Cells sense a variety of extracellular signals balancing their metabolism and physiology according to changing growth conditions. Plasma membranes are the outermost informational barriers that render cells sensitive to regulatory inputs. Membranes are composed of different types of lipids that play not only structural but also informational roles. Hormones and other regulators are sensed by specific receptors leading to the activation of lipid metabolizing enzymes. These enzymes generate lipid second messengers. Among them, phosphatidic acid (PA) is a well-known intracellular messenger that regulates various cellular processes. This lipid affects the functional properties of cell membranes and binds to specific target proteins leading to either genomic (affecting transcriptome) or non-genomic responses. The subsequent biochemical, cellular and physiological reactions regulate plant growth, development and stress tolerance. In the present review, we focus on primary (genome-independent) signaling events triggered by rapid PA accumulation in plant cells and describe the functional role of PA in mediating response to hormones and hormone-like regulators. The contributions of individual lipid signaling enzymes to the formation of PA by specific stimuli are also discussed. We provide an overview of the current state of knowledge and future perspectives needed to decipher the mode of action of PA in the regulation of cell functions.
- MeSH
- fosfolipasa D * metabolismus MeSH
- hormony metabolismus MeSH
- kyseliny fosfatidové * metabolismus MeSH
- proteiny metabolismus MeSH
- rostlinné proteiny genetika MeSH
- rostliny metabolismus MeSH
- signální transdukce fyziologie MeSH
- vývoj rostlin MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
Plant phospholipase Ds (PLDs), essential regulators of phospholipid signaling, function in multiple signal transduction cascades; however, the mechanisms regulating PLDs in response to pathogens remain unclear. Here, we found that Arabidopsis (Arabidopsis thaliana) PLDδ accumulated in cells at the entry sites of the barley powdery mildew fungus, Blumeria graminis f. sp hordei Using fluorescence recovery after photobleaching and single-molecule analysis, we observed higher PLDδ density in the plasma membrane after chitin treatment; PLDδ also underwent rapid exocytosis. Fluorescence resonance energy transfer with fluorescence lifetime imaging microscopy showed that the interaction between PLDδ and the microdomain marker AtREMORIN1.3 (AtREM1.3) increased in response to chitin, indicating that exocytosis facilitates rapid, efficient sorting of PLDδ into microdomains upon pathogen stimulus. We further unveiled a trade-off between brefeldin A (BFA)-resistant and -sensitive pathways in secretion of PLDδ under diverse conditions. Upon pathogen attack, PLDδ secretion involved syntaxin-associated VAMP721/722-mediated exocytosis sensitive to BFA. Analysis of phosphatidic acid (PA), hydrogen peroxide, and jasmonic acid (JA) levels and expression of related genes indicated that the relocalization of PLDδ is crucial for its activation to produce PA and initiate reactive oxygen species and JA signaling pathways. Together, our findings revealed that the translocation of PLDδ to papillae is modulated by exocytosis, thus triggering PA-mediated signaling in plant innate immunity.plantcell;31/12/3015/FX1F1fx1.
- MeSH
- Arabidopsis genetika imunologie metabolismus mikrobiologie MeSH
- Ascomycota patogenita MeSH
- brefeldin A imunologie metabolismus MeSH
- buněčná membrána metabolismus MeSH
- chitin imunologie metabolismus MeSH
- cyklopentany metabolismus MeSH
- exocytóza účinky léků imunologie MeSH
- fosfolipasa D genetika metabolismus MeSH
- kyseliny fosfatidové metabolismus MeSH
- nemoci rostlin imunologie mikrobiologie MeSH
- oxylipiny metabolismus MeSH
- peroxid vodíku metabolismus MeSH
- přirozená imunita * účinky léků MeSH
- proteiny huseníčku metabolismus MeSH
- proteiny Qa-SNARE metabolismus MeSH
- proteiny R-SNARE metabolismus MeSH
- proteiny SNARE genetika metabolismus MeSH
- reaktivní formy kyslíku metabolismus MeSH
- signální transdukce imunologie fyziologie MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Using Arabidopsis thaliana wild type (WT) plants and diacylglycerol kinase knockouts (single mutants - dgk3, dgk1, dgk6; double mutants - dgk3dgk7, dgk5dgk6, dgk1dgk2) we observed that the inhibitor of brassinosteroid (BR) biosynthesis, brassinazole (BRZ), drastically decreased germination of dgk mutants under salt stress, while BRZ co-administration with 24-epibrassinolide (EBL) partially improved germination rates. We also observed a statistically significant decrease in alternative and cytochrome respiratory pathways in response to BRZ treatment under salinity conditions. We showed that production of the lipid second messenger phosphatidic acid (PA) is impaired in dgk mutants in response to EBL treatment and inhibitor of diacylglycerol kinase (DGK) - R59022. This study demonstrates that dgk mutants possess lower germination rates, lower total respiration rates, an alternative respiratory pathway and PA content under optimal and high salinity conditions in response to EBL treatment comparing to WT plants.
- MeSH
- Arabidopsis chemie metabolismus MeSH
- brassinosteroidy farmakologie MeSH
- diacylglycerolkinasa antagonisté a inhibitory nedostatek metabolismus MeSH
- kyseliny fosfatidové chemie metabolismus MeSH
- salinita MeSH
- semena rostlinná účinky léků růst a vývoj metabolismus MeSH
- triazoly farmakologie MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Phosphatidic acid (PA) is a simple phospholipid observed in most organisms. PA acts as a key metabolic intermediate and a second messenger that regulates many cell activities. In plants, PA is involved in numerous cell responses induced by hormones, stress inputs and developmental processes. Interestingly, PA production can be triggered by opposite stressors, such as cold and heat, or by hormones that are considered to be antagonistic, such as abscisic acid and salicylic acid. This property questions the specificity of the responses controlled by PA. Are there generic responses to PA, meaning that cell regulation triggered by PA would be always the same, even in opposite physiological situations? Alternatively, do the responses to PA differ according to the physiological context within the cells? If so, the mechanisms that regulate the divergence of PA-controlled reactions are poorly defined. This review summarizes the latest opinions on how PA signalling is directed in plant cells and examines the intrinsic properties of PA that enable its regulatory diversity. We propose a concept whereby PA regulatory messages are perceived as complex "signatures" that take into account their production site, the availability of target proteins and the relevant cellular environments.
- MeSH
- fyziologie rostlin * MeSH
- kyseliny fosfatidové chemie metabolismus MeSH
- molekulární struktura MeSH
- rostlinné proteiny genetika metabolismus MeSH
- rostliny chemie genetika metabolismus MeSH
- sekvence aminokyselin MeSH
- signální transdukce * MeSH
- vazba proteinů MeSH
- vazebná místa genetika MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
Membrane surface charge is critical for the transient, yet specific recruitment of proteins with polybasic regions to certain organelles. In eukaryotes, the plasma membrane (PM) is the most electronegative compartment of the cell, which specifies its identity. As such, membrane electrostatics is a central parameter in signaling, intracellular trafficking, and polarity. Here, we explore which are the lipids that control membrane electrostatics using plants as a model. We show that phosphatidylinositol-4-phosphate (PI4P), phosphatidic acidic (PA), and phosphatidylserine (PS) are separately required to generate the electrostatic signature of the plant PM. In addition, we reveal the existence of an electrostatic territory that is organized as a gradient along the endocytic pathway and is controlled by PS/PI4P combination. Altogether, we propose that combinatorial lipid composition of the cytosolic leaflet of organelles not only defines the electrostatic territory but also distinguishes different functional compartments within this territory by specifying their varying surface charges.
- MeSH
- Arabidopsis růst a vývoj metabolismus MeSH
- buněčná membrána metabolismus MeSH
- fosfatidylinositolfosfáty metabolismus MeSH
- fosfatidylseriny metabolismus MeSH
- kořeny rostlin růst a vývoj metabolismus MeSH
- kyseliny fosfatidové metabolismus MeSH
- organely MeSH
- proteiny huseníčku metabolismus MeSH
- signální transdukce MeSH
- statická elektřina * MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Using Brassica napus roots we observed statistically significant increase in alternative respiratory pathway in response to exogenous 24-epibrassinolide (EBL) under optimal conditions and salinity. Also we observed activation of phospholipid signaling under the same conditions in response to EBL by measuring levels of lipid second messengers - diacylglycerol (DAG) and phosphatidic acid (PA). We found that brassinosteroids cause closure of stomata in isolated leaf disks while inhibitors of alternative oxidase cancelled these effects. This study demonstrates that BRs activate total respiration rate, alternative respiratory pathway, production of PA and DAG, stimulate stomata closure and growth under optimal conditions and salinity. Also, specific inhibitor of brassinosteroids biosynthesis decreased alternative respiratory pathway and production of lipid messengers in rape plants.
- MeSH
- Brassica napus účinky léků enzymologie metabolismus MeSH
- brassinosteroidy farmakologie MeSH
- diglyceridy metabolismus MeSH
- kořeny rostlin účinky léků enzymologie metabolismus MeSH
- kyseliny fosfatidové metabolismus MeSH
- listy rostlin účinky léků enzymologie metabolismus MeSH
- mitochondriální proteiny metabolismus MeSH
- oxidoreduktasy metabolismus MeSH
- průduchy rostlin účinky léků enzymologie metabolismus MeSH
- rostlinné proteiny metabolismus MeSH
- steroidy heterocyklické farmakologie MeSH
- Publikační typ
- časopisecké články MeSH
Although phosphatidic acid (PA) is structurally the simplest membrane phospholipid, it has been implicated in the regulation of many cellular events, including cytoskeletal dynamics, membrane trafficking and stress responses. Plant PA shows rapid turnover but the information about its spatio-temporal distribution in plant cells is missing. Here we demonstrate the use of a lipid biosensor that enables us to monitor PA dynamics in plant cells. The biosensor consists of a PA-binding domain of yeast SNARE Spo20p fused to fluorescent proteins. Live-cell imaging of PA dynamics in transiently transformed tobacco (Nicotiana tabacum) pollen tubes was performed using confocal laser scanning microscopy. In growing pollen tubes, PA shows distinct annulus-like fluorescence pattern in the plasma membrane behind the extreme tip. Coexpression studies with markers for other plasmalemma signaling lipids phosphatidylinositol 4,5-bisphosphate and diacylglycerol revealed limited colocalization at the shoulders of the apex. PA distribution and concentrations show distinct responses to various lipid signaling inhibitors. Fluorescence recovery after photobleaching (FRAP) analysis suggests high PA turnover in the plasma membrane. Our data show that a biosensor based on the Spo20p-PA binding domain is suitable for live-cell imaging of PA also in plant cells. In tobacco pollen tubes, distinct subapical PA maximum corroborates its involvement in the regulation of endocytosis and actin dynamics.
- MeSH
- biosenzitivní techniky metody MeSH
- buněčná membrána chemie metabolismus MeSH
- diglyceridy metabolismus MeSH
- fluorescence MeSH
- fosfatidylinositol-4,5-difosfát metabolismus MeSH
- fosfolipasa D metabolismus MeSH
- fotovybělování MeSH
- kyseliny fosfatidové analýza metabolismus MeSH
- počítačové zpracování obrazu MeSH
- proteiny Qb-SNARE genetika metabolismus MeSH
- proteiny Qc-SNARE genetika metabolismus MeSH
- pylová láčka genetika růst a vývoj metabolismus MeSH
- rekombinantní fúzní proteiny genetika metabolismus MeSH
- Saccharomyces cerevisiae - proteiny genetika metabolismus MeSH
- tabák cytologie metabolismus MeSH
- vazebná místa MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Plants respond to diverse biotic and abiotic stimuli as well as to endogenous developmental cues. Many of these stimuli result in altered activity of phospholipase D (PLD), an enzyme that hydrolyzes structural phospholipids producing phosphatidic acid (PA). PA is a key signaling intermediate in animals, but its targets in plants are relatively uncharacterized. Recent studies have demonstrated that the cytoskeleton is a major target of PLD-PA signaling and identified a positive feedback loop between actin turnover and PLD activity. Moreover, two cytoskeletal proteins, capping protein and MAP65-1, have been identified as PA-binding proteins regulating actin and microtubule organization and dynamics. In this review, we highlight the role of the PLD-PA module as an important hub for housekeeping and stress-induced regulation of membrane-associated cytoskeletal dynamics.
- MeSH
- aktiny metabolismus MeSH
- buněčná membrána metabolismus MeSH
- cytoskelet metabolismus MeSH
- fosfolipasa D metabolismus MeSH
- fyziologický stres MeSH
- fyziologie rostlin MeSH
- kyseliny fosfatidové metabolismus MeSH
- mikrotubuly metabolismus MeSH
- rostlinné proteiny metabolismus MeSH
- rostliny enzymologie MeSH
- signální transdukce MeSH
- vazba proteinů MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
- Research Support, U.S. Gov't, Non-P.H.S. MeSH
Phosphoglycerolipids are essential structural constituents of membranes and some also have important cell signalling roles. In this review, we focus on phosphoglycerolipids that are mediators in hormone signal transduction in plants. We first describe the structures of the main signalling phosphoglycerolipids and the metabolic pathways that generate them, namely the phospholipase and lipid kinase pathways. In silico analysis of Arabidopsis transcriptome data provides evidence that the genes encoding the enzymes of these pathways are transcriptionally regulated in responses to hormones, suggesting some link with hormone signal transduction. The involvement of phosphoglycerolipid signalling in the early responses to abscisic acid, salicylic acid and auxins is then detailed. One of the most important signalling lipids in plants is phosphatidic acid. It can activate or inactivate protein kinases and/or protein phosphatases involved in hormone signalling. It can also activate NADPH oxidase leading to the production of reactive oxygen species. We will interrogate the mechanisms that allow the activation/deactivation of the lipid pathways, in particular the roles of G proteins and calcium. Mediating lipids thus appear as master players of cell signalling, modulating, if not controlling, major transducing steps of hormone signals.
- MeSH
- Arabidopsis fyziologie MeSH
- fosfolipasy metabolismus MeSH
- fosfotransferasy metabolismus MeSH
- glycerofosfolipidy metabolismus MeSH
- kyselina abscisová metabolismus MeSH
- kyseliny fosfatidové metabolismus MeSH
- regulace genové exprese u rostlin MeSH
- regulátory růstu rostlin metabolismus MeSH
- rostlinné proteiny metabolismus MeSH
- rostliny MeSH
- signální transdukce fyziologie MeSH
- transkriptom MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
The actin cytoskeleton is a dynamic structure that coordinates numerous fundamental processes in eukaryotic cells. Dozens of actin-binding proteins are known to be involved in the regulation of actin filament organization or turnover and many of these are stimulus-response regulators of phospholipid signaling. One of these proteins is the heterodimeric actin-capping protein (CP) which binds the barbed end of actin filaments with high affinity and inhibits both addition and loss of actin monomers at this end. The ability of CP to bind filaments is regulated by signaling phospholipids, which inhibit the activity of CP; however, the exact mechanism of this regulation and the residues on CP responsible for lipid interactions is not fully resolved. Here, we focus on the interaction of CP with two signaling phospholipids, phosphatidic acid (PA) and phosphatidylinositol (4,5)-bisphosphate (PIP(2)). Using different methods of computational biology such as homology modeling, molecular docking and coarse-grained molecular dynamics, we uncovered specific modes of high affinity interaction between membranes containing PA/phosphatidylcholine (PC) and plant CP, as well as between PIP(2)/PC and animal CP. In particular, we identified differences in the binding of membrane lipids by animal and plant CP, explaining previously published experimental results. Furthermore, we pinpoint the critical importance of the C-terminal part of plant CPα subunit for CP-membrane interactions. We prepared a GST-fusion protein for the C-terminal domain of plant α subunit and verified this hypothesis with lipid-binding assays in vitro.
- MeSH
- aktin zastřešující proteiny antagonisté a inhibitory chemie genetika metabolismus MeSH
- fosfatidylinositolfosfáty chemie metabolismus MeSH
- fylogeneze MeSH
- hydrofobní a hydrofilní interakce MeSH
- kur domácí MeSH
- kyseliny fosfatidové chemie metabolismus MeSH
- molekulární modely MeSH
- molekulární sekvence - údaje MeSH
- mutace MeSH
- proteiny huseníčku antagonisté a inhibitory chemie genetika metabolismus MeSH
- ptačí proteiny antagonisté a inhibitory chemie genetika metabolismus MeSH
- sekvence aminokyselin MeSH
- sekvenční seřazení MeSH
- vazba proteinů MeSH
- výpočetní biologie MeSH
- vztahy mezi strukturou a aktivitou MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Research Support, U.S. Gov't, Non-P.H.S. MeSH