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Mechanical Signaling in Plants
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Mechanical Signaling in Plants

A special issue of Plants (ISSN 2223-7747).

Deadline for manuscript submissions: closed (15 November 2020) | Viewed by 82562

Special Issue Editor

Prof. Dr. Hidetoshi Iida

E-Mail Website
Guest Editor
Department of Biology, Tokyo Gakugei University, Nukuikita-machi, Koganei-shi, Tokyo 184-8501, Japan
Interests: Mechanosensitive channels; Mechanosensing mechanism; Calcium channels; Calcium signaling; Plants; Yeasts

Special Issue Information

Dear Colleagues,

The primary purpose of this Special Issue of Plants is to provide a wide audience with the fun of seeing a wide range of plants’ responses to mechanical stimuli. Recent studies have unraveled remarkable behaviors of plants sensing and responding to touch, bending, gravity, invasive microorganisms, and herbivorous insects, all of which affect plant growth and development. In addition, genetic and electrophysiological studies and state-of-the-art technics, such as bioimaging, have brought about the discovery of mechanosensitive channels as mechanosensors and astonishingly ingenious mechanisms of mechanical signaling in plants.

As our fundamental understanding of sensors and mediators of mechanical stimuli has deepened at the molecular level, we have realized that much also remains to be discovered. This Special Issue will highlight the roles of molecules, mechanisms, and systems involved in mechanosensing and mechanotransduction at the molecular, cellular, and tissue levels, as well as the whole plant level.

Prof. Dr. Hidetoshi Iida
Guest Editor

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Plants is an international peer-reviewed open access semimonthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2700 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • mechanical stimulation
  • mechanical stress
  • mechanosensor
  • mechanosensing
  • mechanotransduction
  • mechanical force
  • mechanical signaling
  • calcium signaling
  • mechanosensitive channel
  • stretch-activated channel
  • ion channel
  • transporter
  • touch
  • stretch
  • compression
  • bending
  • wounding
  • gravity
  • osmotic pressure
  • biomechanics
  • electrophysiology
  • bioimaging
  • cell wall
  • leaf
  • stem
  • root
  • sieve tube
  • vessel
  • morphogenesis
  • growth
  • development
  • carnivorous plants
  • sensitive plants
  • plant–microorganism interaction
  • response to insect herbivory

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Published Papers (11 papers)

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Research

Jump to: Review

22 pages, 7049 KiB  
Article
Structure and Biomechanics during Xylem Vessel Transdifferentiation in Arabidopsis thaliana
by Eleftheria Roumeli, Leah Ginsberg, Robin McDonald, Giada Spigolon, Rodinde Hendrickx, Misato Ohtani, Taku Demura, Guruswami Ravichandran and Chiara Daraio
Plants 2020, 9(12), 1715; https://doi.org/10.3390/plants9121715 - 5 Dec 2020
Cited by 9 | Viewed by 4401
Abstract
Individual plant cells are the building blocks for all plantae and artificially constructed plant biomaterials, like biocomposites. Secondary cell walls (SCWs) are a key component for mediating mechanical strength and stiffness in both living vascular plants and biocomposite materials. In this paper, we [...] Read more.
Individual plant cells are the building blocks for all plantae and artificially constructed plant biomaterials, like biocomposites. Secondary cell walls (SCWs) are a key component for mediating mechanical strength and stiffness in both living vascular plants and biocomposite materials. In this paper, we study the structure and biomechanics of cultured plant cells during the cellular developmental stages associated with SCW formation. We use a model culture system that induces transdifferentiation of Arabidopsis thaliana cells to xylem vessel elements, upon treatment with dexamethasone (DEX). We group the transdifferentiation process into three distinct stages, based on morphological observations of the cell walls. The first stage includes cells with only a primary cell wall (PCW), the second covers cells that have formed a SCW, and the third stage includes cells with a ruptured tonoplast and partially or fully degraded PCW. We adopt a multi-scale approach to study the mechanical properties of cells in these three stages. We perform large-scale indentations with a micro-compression system in three different osmotic conditions. Atomic force microscopy (AFM) nanoscale indentations in water allow us to isolate the cell wall response. We propose a spring-based model to deconvolve the competing stiffness contributions from turgor pressure, PCW, SCW and cytoplasm in the stiffness of differentiating cells. Prior to triggering differentiation, cells in hypotonic pressure conditions are significantly stiffer than cells in isotonic or hypertonic conditions, highlighting the dominant role of turgor pressure. Plasmolyzed cells with a SCW reach similar levels of stiffness as cells with maximum turgor pressure. The stiffness of the PCW in all of these conditions is lower than the stiffness of the fully-formed SCW. Our results provide the first experimental characterization of the mechanics of SCW formation at single cell level. Full article
(This article belongs to the Special Issue Mechanical Signaling in Plants)
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11 pages, 2350 KiB  
Communication
Phosphate Deprivation Can Impair Mechano-Stimulated Cytosolic Free Calcium Elevation in Arabidopsis Roots
by Elsa Matthus, Nicholas H. Doddrell, Gaëtan Guillaume, Amirah B. Mohammad-Sidik, Katie A. Wilkins, Stéphanie M. Swarbreck and Julia M. Davies
Plants 2020, 9(9), 1205; https://doi.org/10.3390/plants9091205 - 15 Sep 2020
Cited by 4 | Viewed by 3555
Abstract
The root tip responds to mechanical stimulation with a transient increase in cytosolic free calcium as a possible second messenger. Although the root tip will grow through a heterogeneous soil nutrient supply, little is known of the consequence of nutrient deprivation for such [...] Read more.
The root tip responds to mechanical stimulation with a transient increase in cytosolic free calcium as a possible second messenger. Although the root tip will grow through a heterogeneous soil nutrient supply, little is known of the consequence of nutrient deprivation for such signalling. Here, the effect of inorganic phosphate deprivation on the root’s mechano-stimulated cytosolic free calcium increase is investigated. Arabidopsisthaliana (cytosolically expressing aequorin as a bioluminescent free calcium reporter) is grown in zero or full phosphate conditions, then roots or root tips are mechanically stimulated. Plants also are grown vertically on a solid medium so their root skewing angle (deviation from vertical) can be determined as an output of mechanical stimulation. Phosphate starvation results in significantly impaired cytosolic free calcium elevation in both root tips and whole excised roots. Phosphate-starved roots sustain a significantly lower root skewing angle than phosphate-replete roots. These results suggest that phosphate starvation causes a dampening of the root mechano-signalling system that could have consequences for growth in hardened, compacted soils. Full article
(This article belongs to the Special Issue Mechanical Signaling in Plants)
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14 pages, 2481 KiB  
Article
Xyloglucan Is Not Essential for the Formation and Integrity of the Cellulose Network in the Primary Cell Wall Regenerated from Arabidopsis Protoplasts
by Hiroaki Kuki, Ryusuke Yokoyama, Takeshi Kuroha and Kazuhiko Nishitani
Plants 2020, 9(5), 629; https://doi.org/10.3390/plants9050629 - 14 May 2020
Cited by 23 | Viewed by 5181
Abstract
The notion that xyloglucans (XG) play a pivotal role in tethering cellulose microfibrils in the primary cell wall of plants can be traced back to the first molecular model of the cell wall proposed in 1973, which was reinforced in the 1990s by [...] Read more.
The notion that xyloglucans (XG) play a pivotal role in tethering cellulose microfibrils in the primary cell wall of plants can be traced back to the first molecular model of the cell wall proposed in 1973, which was reinforced in the 1990s by the identification of Xyloglucan Endotransglucosylase/Hydrolase (XTH) enzymes that cleave and reconnect xyloglucan crosslinks in the cell wall. However, this tethered network model has been seriously challenged since 2008 by the identification of the Arabidopsis thaliana xyloglucan-deficient mutant (xxt1 xxt2), which exhibits functional cell walls. Thus, the molecular mechanism underlying the physical integration of cellulose microfibrils into the cell wall remains controversial. To resolve this dilemma, we investigated the cell wall regeneration process using mesophyll protoplasts derived from xxt1 xxt2 mutant leaves. Imaging analysis revealed only a slight difference in the structure of cellulose microfibril network between xxt1 xxt2 and wild-type (WT) protoplasts. Additionally, exogenous xyloglucan application did not alter the cellulose deposition patterns or mechanical stability of xxt1 xxt2 mutant protoplasts. These results indicate that xyloglucan is not essential for the initial assembly of the cellulose network, and the cellulose network formed in the absence of xyloglucan provides sufficient tensile strength to the primary cell wall regenerated from protoplasts. Full article
(This article belongs to the Special Issue Mechanical Signaling in Plants)
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12 pages, 8907 KiB  
Article
Gravity-Sensing Tissues for Gravitropism Are Required for “Anti-Gravitropic” Phenotypes of lzy Multiple Mutants in Arabidopsis
by Nozomi Kawamoto, Yuta Kanbe, Moritaka Nakamura, Akiko Mori and Miyo Terao Morita
Plants 2020, 9(5), 615; https://doi.org/10.3390/plants9050615 - 12 May 2020
Cited by 9 | Viewed by 6127
Abstract
Plant posture is controlled by various environmental cues, such as light, temperature, and gravity. The overall architecture is determined by the growth angles of lateral organs, such as roots and branches. The branch growth angle affected by gravity is known as the gravitropic [...] Read more.
Plant posture is controlled by various environmental cues, such as light, temperature, and gravity. The overall architecture is determined by the growth angles of lateral organs, such as roots and branches. The branch growth angle affected by gravity is known as the gravitropic setpoint angle (GSA), and it has been proposed that the GSA is determined by balancing two opposing growth components: gravitropism and anti-gravitropic offset (AGO). The molecular mechanisms underlying gravitropism have been studied extensively, but little is known about the nature of the AGO. Recent studies reported the importance of LAZY1-LIKE (LZY) family genes in the signaling process for gravitropism, such that loss-of-function mutants of LZY family genes resulted in reversed gravitropism, which we term it here as the “anti-gravitropic” phenotype. We assume that this peculiar phenotype manifests as the AGO due to the loss of gravitropism, we characterized the “anti-gravitropic” phenotype of Arabidopsis lzy multiple mutant genetically and physiologically. Our genetic interaction analyses strongly suggested that gravity-sensing cells are required for the “anti-gravitropic” phenotype in roots and lateral branches. We also show that starch-filled amyloplasts play a significant role in the “anti-gravitropic” phenotype, especially in the root of the lzy multiple mutant. Full article
(This article belongs to the Special Issue Mechanical Signaling in Plants)
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8 pages, 3425 KiB  
Communication
Hechtian Strands Transmit Cell Wall Integrity Signals in Plant Cells
by Arata Yoneda, Misato Ohtani, Daisuke Katagiri, Yoichiroh Hosokawa and Taku Demura
Plants 2020, 9(5), 604; https://doi.org/10.3390/plants9050604 - 9 May 2020
Cited by 14 | Viewed by 5907
Abstract
Hechtian strands are thread-like structures in plasmolyzed plant cells that connect the cell wall to the plasma membrane. Although these strands were first observed more than 100 years ago, their physiological roles are largely unknown. Here, we used intracellular laser microdissection to examine [...] Read more.
Hechtian strands are thread-like structures in plasmolyzed plant cells that connect the cell wall to the plasma membrane. Although these strands were first observed more than 100 years ago, their physiological roles are largely unknown. Here, we used intracellular laser microdissection to examine the effects of disrupting Hechtian strands on plasmolyzed tobacco BY-2 cells. When we focused femtosecond laser pulses on Hechtian strands, targeted disruptions were induced, but no visible changes in cell morphology were detected. However, the calcofluor white signals from β-glucans was detected in plasmolyzed cells with disrupted Hechtian strands, whereas no signals were detected in untreated plasmolyzed cells. These results suggest that Hechtian strands play roles in sensing cell wall integrity. Full article
(This article belongs to the Special Issue Mechanical Signaling in Plants)
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9 pages, 2321 KiB  
Article
MCA1 and MCA2 Are Involved in the Response to Hypergravity in Arabidopsis Hypocotyls
by Takayuki Hattori, Yasuhiro Otomi, Yohei Nakajima, Kouichi Soga, Kazuyuki Wakabayashi, Hidetoshi Iida and Takayuki Hoson
Plants 2020, 9(5), 590; https://doi.org/10.3390/plants9050590 - 5 May 2020
Cited by 30 | Viewed by 5197
Abstract
Plants respond to and resist gravitational acceleration, but the mechanism of signal perception in the response is unknown. We studied the role of MCA (mid1-complementing activity) proteins in gravity perception by analyzing the expression of the MCA1 and MCA2 genes, and the growth [...] Read more.
Plants respond to and resist gravitational acceleration, but the mechanism of signal perception in the response is unknown. We studied the role of MCA (mid1-complementing activity) proteins in gravity perception by analyzing the expression of the MCA1 and MCA2 genes, and the growth of hypocotyls of mca mutants, under hypergravity conditions in the dark. An MCA1 promoter::GUS fusion reporter gene construct (MCA1p::GUS) and MCA2p::GUS were expressed almost universally in etiolated seedlings. Under hypergravity conditions, the expression levels of both genes increased compared with that under the 1 g condition, and remained higher, especially in the basal supporting region. On the other hand, mca-null and MCA-overexpressing seedlings showed normal growth under the 1 g condition. Hypergravity suppressed elongation growth of hypocotyls, but this effect was reduced in hypocotyls of mca-null mutants compared with the wild type. In contrast, MCA-overexpressing seedlings were hypersensitive to increased gravity; suppression of elongation growth was detected at a lower gravity level than that in the wild type. These results suggest that MCAs are involved in the perception of gravity signals in plants, and may be responsible for resistance to hypergravity. Full article
(This article belongs to the Special Issue Mechanical Signaling in Plants)
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Review

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23 pages, 2424 KiB  
Review
Gravity Signaling in Flowering Plant Roots
by Shih-Heng Su, Marie A. Keith and Patrick H. Masson
Plants 2020, 9(10), 1290; https://doi.org/10.3390/plants9101290 - 29 Sep 2020
Cited by 20 | Viewed by 6429
Abstract
Roots typically grow downward into the soil where they anchor the plant and take up water and nutrients necessary for plant growth and development. While the primary roots usually grow vertically downward, laterals often follow a gravity set point angle that allows them [...] Read more.
Roots typically grow downward into the soil where they anchor the plant and take up water and nutrients necessary for plant growth and development. While the primary roots usually grow vertically downward, laterals often follow a gravity set point angle that allows them to explore the surrounding environment. These responses can be modified by developmental and environmental cues. This review discusses the molecular mechanisms that govern root gravitropism in flowering plant roots. In this system, the primary site of gravity sensing within the root cap is physically separated from the site of curvature response at the elongation zone. Gravity sensing involves the sedimentation of starch-filled plastids (statoliths) within the columella cells of the root cap (the statocytes), which triggers a relocalization of plasma membrane-associated PIN auxin efflux facilitators to the lower side of the cell. This process is associated with the recruitment of RLD regulators of vesicular trafficking to the lower membrane by LAZY proteins. PIN relocalization leads to the formation of a lateral gradient of auxin across the root cap. Upon transmission to the elongation zone, this auxin gradient triggers a downward curvature. We review the molecular mechanisms that control this process in primary roots and discuss recent insights into the regulation of oblique growth in lateral roots and its impact on root-system architecture, soil exploration and plant adaptation to stressful environments. Full article
(This article belongs to the Special Issue Mechanical Signaling in Plants)
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10 pages, 450 KiB  
Review
The Effect of Mechanical Stress on Plant Susceptibility to Pests: A Mini Opinion Review
by Catherine Coutand
Plants 2020, 9(5), 632; https://doi.org/10.3390/plants9050632 - 14 May 2020
Cited by 15 | Viewed by 3870
Abstract
Plants are subject to multiple pest attacks during their growing cycle. In order to address consumers’ desire to buy healthy vegetables and fruits, i.e., without chemical residues, and to develop environment-friendly agriculture, major research efforts are being made to find alternative methods to [...] Read more.
Plants are subject to multiple pest attacks during their growing cycle. In order to address consumers’ desire to buy healthy vegetables and fruits, i.e., without chemical residues, and to develop environment-friendly agriculture, major research efforts are being made to find alternative methods to reduce or suppress the use of chemicals. Many methods are currently being tested. Among these methods, some are being tested in order to modify plant physiology to render it less susceptible to pathogen and pest attacks by developing plant immunity. An emerging potentially interesting method that is being studied at this time is mechanical stimuli (MS). Although the number of articles on the effect of MS on plant immunity is still not large, it has been reported that several types of mechanical stimuli induce a reduction of plant susceptibility to pests for different plant species in the case of wounding and non-wounding stimuli. This mini review aims to summarize the knowledge available at this time by raising questions that should be addressed before considering MS as an operable alternative method to increase plant immunity for crop protection. Full article
(This article belongs to the Special Issue Mechanical Signaling in Plants)
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10 pages, 2944 KiB  
Review
Mechanical Signaling in the Sensitive Plant Mimosa pudica L.
by Takuma Hagihara and Masatsugu Toyota
Plants 2020, 9(5), 587; https://doi.org/10.3390/plants9050587 - 4 May 2020
Cited by 55 | Viewed by 18340
Abstract
As sessile organisms, plants do not possess the nerves and muscles that facilitate movement in most animals. However, several plant species can move quickly in response to various stimuli (e.g., touch). One such plant species, Mimosa pudica L., possesses the motor organ pulvinus [...] Read more.
As sessile organisms, plants do not possess the nerves and muscles that facilitate movement in most animals. However, several plant species can move quickly in response to various stimuli (e.g., touch). One such plant species, Mimosa pudica L., possesses the motor organ pulvinus at the junction of the leaflet-rachilla, rachilla-petiole, and petiole-stem, and upon mechanical stimulation, this organ immediately closes the leaflets and moves the petiole. Previous electrophysiological studies have demonstrated that a long-distance and rapid electrical signal propagates through M. pudica in response to mechanical stimulation. Furthermore, the spatial and temporal patterns of the action potential in the pulvinar motor cells were found to be closely correlated with rapid movements. In this review, we summarize findings from past research and discuss the mechanisms underlying long-distance signal transduction in M. pudica. We also propose a model in which the action potential, followed by water flux (i.e., a loss of turgor pressure) in the pulvinar motor cells is a critical step to enable rapid movement. Full article
(This article belongs to the Special Issue Mechanical Signaling in Plants)
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18 pages, 1857 KiB  
Review
The Role of Mechanoperception in Plant Cell Wall Integrity Maintenance
by Laura Bacete and Thorsten Hamann
Plants 2020, 9(5), 574; https://doi.org/10.3390/plants9050574 - 1 May 2020
Cited by 79 | Viewed by 9823
Abstract
The plant cell walls surrounding all plant cells are highly dynamic structures, which change their composition and organization in response to chemical and physical stimuli originating both in the environment and in plants themselves. They are intricately involved in all interactions between plants [...] Read more.
The plant cell walls surrounding all plant cells are highly dynamic structures, which change their composition and organization in response to chemical and physical stimuli originating both in the environment and in plants themselves. They are intricately involved in all interactions between plants and their environment while also providing adaptive structural support during plant growth and development. A key mechanism contributing to these adaptive changes is the cell wall integrity (CWI) maintenance mechanism. It monitors and maintains the functional integrity of cell walls by initiating adaptive changes in cellular and cell wall metabolism. Despite its importance, both our understanding of its mode of action and knowledge regarding the molecular components that form it are limited. Intriguingly, the available evidence implicates mechanosensing in the mechanism. Here, we provide an overview of the knowledge available regarding the molecular mechanisms involved in and discuss how mechanoperception and signal transduction may contribute to plant CWI maintenance. Full article
(This article belongs to the Special Issue Mechanical Signaling in Plants)
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16 pages, 2707 KiB  
Review
The Plasma Membrane—An Integrating Compartment for Mechano-Signaling
by Frank Ackermann and Thomas Stanislas
Plants 2020, 9(4), 505; https://doi.org/10.3390/plants9040505 - 14 Apr 2020
Cited by 33 | Viewed by 12015
Abstract
Plants are able to sense their mechanical environment. This mechanical signal is used by the plant to determine its phenotypic features. This is true also at a smaller scale. Morphogenesis, both at the cell and tissue level, involves mechanical signals that influence specific [...] Read more.
Plants are able to sense their mechanical environment. This mechanical signal is used by the plant to determine its phenotypic features. This is true also at a smaller scale. Morphogenesis, both at the cell and tissue level, involves mechanical signals that influence specific patterns of gene expression and trigger signaling pathways. How a mechanical stress is perceived and how this signal is transduced into the cell remains a challenging question in the plant community. Among the structural components of plant cells, the plasma membrane has received very little attention. Yet, its position at the interface between the cell wall and the interior of the cell makes it a key factor at the nexus between biochemical and mechanical cues. So far, most of the key players that are described to perceive and maintain mechanical cell status and to respond to a mechanical stress are localized at or close to the plasma membrane. In this review, we will focus on the importance of the plasma membrane in mechano-sensing and try to illustrate how the composition of this dynamic compartment is involved in the regulatory processes of a cell to respond to mechanical stress. Full article
(This article belongs to the Special Issue Mechanical Signaling in Plants)
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