Endocytic Trafficking Promotes Vacuolar Enlargements for Fast Cell Expansion Rates in Plants

The vacuole has a space-filling function, allowing a particularly rapid plant cell expansion with very little increase in cytosolic content (Loefke et al., 2015; Scheuring et al., 2016; Duenser et al., 2019). Despite its importance for cell size determination in plants, very little is known about the mechanisms that define vacuolar size. Here we show that the cellular and vacuolar size expansions are coordinated. By developing a pharmacological tool, we enabled the investigation of membrane delivery to the vacuole during cellular expansion. Counterintuitively, our data reveal that endocytic trafficking from the plasma membrane to the vacuole is enhanced in the course of rapid root cell expansion. While this "compromise" mechanism may theoretically at first decelerate cell surface enlargements, it fuels vacuolar expansion and, thereby, ensures the coordinated augmentation of vacuolar occupancy in dynamically expanding plant cells.

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Spatial differences in stoichiometry of EGR phosphatase and Microtubule-Associated Stress Protein 1 control root meristem activity during drought stress.

10.1101/2021.10.06.463370 ◽

2021 ◽

Author(s):

Toshisagba Longkumer ◽

Chih-Yun Chen ◽

Marco Biancucci ◽

Bhaskara Govinal Badiger ◽

Paul E. Verslues

Keyword(s):

Cell Division ◽

Cell Size ◽

Cell Expansion ◽

Growth Regulation ◽

Root Meristem ◽

Stress Protein ◽

Root Cell ◽

Root Cortex ◽

Meristem Cell ◽

Meristem Size

During moderate severity drought and low water potential (Ψw) stress, poorly understood signaling mechanisms restrict both meristem cell division and subsequent cell expansion. We found that the Clade E Growth-Regulating 2 (EGR2) protein phosphatase and Microtubule Associated Stress Protein 1 (MASP1) differed in their stoichiometry of expression across the root meristem and had opposing effects on root meristem activity at low Ψw. Ectopic MASP1 or EGR expression increased or decreased, respectively, root meristem size and root elongation during low Ψw stress. This, along with the ability of phosphomimic MASP1 to overcome EGR suppression of root meristem size and observation that ectopic EGR expression had no effect on unstressed plants, indicated that during low Ψw EGR activation and attenuation of MASP1 phosphorylation in their overlapping zone of expression determines root meristem size and activity. Ectopic EGR expression also decreased root cell size at low Ψw. Conversely, both the egr1-1egr2-1 and egr1-1egr2-1masp1-1 mutants had similarly increased root cell size; but, only egr1-1egr2-1 had increased cell division. These observations demonstrated that EGRs affect meristem activity via MASP1 but affect cell expansion via other mechanisms. Interestingly, EGR2 was highly expressed in the root cortex, a cell type important for growth regulation and environmental response.

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Regulation of caveolin-1 membrane trafficking by the Na/K-ATPase

The Journal of Cell Biology ◽

10.1083/jcb.200712022 ◽

2008 ◽

Vol 182 (6) ◽

pp. 1153-1169 ◽

Cited By ~ 83

Author(s):

Ting Cai ◽

Haojie Wang ◽

Yiliang Chen ◽

Lijun Liu ◽

William T Gunning ◽

...

Keyword(s):

Plasma Membrane ◽

Cell Surface ◽

Long Range ◽

Membrane Trafficking ◽

Endocytic Trafficking ◽

Binding Motif ◽

Caveolin 1 ◽

Pumping Function ◽

Α1 Subunit

Here, we show that the Na/K-ATPase interacts with caveolin-1 (Cav1) and regulates Cav1 trafficking. Graded knockdown of Na/K-ATPase decreases the plasma membrane pool of Cav1, which results in a significant reduction in the number of caveolae on the cell surface. These effects are independent of the pumping function of Na/K-ATPase, and instead depend on interaction between Na/K-ATPase and Cav1 mediated by an N-terminal caveolin-binding motif within the ATPase α1 subunit. Moreover, knockdown of the Na/K-ATPase increases basal levels of active Src and stimulates endocytosis of Cav1 from the plasma membrane. Microtubule-dependent long-range directional trafficking in Na/K-ATPase–depleted cells results in perinuclear accumulation of Cav1-positive vesicles. Finally, Na/K-ATPase knockdown has no effect on processing or exit of Cav1 from the Golgi. Thus, the Na/K-ATPase regulates Cav1 endocytic trafficking and stabilizes the Cav1 plasma membrane pool.

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

10.21203/rs.3.rs-203621/v1 ◽

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.

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Regulation by Gibberellins of the Orientation of Cortical Microtubules in Plant Cells

Functional Plant Biology ◽

10.1071/pp9930461 ◽

1993 ◽

Vol 20 (5) ◽

pp. 461 ◽

Cited By ~ 20

Author(s):

H Shibaoka

Keyword(s):

Plasma Membrane ◽

Cell Expansion ◽

Plant Cells ◽

Cellulose Microfibrils ◽

Molecular Architecture ◽

Cortical Microtubules ◽

Microtubule Stability ◽

The Stability ◽

The Way

Gibberellins control the direction of expansion of plant cells. They change the orientation of cellulose microfibrils by changing the orientation of cortical microtubules and, hence, the direction of cell expansion. When gibberellins change the orientation of cortical microtubules, they also change their stability. If the way in which gibberellins change the orientation of microtubules is identical to the way in which they change microtubule stability, then studies on the mechanism that regulates this stability should give us some clues to the mechanism that regulates the orientation of microtubules. With this possibility in mind, we undertook a series of studies on the stability of cortical microtubules. These revealed that the association of cortical microtubules with the plasma membrane is an important part of the mechanism for their stabilisation. Gibberellins seem to change the stability of microtubules by affecting their association with the plasma membrane. To study the way in which the gibberellins affect this association, it is necessary to clarify the molecular architecture of the structure that links cortical microtubules with the plasma membrane.

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an3-Mediated Compensation Is Dependent on a Cell-Autonomous Mechanism in Leaf Epidermal Tissue

Plant and Cell Physiology ◽

10.1093/pcp/pcaa048 ◽

2020 ◽

Vol 61 (6) ◽

pp. 1181-1190

Author(s):

Mamoru Nozaki ◽

Kensuke Kawade ◽

Gorou Horiguchi ◽

Hirokazu Tsukaya

Keyword(s):

Cell Proliferation ◽

Cell Size ◽

Leaf Development ◽

Cell Expansion ◽

Size Determination ◽

Wild Type ◽

Specific Expression ◽

Autonomous Action ◽

Epidermal Tissue ◽

A Cell

Abstract Leaves are formed by coordinated growth of tissue layers driven by cell proliferation and expansion. Compensation, in which a defect in cell proliferation induces compensated cell enlargement (CCE), plays an important role in cell-size determination during leaf development. We previously reported that CCE triggered by the an3 mutation is observed in epidermal and subepidermal layers in Arabidopsis thaliana (Arabidopsis) leaves. Interestingly, CCE is induced in a non-cell autonomous manner between subepidermal cells. However, whether CCE in the subepidermis affects cell size in the adjacent epidermis is still unclear. We induced layer-specific expression of AN3 in an3 leaves and found that CCE in the subepidermis had little impact on cell-size determination in the epidermis, and vice versa, suggesting that CCE is induced in a tissue-autonomous manner. Examination of the epidermis in an3 leaves having AN3-positive and -negative sectors generated by Cre/loxP revealed that, in contrast to the subepidermis, CCE occurred exclusively in AN3-negative epidermal cells, indicating a cell autonomous action of an3-mediated compensation in the epidermis. These results clarified that the epidermal and subepidermal tissue layers have different cell autonomies in CCE. In addition, quantification of cell-expansion kinetics in epidermal and subepidermal tissues of the an3 showed that the tissues exhibited a similar temporal profile to reach a peak cell-expansion rate as compared to wild type. This might be one feature representing that the two tissue layers retain their growth coordination even in the presence of CCE.

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

10.1101/231043 ◽

2017 ◽

Cited By ~ 3

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.

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

Nature ◽

10.1038/s41586-021-03976-4 ◽

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.

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