchored scaffolding complex. We identified that PI4Kα1 is part of a heterotetrameric complex composed of proteins from the NO-POLLEN-GERMINATION, EFR3-OF-PLANTS, and HYCCIN families. Comprehensive knock-out and knock-down strategies revealed that subunits of the PI4Kα1 complex are essential for pollen, embryonic and post-embryonic development. We further found that the PI4Kα1 complex is immobilized in plasma membrane nanodomains. Using synthetic mis-targeting strategies, we demonstrate that a combination of lipid anchoring and scaffolding localizes PI4Kα1 to the plasma membrane, which is essential for its function. Together, this work opens new perspectives on the mechanisms and function of plasma membrane nanopatterning by lipid kinases.

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“…An increase in IP3 levels may result from the hydrolysis of the PIPs to produce diacyl glycerol (DAG) due to the activation of the phospholipase C activation in response to stress (Bian et al, 2018;Saheki et al, 2016). Moreover, it has been proposed that the role of SYT1 and SYT3 in plants-and E-Syts in mammals-is to transfer DAG form the PM to the ER to maintain membrane stability (Ruiz-Lopez et al, 2020;Saheki et al, 2016). Thus, our data provide insights for the regulation of SYTs in response to IP3 and DAG production at membrane CS.…”

Section: The C2a Domain Of Syt1 Regulates Protein Functionmentioning

confidence: 99%

“…Conversely, DAG imposes negative curvature as it has no polar head (Di Paolo and De Camilli, 2006). E-Syts are regulated by the accumulation of PIPs in the PM and their function is to clear away the DAG formed by the action of phospholipase C (Ruiz-Lopez et al, 2020;Saheki et al, 2016). This suggests that the clearance of DAG, by itself, may act as a regulator of protein function as this process will contribute to membrane stabilization and hinder lipid extraction.…”

Section: Syt1 Induce Membrane Instability To Favor Lipid Transfermentioning

confidence: 99%

The structure and flexibility analysis of the Arabidopsis Synaptotagmin 1 reveal the basis of its regulation at membrane contact sites

Benavente

Siliqi

Infantes

et al. 2021

Preprint

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Cell function requires the maintenance of membrane lipid homeostasis as changes in cellular environment unbalance this equilibrium. The non-vesicular lipid transfer at endoplasmic reticulum (ER) and plasma membrane (PM) contact sites (CS) is central to restore it. Extended synaptotagmins (E-Syts) are ER proteins that play a central role in this process as they act as molecular tethers with PM and as lipid transfer proteins between these organelles. E-Syts are constitutively anchored to the ER through an N-terminal hydrophobic segment and bind to the PM via C-terminal C2 domains. In plants, synaptotagmins (SYTs) are orthologous of E-Syts and regulate the ER-PM communication by the activity of their two C2 domains in response to abiotic stresses. We have combined macromolecular crystallography, small-angle X-ray scattering, structural bioinformatics and biochemical data to analyze the regulation of plant synaptotagmin 1 (SYT1). Our data show that the binding of SYT1 to the PM is regulated by the interaction of the first C2 domain through a Ca2+-dependent lipid binding site and by a site for phosphorylated forms of phosphatidylinositol in such a way that two different molecular signals are integrated in response to stress. In addition, our data show that SYT1 is highly flexible by virtue of up to three hinge points, including one that connects the two C2 domains. This feature provides conformational freedom to SYT1 to define a large and complementary interaction surface with the PM. This structural plasticity, in turn, may facilitate lipid extraction, protein loading and subsequent transfer between PM and ER.

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Synaptotagmins Maintain Diacylglycerol Homeostasis at Endoplasmic Reticulum-Plasma Membrane Contact Sites during Abiotic Stress

Cited by 13 publications

References 89 publications

Hot topic: Thermosensing in plants

Hot topic: Thermosensing in plants

A nanodomain anchored-scaffolding complex is required for PI4Kα function and localization in plants

The structure and flexibility analysis of the Arabidopsis Synaptotagmin 1 reveal the basis of its regulation at membrane contact sites

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