Nejvíce citovaný článek - PubMed ID 22639652
Turnover of Phosphatidic Acid through Distinct Signaling Pathways Affects Multiple Aspects of Pollen Tube Growth in Tobacco
Flagellin perception is a keystone of pattern-triggered immunity in plants. The recognition of this protein by a plasma membrane (PM) receptor complex is the beginning of a signaling cascade that includes protein phosphorylation and the production of reactive oxygen species (ROS). In both Arabidopsis (Arabidopsis thaliana) seedlings and suspension cells, we found that treatment with flg22, a peptide corresponding to the most conserved domain of bacterial flagellin, caused a rapid and transient decrease in the level of phosphatidylinositol (PI) 4,5-bisphosphate along with a parallel increase in phosphatidic acid (PA). In suspension cells, inhibitors of either phosphoinositide-dependent phospholipases C (PLC) or diacylglycerol kinases (DGKs) inhibited flg22-triggered PA production and the oxidative burst. In response to flg22, receptor-like kinase-deficient fls2, bak1, and bik1 mutants (FLAGELLIN SENSITIVE 2, BRASSINOSTEROID INSENSITIVE 1-associated kinase 1, and BOTRYTIS-INDUCED KINASE 1, respectively) produced less PA than wild-type (WT) plants, whereas this response did not differ in NADPH oxidase-deficient rbohD (RESPIRATORY BURST OXIDASE HOMOLOG D) plants. Among the DGK-deficient lines tested, the dgk5.1 mutant produced less PA and less ROS after flg22 treatment compared with WT seedlings. In response to flg22, dgk5.1 plants showed lower callose accumulation and impaired resistance to Pseudomonas syringae pv. tomato DC3000 hrcC-. Transcriptomics revealed that the basal expression of defense-related genes was altered in dgk5.1 seedlings compared with the WT. A GFP-DGK5 fusion protein localized to the PM, where RBOHD and PLC2 (proteins involved in plant immunity) are also located. The role of DGK5 and its enzymatic activity in flagellin signaling and fine-tuning of early immune responses in plant-microbe interactions is discussed.
- MeSH
- Arabidopsis * metabolismus MeSH
- diacylglycerolkinasa genetika metabolismus MeSH
- flagelin farmakologie genetika MeSH
- imunita rostlin MeSH
- protein-serin-threoninkinasy MeSH
- proteiny huseníčku * genetika metabolismus MeSH
- Pseudomonas syringae fyziologie MeSH
- reaktivní formy kyslíku metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- BIK1 protein, Arabidopsis MeSH Prohlížeč
- diacylglycerolkinasa MeSH
- flagelin MeSH
- protein-serin-threoninkinasy MeSH
- proteiny huseníčku * MeSH
- reaktivní formy kyslíku MeSH
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.
- Klíčová slova
- autophagy, biologically active substance, diacylglycerol kinase, phosphatidic acid, phospholipase, phospholipid, signal transduction, targets,
- 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
- Názvy látek
- fosfolipasa D * MeSH
- hormony MeSH
- kyseliny fosfatidové * MeSH
- proteiny MeSH
- rostlinné proteiny MeSH
Polarized exocytosis is essential for many vital processes in eukaryotic cells, where secretory vesicles are targeted to distinct plasma membrane domains characterized by their specific lipid-protein composition. Heterooctameric protein complex exocyst facilitates the vesicle tethering to a target membrane and is a principal cell polarity regulator in eukaryotes. The architecture and molecular details of plant exocyst and its membrane recruitment have remained elusive. Here, we show that the plant exocyst consists of two modules formed by SEC3-SEC5-SEC6-SEC8 and SEC10-SEC15-EXO70-EXO84 subunits, respectively, documenting the evolutionarily conserved architecture within eukaryotes. In contrast to yeast and mammals, the two modules are linked by a plant-specific SEC3-EXO70 interaction, and plant EXO70 functionally dominates over SEC3 in the exocyst recruitment to the plasma membrane. Using an interdisciplinary approach, we found that the C-terminal part of EXO70A1, the canonical EXO70 isoform in Arabidopsis, is critical for this process. In contrast to yeast and animal cells, the EXO70A1 interaction with the plasma membrane is mediated by multiple anionic phospholipids uniquely contributing to the plant plasma membrane identity. We identified several evolutionary conserved EXO70 lysine residues and experimentally proved their importance for the EXO70A1-phospholipid interactions. Collectively, our work has uncovered plant-specific features of the exocyst complex and emphasized the importance of the specific protein-lipid code for the recruitment of peripheral membrane proteins.
- Klíčová slova
- EXO70A1, cell polarity, exocyst, phospholipids, plasma membrane,
- MeSH
- Arabidopsis metabolismus MeSH
- buněčná membrána metabolismus MeSH
- cytoplazma metabolismus MeSH
- exocytóza MeSH
- fosfolipidy metabolismus MeSH
- polarita buněk MeSH
- proteiny huseníčku metabolismus MeSH
- proteomika metody MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- EXO70A1 protein, Arabidopsis MeSH Prohlížeč
- fosfolipidy MeSH
- proteiny huseníčku MeSH
Increasing evidence suggests that posttranscriptional regulation is a key player in the transition between mature pollen and the progamic phase (from pollination to fertilization). Nonetheless, the actors in this messenger RNA (mRNA)-based gene expression reprogramming are poorly understood. We demonstrate that the evolutionarily conserved RNA-binding protein LARP6C is necessary for the transition from dry pollen to pollen tubes and the guided growth of pollen tubes towards the ovule in Arabidopsis thaliana. In dry pollen, LARP6C binds to transcripts encoding proteins that function in lipid synthesis and homeostasis, vesicular trafficking, and polarized cell growth. LARP6C also forms cytoplasmic granules that contain the poly(A) binding protein and possibly represent storage sites for translationally silent mRNAs. In pollen tubes, the loss of LARP6C negatively affects the quantities and distribution of storage lipids, as well as vesicular trafficking. In Nicotiana benthamiana leaf cells and in planta, analysis of reporter mRNAs designed from the LARP6C target MGD2 provided evidence that LARP6C can shift from a repressor to an activator of translation when the pollen grain enters the progamic phase. We propose that LARP6C orchestrates the timely posttranscriptional regulation of a subset of mRNAs in pollen during the transition from the quiescent to active state and along the progamic phase to promote male fertilization in plants.
- MeSH
- 5' nepřekládaná oblast MeSH
- Arabidopsis cytologie genetika růst a vývoj MeSH
- cytoplazmatická granula genetika metabolismus MeSH
- geneticky modifikované rostliny MeSH
- lipidy biosyntéza genetika MeSH
- messenger RNA genetika metabolismus MeSH
- proteiny huseníčku genetika metabolismus MeSH
- proteiny vázající RNA genetika metabolismus MeSH
- pylová láčka cytologie genetika růst a vývoj MeSH
- regulace genové exprese u rostlin MeSH
- RNA rostlin metabolismus MeSH
- tabák genetika MeSH
- vazba proteinů MeSH
- vazebná místa MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- 5' nepřekládaná oblast MeSH
- AT3G19090 protein, Arabidopsis MeSH Prohlížeč
- lipidy MeSH
- messenger RNA MeSH
- proteiny huseníčku MeSH
- proteiny vázající RNA MeSH
- RNA rostlin MeSH
Phospholipases (PLs) are lipid-hydrolyzing enzymes known to have diverse signaling roles during plant abiotic and biotic stress responses. They catalyze lipid remodeling, which is required to generate rapid responses of plants to environmental cues. Moreover, they produce second messenger molecules, such as phosphatidic acid (PA) and thus trigger or modulate signaling cascades that lead to changes in gene expression. The roles of phospholipases in plant abiotic and biotic stress responses have been intensively studied. Nevertheless, emerging evidence suggests that they also make significant contributions to plants' cellular and developmental processes. In this mini review, we summarized recent advances in the study of the cellular and developmental roles of phospholipases in plants.
- Klíčová slova
- cellular functions, phosphatidic acid, phospholipase A, phospholipase C, phospholipase D, phospholipases, phytohormones, plant development,
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
Phytohormone salicylic acid (SA) is a crucial component of plant-induced defense against biotrophic pathogens. Although the key players of the SA pathway are known, there are still gaps in the understanding of the molecular mechanism and the regulation of particular steps. In our previous research, we showed in Arabidopsis suspension cells that n-butanol, which specifically modulates phospholipase D activity, significantly suppresses the transcription of the pathogenesis related (PR-1) gene, which is generally accepted as the SA pathway marker. In the presented study, we have investigated the site of n-butanol action in the SA pathway. We were able to show in Arabidopsis plants treated with SA that n-butanol inhibits the transcription of defense genes (PR-1, WRKY38). Fluorescence microscopy of Arabidopsis thaliana mutants expressing 35S::NPR1-GFP (nonexpressor pathogenesis related 1) revealed significantly decreased nuclear localization of NPR1 in the presence of n-butanol. On the other hand, n-butanol did not decrease the nuclear localization of NPR1 in 35S::npr1C82A-GFP and 35S::npr1C216A-GFP mutants constitutively expressing NPR1 monomers. Mass spectrometric analysis of plant extracts showed that n-butanol significantly changes the metabolic fingerprinting while t-butanol had no effect. We found groups of the plant metabolites, influenced differently by SA and n-butanol treatment. Thus, we proposed several metabolites as markers for n-butanol action.
- Klíčová slova
- NPR1, PR-1, metabolome, n-butanol, phospholipase D, salicylic acid, signaling,
- Publikační typ
- časopisecké články MeSH
Aluminum ions (Al) have been recognized as a major toxic factor for crop production in acidic soils. The first indication of the Al toxicity in plants is the cessation of root growth, but the mechanism of root growth inhibition is largely unknown. Here we examined the impact of Al on the expression, activity, and function of the non-specific phospholipase C4 (NPC4), a plasma membrane-bound isoform of NPC, a member of the plant phospholipase family, in Arabidopsis thaliana. We observed a lower expression of NPC4 using β-glucuronidase assay and a decreased formation of labeled diacylglycerol, product of NPC activity, using fluorescently labeled phosphatidylcholine as a phospholipase substrate in Arabidopsis WT seedlings treated with AlCl3 for 2 h. The effect on in situ NPC activity persisted for longer Al treatment periods (8, 14 h). Interestingly, in seedlings overexpressing NPC4, the Al-mediated NPC-inhibiting effect was alleviated at 14 h. However, in vitro activity and localization of NPC4 were not affected by Al, thus excluding direct inhibition by Al ions or possible translocation of NPC4 as the mechanisms involved in NPC-inhibiting effect. Furthermore, the growth of tobacco pollen tubes rapidly arrested by Al was partially rescued by the overexpression of AtNPC4 while Arabidopsis npc4 knockout lines were found to be more sensitive to Al stress during long-term exposure of Al at low phosphate conditions. Our observations suggest that NPC4 plays a role in both early and long-term responses to Al stress.
- Klíčová slova
- Arabidopsis, aluminum toxicity, diacylglycerol, non-specific phospholipase C, plasma membrane, pollen tube, signaling, tobacco,
- Publikační typ
- časopisecké články MeSH
The actin cytoskeleton plays a key role in the plant morphogenesis and is involved in polar cell growth, movement of subcellular organelles, cell division, and plant defense. Organization of actin cytoskeleton undergoes dynamic remodeling in response to internal developmental cues and diverse environmental signals. This dynamic behavior is regulated by numerous actin-binding proteins (ABPs) that integrate various signaling pathways. Production of the signaling lipids phosphatidylinositol 4,5-bisphosphate and phosphatidic acid affects the activity and subcellular distribution of several ABPs, and typically correlates with increased actin polymerization. Here we review current knowledge of the inter-regulatory dynamics between signaling phospholipids and the actin cytoskeleton in plant cells.
- Klíčová slova
- actin, actin-binding proteins, capping protein, cytoskeleton, phosphatidic acid, phosphatidylinositol 4,5-bisphosphate, phospholipase D, signaling,
- Publikační typ
- časopisecké články MeSH
- přehledy 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
- Názvy látek
- fosfolipasy MeSH
- fosfotransferasy MeSH
- glycerofosfolipidy MeSH
- kyselina abscisová MeSH
- kyseliny fosfatidové MeSH
- regulátory růstu rostlin MeSH
- rostlinné proteiny MeSH
UNLABELLED: Invasive cell growth and migration is usually considered a specifically metazoan phenomenon. However, common features and mechanisms of cytoskeletal rearrangements, membrane trafficking and signalling processes contribute to cellular invasiveness in organisms as diverse as metazoans and plants - two eukaryotic realms genealogically connected only through the last common eukaryotic ancestor (LECA). By comparing current understanding of cell invasiveness in model cell types of both metazoan and plant origin (invadopodia of transformed metazoan cells, neurites, pollen tubes and root hairs), we document that invasive cell behavior in both lineages depends on similar mechanisms. While some superficially analogous processes may have arisen independently by convergent evolution (e.g. secretion of substrate- or tissue-macerating enzymes by both animal and plant cells), at the heart of cell invasion is an evolutionarily conserved machinery of cellular polarization and oriented cell mobilization, involving the actin cytoskeleton and the secretory pathway. Its central components - small GTPases (in particular RHO, but also ARF and Rab), their specialized effectors, actin and associated proteins, the exocyst complex essential for polarized secretion, or components of the phospholipid- and redox- based signalling circuits (inositol-phospholipid kinases/PIP2, NADPH oxidases) are aparently homologous among plants and metazoans, indicating that they were present already in LECA. REVIEWER: This article was reviewed by Arcady Mushegian, Valerian Dolja and Purificacion Lopez-Garcia.
- MeSH
- aktiny metabolismus MeSH
- cytoskelet metabolismus MeSH
- lidé MeSH
- pohyb buněk fyziologie MeSH
- pylová láčka cytologie metabolismus MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
- Názvy látek
- aktiny MeSH