Many signaling proteins permanently or transiently localize to specific organelles for function. It is well established that certain lipids act as biochemical landmarks to specify compartment identity. However, they also influence membrane biophysical properties, which emerge as important features in specifying cellular territories. Such parameters include the membrane inner surface potential, which varies according to the lipid composition of each organelle. Here, we found that the plant plasma membrane (PM) and the cell plate of dividing cells have a unique electrostatic signature controlled by phosphatidylinositol-4-phosphate (PI4P). Our results further reveal that, contrarily to other eukaryotes, PI4P massively accumulates at the PM, establishing it as a critical hallmark of this membrane in plants. Membrane surface charges control the PM localization and function of the polar auxin transport regulator PINOID, as well as proteins from the BRI1 KINASE INHIBITOR1 (BKI1)/MEMBRANE ASSOCIATED KINASE REGULATORs (MAKRs) family, which are involved in brassinosteroid and receptor-like kinase signaling. We anticipate that this PI4P-driven physical membrane property will control the localization and function of many proteins involved in development, reproduction, immunity and nutrition.
Rho guanosine triphosphatases (GTPases) are master regulators of cell signaling, but how they are regulated depending on the cellular context is unclear. We found that the phospholipid phosphatidylserine acts as a developmentally controlled lipid rheostat that tunes Rho GTPase signaling in Arabidopsis. Live superresolution single-molecule imaging revealed that the protein Rho of Plants 6 (ROP6) is stabilized by phosphatidylserine into plasma membrane nanodomains, which are required for auxin signaling. Our experiments also revealed that the plasma membrane phosphatidylserine content varies during plant root development and that the level of phosphatidylserine modulates the quantity of ROP6 nanoclusters induced by auxin and hence downstream signaling, including regulation of endocytosis and gravitropism. Our work shows that variations in phosphatidylserine levels are a physiological process that may be leveraged to regulate small GTPase signaling during development.
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.
The directional transport of auxin, known as polar auxin transport (PAT), allows asymmetric distribution of this hormone in different cells and tissues. This system creates local auxin maxima, minima, and gradients that are instrumental in both organ initiation and shape determination. As such, PAT is crucial for all aspects of plant development but also for environmental interaction, notably in shaping plant architecture to its environment. Cell to cell auxin transport is mediated by a network of auxin carriers that are regulated at the transcriptional and post-translational levels. Here we review our current knowledge on some aspects of the 'non-genomic' regulation of auxin transport, placing an emphasis on how phosphorylation by protein and lipid kinases controls the polarity, intracellular trafficking, stability, and activity of auxin carriers. We describe the role of several AGC kinases, including PINOID, D6PK, and the blue light photoreceptor phot1, in phosphorylating auxin carriers from the PIN and ABCB families. We also highlight the function of some receptor-like kinases (RLKs) and two-component histidine kinase receptors in PAT, noting that there are probably RLKs involved in co-ordinating auxin distribution yet to be discovered. In addition, we describe the emerging role of phospholipid phosphorylation in polarity establishment and intracellular trafficking of PIN proteins. We outline these various phosphorylation mechanisms in the context of primary and lateral root development, leaf cell shape acquisition, as well as root gravitropism and shoot phototropism.
21Membrane surface charge is critical for the transient, yet specific recruitment of proteins with polybasic 22 regions to certain organelles. In all eukaryotes, the plasma membrane (PM) is the most electronegative 23 compartment of the cell, which specifies its identity. As such, membrane electrostatics is a central parameter 24 in signaling, intracellular trafficking and polarity. Here, we explore which are the lipids that control membrane 25 electrostatics using plants as a model. We show that phosphatidic acidic (PA), phosphatidylserine (PS) and 26 phosphatidylinositol-4-phosphate (PI4P) are separately required to generate the electrostatic signature of the 27 plant PM. In addition, we reveal the existence of an electrostatic territory that is organized as a gradient along 28 the endocytic pathway and is controlled by PS/PI4P combination. Altogether, we propose that combinatorial 29 lipid composition of the cytosolic leaflet of cellular organelles not only defines the plant electrostatic territory 30 but also distinguishes different compartments within this territory by specifying their varying surface charges.
SUMMARYWe have previously reported that CK2-defective Arabidopsis thaliana plants (CK2mut plants) were impaired severely in root development and auxin polar transport, and exhibited transcriptional misregulation of auxin-efflux transporters (Plant J., 67, 2011a, 169). In this work we show that CK2mut roots accumulate high levels of salicylic acid (SA) and that the gene that encodes isochorismate synthase (SID2) is overexpressed, strongly suggesting that CK2 activity is required for SA biosynthesis via the shikimate pathway. Moreover, SA activates transcription of CK2-encoding genes and, thus, SA and CK2 appear to be part of an autoregulatory feed-back loop to fine-tune each other's activities. We also show that exogenous SA and constitutive high SA levels in cpr mutants reproduce the CK2mut root phenotypes (decrease of root length and of number of lateral roots), whereas inhibition of CK2 activity in SA-defective and SA-signalling mutants lead to less severe phenotypes, suggesting that the CK2mut root phenotypes are SA-mediated effects. Moreover, exogenous SA mediates transcriptional repression of most of PIN-FORMED (PIN) genes, which is the opposite effect observed in CK2mut roots. These results prompted us to propose a model in which CK2 acts as a link between SA homeostasis and transcriptional regulation of auxin-efflux transporters. We also show that CK2 overexpression in Arabidopsis has neither impact on SA biosynthesis nor on auxin transport, but it improves the Arabidopsis root system. Thus, unlike the outcome in mammals, an excess of CK2 in plant cells does not produce neoplasia, but it might be advantageous for plant fitness.
Highlights d MAKR2 is co-expressed with PIN2 and regulates the pace of root gravitropism d MAKR2 controls PIN2 asymmetric accumulation at the root level during gravitropism d MAKR2 binds to and is a negative regulator of the TMK1 receptor kinase d Auxin antagonizes the MAKR2 inhibition of TMK1 by delocalizing MAKR2 in the cytosol
Membrane lipids, and especially phosphoinositides, are differentially enriched within the eukaryotic endomembrane system. This generates a landmark code by modulating the properties of each membrane. Phosphatidylinositol 4,5-bisphosphate [PI(4,5)P2] specifically accumulates at the plasma membrane in yeast, animal, and plant cells, where it regulates a wide range of cellular processes including endocytic trafficking. However, the functional consequences of mispatterning PI(4,5)P2 in plants are unknown. Here, we functionally characterized the putative phosphoinositide phosphatase SUPPRESSOR OF ACTIN9 (SAC9) in Arabidopsis thaliana (Arabidopsis). We found that SAC9 depletion led to the ectopic localization of PI(4,5)P2 on cortical intracellular compartments, which depends on PI4P and PI(4,5)P2 production at the plasma membrane. SAC9 localizes to a subpopulation of trans-Golgi Network/early endosomes that are enriched in a region close to the cell cortex and that are coated with clathrin. Furthermore, it interacts and colocalizes with Src Homology 3 Domain Protein 2 (SH3P2), a protein involved in endocytic trafficking. In the absence of SAC9, SH3P2 localization is altered and the clathrin-mediated endocytosis rate is reduced. Together, our results highlight the importance of restricting PI(4,5)P2 at the plasma membrane and illustrate that one of the consequences of PI(4,5)P2 misspatterning in plants is to impact the endocytic trafficking.
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