scholarly journals TMK-based cell-surface auxin signalling activates cell-wall acidification

Nature ◽  
2021 ◽  
Author(s):  
Wenwei Lin ◽  
Xiang Zhou ◽  
Wenxin Tang ◽  
Koji Takahashi ◽  
Xue Pan ◽  
...  
Keyword(s):  
Cell Wall ◽  
Plasma Membrane ◽  
Cell Surface ◽  
Cell Expansion ◽  
Molecular Evidence ◽  
Acid Growth ◽  
Threonine Residue ◽  
Auxin Signalling ◽  
Cell Wall Acidification ◽  
Growth Hypothesis

AbstractThe phytohormone auxin controls many processes in plants, at least in part through its regulation of cell expansion1. The acid growth hypothesis has been proposed to explain auxin-stimulated cell expansion for five decades, but the mechanism that underlies auxin-induced cell-wall acidification is poorly characterized. Auxin induces the phosphorylation and activation of the plasma membrane H+-ATPase that pumps protons into the apoplast2, yet how auxin activates its phosphorylation remains unclear. Here we show that the transmembrane kinase (TMK) auxin-signalling proteins interact with plasma membrane H+-ATPases, inducing their phosphorylation, and thereby promoting cell-wall acidification and hypocotyl cell elongation in Arabidopsis. Auxin induced interactions between TMKs and H+-ATPases in the plasma membrane within seconds, as well as TMK-dependent phosphorylation of the penultimate threonine residue on the H+-ATPases. Our genetic, biochemical and molecular evidence demonstrates that TMKs directly phosphorylate plasma membrane H+-ATPase and are required for auxin-induced H+-ATPase activation, apoplastic acidification and cell expansion. Thus, our findings reveal a crucial connection between auxin and plasma membrane H+-ATPase activation in regulating apoplastic pH changes and cell expansion through TMK-based cell surface auxin signalling.

scholarly journals TMK-based cell surface auxin signaling activates cell wall acidification in Arabidopsis

2021 ◽  
Author(s):  
Zhenbiao Yang ◽  
Wenwei Lin ◽  
Wenxin Tang ◽  
Koji Takahashi ◽  
Hong Ren ◽  
...  
Keyword(s):  
Cell Wall ◽  
Plasma Membrane ◽  
Cell Surface ◽  
Cell Expansion ◽  
Auxin Signaling ◽  
Molecular Evidence ◽  
Signaling Proteins ◽  
Acid Growth ◽  
Cell Wall Acidification ◽  
Growth Hypothesis

Abstract The phytohormone auxin controls a myriad of processes in plants, at least in part through its regulation of cell expansion. The "acid growth hypothesis" has been proposed to explain auxin-stimulated cell expansion for five decades, but the mechanism underlying auxin-induced cell wall acidification is poorly characterized. Auxin induces the phosphorylation and activation of the plasma membrane (PM) H+-ATPase that pumps protons into the apoplast, yet how auxin activates its phosphorylation remains elusive. Here, we show that the transmembrane kinase (TMK) auxin signaling proteins interact with PM H+-ATPases and activate their phosphorylation to promote cell wall acidification and hypocotyl cell elongation in Arabidopsis. Auxin induced TMK's interaction with H+-ATPase on the plasma membrane within 1-2 minutes as well as TMK-dependent phosphorylation of the penultimate Thr residue. Genetic, biochemical, and molecular evidence demonstrates that TMKs are required for auxin-induced PM H+-ATPase activation, apoplastic acidification, and cell expansion. Thus, our findings reveal a crucial connection between auxin and PM H+-ATPase activation in regulating apoplastic pH changes and cell expansion via TMK-based cell surface auxin signaling.

scholarly journals LRX- and FER-dependent extracellular sensing coordinates vacuolar size for cytosol homeostasis

2017 ◽  
Author(s):  
Kai Dünser ◽  
Shibu Gupta ◽  
Christoph Ringli ◽  
Jürgen Kleine-Vehn
Keyword(s):  
Cell Wall ◽  
Plasma Membrane ◽  
Plant Cell ◽  
Cell Expansion ◽  
Leucine Rich Repeat ◽  
Sensing Mechanism ◽  
Extracellular Signals ◽  
Receptor Like Kinase ◽  
Cell Wall Acidification

Cellular elongation requires the defined coordination of intra- and extracellular processes. The vacuole is the biggest plant organelle and its dimension has a role in limiting cell expansion (Löfke et al., 2015; Scheuring et al., 2016). We reveal that the increase in vacuolar occupancy enables cellular elongation with relatively little enlargement of the cytosole. It remains, however, completely unknown how the vacuolar size is coordinated with other growth-relevant processes. Intriguingly, we show that extracellular constraints impact on the intracellular expansion of the vacuole. The underlying cell wall sensing mechanism requires the interaction of the extracellular leucine-rich repeat extensin (LRX) with the receptor-like kinase Feronia (FER). Our data suggests that LRX links the plasma membrane localised FER with the cell wall, allowing this module to jointly sense and convey extracellular signals to the underlying cell. This mechanism coordinates cell wall acidification/loosening with the increase in vacuolar size, contributing cytosol homeostasis during plant cell expansion.

scholarly journals FERONIA regulates FLS2 plasma membrane nanoscale dynamics to modulate plant immune signaling

2020 ◽  
Author(s):  
Julien Gronnier ◽  
Christina M. Franck ◽  
Martin Stegmann ◽  
Thomas A. DeFalco ◽  
Alicia Abarca Cifuentes ◽  
...  
Keyword(s):  
Cell Wall ◽  
Plasma Membrane ◽  
Complex Formation ◽  
Cell Surface ◽  
Single Particle Tracking ◽  
Receptor Kinase ◽  
Leucine Rich Repeat ◽  
Immune Signaling ◽  
Receptor Complexes ◽  
Nanoscale Dynamics

ABSTRACTCell surface receptors survey and relay information to ensure the development and survival of multicellular organisms. In the model plant Arabidopsis thaliana, the Catharanthus roseus RLK1-like receptor kinase FERONIA (FER) regulates myriad of biological processes to coordinate development, growth and responses to the environment. We recently showed that FER positively regulates immune signaling by controlling the ligand-induced complex formation between the leucine-rich repeat receptor kinase (LRR-RK) FLAGELLIN SENSING 2 (FLS2) and its co-receptor BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED KINASE 1/SOMATIC EMBRYOGENESIS RECEPTOR KINASE 3 (BAK1/SERK3). In this context, FER function is inhibited by binding of its peptide ligand RAPID ALKALINIZATION FACTOR 23 (RALF23). However, the mechanisms by which FER regulates FLS2-BAK1 complex formation remain unclear. Here, we show that FER-dependent regulation of immune signaling is independent of its kinase activity, indicating that FER rather plays a structural role. FER has been proposed to bind directly to the plant cell wall, but we found that a FER mutant unable to bind pectin is still functional in regulating immune signaling. Instead, FER- and cell wall-associated LEUCINE RICH REPEAT-EXTENSIN proteins are required for this regulation. Using high-resolution live-imaging and single-particle tracking, we observed that FER regulates FLS2 plasma membrane nanoscale dynamics, which may explain its role in controlling ligand-induced FLS2-BAK1 association. We propose that FER acts as an anchoring point connecting cell wall and plasma membrane nano-environments to enable the nucleation of pre-formed receptor/co-receptor complexes at the cell surface.

scholarly journals TIR1/AFB-Aux/IAA auxin perception mediates rapid cell wall acidification and growth of Arabidopsis hypocotyls

eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Matyáš Fendrych ◽  
Jeffrey Leung ◽  
Jiří Friml
Keyword(s):  
Cell Wall ◽  
Gene Transcription ◽  
Growth Theory ◽  
Auxin Signaling ◽  
Differential Growth ◽  
Acid Growth ◽  
Genetic Manipulations ◽  
Gravity Response ◽  
Acid Growth Theory ◽  
Cell Wall Acidification

Despite being composed of immobile cells, plants reorient along directional stimuli. The hormone auxin is redistributed in stimulated organs leading to differential growth and bending. Auxin application triggers rapid cell wall acidification and elongation of aerial organs of plants, but the molecular players mediating these effects are still controversial. Here we use genetically-encoded pH and auxin signaling sensors, pharmacological and genetic manipulations available for Arabidopsis etiolated hypocotyls to clarify how auxin is perceived and the downstream growth executed. We show that auxin-induced acidification occurs by local activation of H+-ATPases, which in the context of gravity response is restricted to the lower organ side. This auxin-stimulated acidification and growth require TIR1/AFB-Aux/IAA nuclear auxin perception. In addition, auxin-induced gene transcription and specifically SAUR proteins are crucial downstream mediators of this growth. Our study provides strong experimental support for the acid growth theory and clarified the contribution of the upstream auxin perception mechanisms.

scholarly journals A pathway for cell wall anchorage of Saccharomyces cerevisiae alpha-agglutinin.

1994 ◽  
Vol 14 (7) ◽  
pp. 4825-4833 ◽  
Author(s):  
C F Lu ◽  
J Kurjan ◽  
P N Lipke
Keyword(s):  
Saccharomyces Cerevisiae ◽  
Cell Wall ◽  
Plasma Membrane ◽  
Cell Surface ◽  
Soluble Form ◽  
Gpi Anchor ◽  
Glycosyl Phosphatidylinositol ◽  
Experimental Support ◽  
Cell Biol ◽  
A Cell

Saccharomyces cerevisiae alpha-agglutinin is a cell wall-anchored adhesion glycoprotein. The previously identified 140-kDa form, which contains a glycosyl-phosphatidylinositol (GPI) anchor (D. Wojciechowicz, C.-F. Lu, J. Kurjan, and P. N. Lipke, Mol. Cell. Biol. 13:2554-2563, 1993), and additional forms of 80, 150, 250 to 300, and > 300 kDa had the properties of intermediates in a transport and cell wall anchorage pathway. N glycosylation and additional modifications resulted in successive increases in size during transport. The 150- and 250- to 300-kDa forms were membrane associated and are likely to be intermediates between the 140-kDa form and a cell surface GPI-anchored form of > 300 kDa. A soluble form of > 300 kDa that lacked the GPI anchor had properties of a periplasmic intermediate between the plasma membrane form and the > 300-kDa cell wall-anchored form. These results constitute experimental support for the hypothesis that GPI anchors act to localize alpha-agglutinin to the plasma membrane and that cell wall anchorage involves release from the GPI anchor to produce a periplasmic intermediate followed by linkage to the cell wall.

scholarly journals Cellulose synthase complexes display distinct dynamic behaviors during xylem transdifferentiation

2018 ◽  
Vol 115 (27) ◽  
pp. E6366-E6374 ◽  
Author(s):  
Yoichiro Watanabe ◽  
Rene Schneider ◽  
Sarah Barkwill ◽  
Eliana Gonzales-Vigil ◽  
Joseph L. Hill ◽  
...  
Keyword(s):  
Cell Wall ◽  
Plasma Membrane ◽  
Cell Expansion ◽  
Secondary Wall ◽  
Transition Period ◽  
Cellulose Synthase ◽  
Wall Thickening ◽  
Cellulose Synthesis ◽  
Primary Wall ◽  
Dynamic Behaviors

In plants, plasma membrane-embedded CELLULOSE SYNTHASE (CESA) enzyme complexes deposit cellulose polymers into the developing cell wall. Cellulose synthesis requires two different sets of CESA complexes that are active during cell expansion and secondary cell wall thickening, respectively. Hence, developing xylem cells, which first undergo cell expansion and subsequently deposit thick secondary walls, need to completely reorganize their CESA complexes from primary wall- to secondary wall-specific CESAs. Using live-cell imaging, we analyzed the principles underlying this remodeling. At the onset of secondary wall synthesis, the primary wall CESAs ceased to be delivered to the plasma membrane and were gradually removed from both the plasma membrane and the Golgi. For a brief transition period, both primary wall- and secondary wall-specific CESAs coexisted in banded domains of the plasma membrane where secondary wall synthesis is concentrated. During this transition, primary and secondary wall CESAs displayed discrete dynamic behaviors and sensitivities to the inhibitor isoxaben. As secondary wall-specific CESAs were delivered and inserted into the plasma membrane, the primary wall CESAs became concentrated in prevacuolar compartments and lytic vacuoles. This adjustment in localization between the two CESAs was accompanied by concurrent decreased primary wall CESA and increased secondary wall CESA protein abundance. Our data reveal distinct and dynamic subcellular trafficking patterns that underpin the remodeling of the cellulose biosynthetic machinery, resulting in the removal and degradation of the primary wall CESA complex with concurrent production and recycling of the secondary wall CESAs.

scholarly journals Auxin steers root cell expansion via apoplastic pH regulation in Arabidopsis thaliana

2017 ◽  
Vol 114 (24) ◽  
pp. E4884-E4893 ◽  
Author(s):  
Elke Barbez ◽  
Kai Dünser ◽  
Angelika Gaidora ◽  
Thomas Lendl ◽  
Wolfgang Busch
Keyword(s):  
Arabidopsis Thaliana ◽  
Cell Wall ◽  
Cell Expansion ◽  
Ph Regulation ◽  
Root Cell ◽  
Auxin Signaling ◽  
Acid Growth ◽  
Gravitropic Response ◽  
Apoplastic Ph ◽  
Cellular Resolution

Plant cells are embedded within cell walls, which provide structural integrity, but also spatially constrain cells, and must therefore be modified to allow cellular expansion. The long-standing acid growth theory postulates that auxin triggers apoplast acidification, thereby activating cell wall-loosening enzymes that enable cell expansion in shoots. Interestingly, this model remains heavily debated in roots, because of both the complex role of auxin in plant development as well as technical limitations in investigating apoplastic pH at cellular resolution. Here, we introduce 8-hydroxypyrene-1,3,6-trisulfonic acid trisodium salt (HPTS) as a suitable fluorescent pH indicator for assessing apoplastic pH, and thus acid growth, at a cellular resolution in Arabidopsis thaliana roots. Using HPTS, we demonstrate that cell wall acidification triggers cellular expansion, which is correlated with a preceding increase of auxin signaling. Reduction in auxin levels, perception, or signaling abolishes both the extracellular acidification and cellular expansion. These findings jointly suggest that endogenous auxin controls apoplastic acidification and the onset of cellular elongation in roots. In contrast, an endogenous or exogenous increase in auxin levels induces a transient alkalinization of the extracellular matrix, reducing cellular elongation. The receptor-like kinase FERONIA is required for this physiological process, which affects cellular root expansion during the gravitropic response. These findings pinpoint a complex, presumably concentration-dependent role for auxin in apoplastic pH regulation, steering the rate of root cell expansion and gravitropic response.

scholarly journals Antagonistic cell surface and intracellular auxin signalling regulate plasma membrane H -fluxes for root growth

2021 ◽  
Author(s):  
Lanxin Li ◽  
Inge Verstraeten ◽  
Mark Roosjen ◽  
Koji Takahashi ◽  
Lesia Rodriguez ◽  
...  
Keyword(s):  
Plasma Membrane ◽  
Cell Surface ◽  
Root Growth ◽  
Growth Regulation ◽  
Growth Modulation ◽  
Auxin Signalling ◽  
Direct Growth ◽  
Simultaneous Activation ◽  
Growth Adaptation ◽  
Apoplast Acidification

Abstract Growth regulation tailors plant development to its environment. A showcase is growth adaptation to gravity, where shoots bend up and roots down. This paradox is based on different responses to the phytohormone auxin, which promotes cell expansion in shoots, while inhibiting it in roots via a yet unknown cellular mechanism. Here, by combining microfluidics, live imaging, genetic engineering and phospho-proteomics in Arabidopsis thaliana, we reveal how auxin inhibits root growth. We show that auxin activates two distinct, antagonistically acting signalling pathways that converge on the rapid regulation of the apoplastic pH, which is the direct growth-determining mechanism. Cell surface-based TRANSMEMBRANE KINASE 1 (TMK1) interacts with and mediates phosphorylation and activation of plasma membrane H+-ATPases for apoplast acidification, while intracellular TIR1/AFB-mediated signalling triggers net cellular H+-influx, causing apoplast alkalinisation. The simultaneous activation of these two counteracting mechanisms poises the root for a rapid, fine-tuned growth modulation to subtle changes in the environment.

scholarly journals Rapid Auxin-Mediated Cell Expansion

2020 ◽  
Vol 71 (1) ◽  
pp. 379-402 ◽  
Author(s):  
Minmin Du ◽  
Edgar P. Spalding ◽  
William M. Gray
Keyword(s):  
Plasma Membrane ◽  
Cell Expansion ◽  
Plant Hormone ◽  
Molecular Level ◽  
Good News ◽  
Growth Theory ◽  
Acid Growth ◽  
Promotive Effect ◽  
Acid Growth Theory ◽  
Regulate Protein

The promotive effect of auxin on shoot cell expansion provided the bioassay used to isolate this central plant hormone nearly a century ago. While the mechanisms underlying auxin perception and signaling to regulate transcription have largely been elucidated, how auxin controls cell expansion is only now attaining molecular-level definition. The good news is that the decades-old acid growth theory invoking plasma membrane H+-ATPase activation is still useful. The better news is that a mechanistic framework has emerged, wherein Small Auxin Up RNA (SAUR) proteins regulate protein phosphatases to control H+-ATPase activity. In this review, we focus on rapid auxin effects, their relationship to H+-ATPase activation and other transporters, and dependence on TIR1/AFB signaling. We also discuss how some observations, such as near-instantaneous effects on ion transport and root growth, do not fit into a single, comprehensive explanation of how auxin controls cell expansion, and where more research is warranted.

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