Download The Plant Cell Wall Integrity Maintenance

Thorsten Hamann*
Department of Biology, Høgskoleringen 5, Realfagbygget, Norwegian University of Science and Technology, 7491 Trondheim, Norway
*Corresponding author: E-mail, [email protected]; Fax, +47 73596100.
(Received October 3, 2014; Accepted November 10, 2014)
One of the main differences between plant and animal cells
are the walls surrounding plant cells providing structural
support during development and protection like an adaptive
armor against biotic and abiotic stress. During recent years it
has become widely accepted that plant cells use a dedicated
system to monitor and maintain the functional integrity of
their walls. Maintenance of integrity is achieved by modifying the cell wall and cellular metabolism in order to permit
tightly controlled changes in wall composition and structure. While a substantial amount of evidence supporting
the existence of the mechanism has been reported, knowledge regarding its precise mode of action is still limited. The
currently available evidence suggests similarities of the plant
mechanism with respect to both design principles and molecular components involved to the very well characterized
system active in the model organism Saccharomyces cerevisiae. There the system has been implicated in cell morphogenesis as well as response to abiotic stresses such as osmotic
challenges. Here the currently available knowledge on the
yeast system will be reviewed initially to provide a framework for the subsequent discussion of the plant cell wall
integrity maintenance mechanism. The review will then
end with a discussion on possible design principles for the
cell wall integrity maintenance mechanism and the function
of the plant turgor pressure in this context.
Keywords: Biotic stress Cell wall integrity Mechanoperception Osmosensing Plant cell wall Turgor.
Abbreviations: ACC, aminocyclopropane carboxylic acid;
CRD, cysteine-rich domain; CWI, cell wall integrity; CWS,
cell wall stress; DAMP, damage-associated molecular pattern;
GAP, GTPase-activating protein; GEF, guanosine nucleotide
exchange factor; JA, jasmonic acid; MAPK, mitogen-activated
protein kinase; PKC, protein kinase C; RLK, receptor-like
kinase; ROS, reactive oxygen species; SA, salicylic acid; STR,
serine-threonine-rich; WAK, wall-associated kinase.
Introduction
Over the course of time, the perception of plant cell walls in the
research community has changed dramatically. It has become
generally accepted that plant cell walls are not inert objects but
highly dynamic structures, which are intricately involved in
biological processes such as cell morphogenesis as well as response to both biotic and abiotic stresses (Landrein and
Hamant 2013, Malinovsky et al. 2014). Plant cell walls are able
to perform their respective functions during different biological
processes because their composition and fine structure are
modified in response to different types of stimuli. While extensive research has been performed to understand cell wall metabolism, understanding of the mechanisms regulating
stimulus-induced changes in wall composition and structure
is still limited. These mechanisms must perceive and translate
chemical or physical stimuli into quantitative chemical signals,
which lead to modifications in cell wall and cellular metabolism
that in turn bring about specific changes in wall structure and
composition. An example of such a mechanism is the plant cell
wall integrity (CWI) maintenance mechanism, which exhibits
similarities to the one existing in Saccharomyces cerevisiae
(Hamann and Denness 2011). The mechanism is monitoring
the functional integrity of the plant cell wall and maintains
integrity by inducing modifications in wall and cellular metabolism in response to cell wall stress (CWS). CWSs can be defined
as all events which impair the functional integrity of the plant
cell wall. Such events can occur during interaction with the
environment (such as wounding, pathogen infection and exposure to abiotic stresses such as drought) and biological processes (such as rapid cell elongation). While the range of
processes where CWS occurs is quite diverse, the effects on
the cell wall and the plasma membrane are probably fairly specific and possibly quite local. They could involve membrane
stretch/distortion, cell wall-derived ligand/fragment formation
and/or cell wall epitope modifications. In yeast, such effects are
perceived by different osmo-, mechano- and dedicated CWS
sensing mechanisms, which activate different adaptive responses involving changes in cell wall metabolism, cytoskeletal
organization, vesicle transport and cell cycle progression (Levin
2011). Since the yeast CWI maintenance mechanism was discovered quite some time ago, extensive research has been performed leading to a detailed understanding of its mode of
action as well as the molecular machinery involved (Levin
2011).
While evidence supporting the existence of a dedicated
plant CWI maintenance mechanism has accumulated, precise
knowledge of its mode of action and molecular components is
limited. During recent years, different aspects of the plant CWI
maintenance mechanism have been reviewed (Seifert and
Plant Cell Physiol. 56(2): 215–223 (2015) doi:10.1093/pcp/pcu164, Advance Access publication on 21 November 2014,
available online at www.pcp.oxfordjournals.org
! The Author 2014. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists.
All rights reserved. For permissions, please email: [email protected]
Special Focus Issue – Mini Review
The Plant Cell Wall Integrity Maintenance Mechanism—
Concepts for Organization and Mode of Action
T. Hamann | Concepts for plant cell wall integrity maintenance
Blaukopf 2010, Nühse 2012, Wolf et al. 2012, Engelsdorf and
Hamann 2014, Malinovsky et al. 2014, Wolf and Hofte 2014).
While these reviews covered particular aspects such as receptor-like kinase (RLK)-based signaling processes and cell wall
metabolism in the context of the plant CWI maintenance
mechanism very thoroughly, the role of turgor pressure
during CWI maintenance has only been addressed to a limited
extent. Therefore this review will try to assess the function of
turgor pressure in CWI maintenance and discuss different
design possibilities for the mechanism. Information about the
S. cerevisiae CWI maintenance mechanism will be used initially
as a framework for the discussion, since the currently available
knowledge from plants suggests that there may be functional
and design similarities between the plant and yeast
mechanisms.
The Cell Wall Integrity Maintenance
Mechanism in Sacharomyces cerevisiae
Although yeast is a single-celled organism with a cell wall exhibiting a significantly simpler design than the one found in
multicellular plants, the principal problems and functional requirements encountered by both organisms are similar (Levin
2011, Free 2013). In both species, cells need to be plastic during
development to allow changes in shape and size. In parallel,
both require sturdy cell walls to withstand high levels of
turgor pressure and environmental stresses such as drought.
What both organisms also have in common is the need to
maintain the functional integrity of their walls during exposure
to stress and cell morphogenesis. In yeast, cell wall-damaging
agents (zymolase), hypo/hyperosmotic shock, heat and endoplasmatic reticulum stress as well as reorganization of the cytoskeleton or pheromone-induced morphogenesis activate the
CWI maintenance mechanism (Levin 2011). Since they are
comparable with processes that plant cells experience
(wounding, exposure to biotic/abiotic stress and cell elongation), they provide an indication of the large number of biological processes in which the plant CWI maintenance
mechanism is potentially involved. During the different processes in yeast, the initial stimulus perceived seems to be distortion and/or displacement of the plasma membrane relative
to the cell wall. Detecting this type of stimulus has several advantages such as being, on the one hand, highly sensitive, so
even minor CWI impairment events can be detected, while in
parallel permitting a quantitative perception of the damage.
The importance of turgor pressure levels in this context is illustrated by the observation that provision of osmotic support
(light hyperosmotic stress treatment) often neutralizes the effects of CWS-inducing treatments and prevents activation of
CWI maintenance responses in yeast and plants (Kamada et al.
1995, de Nobel et al. 2000, Hamann et al. 2009). Important
aspects which obviously complicate the situation in plants
are multicellularity, higher chemical and structural complexity
of plant cell walls, as well as differences in wall composition and
structure between different cell types. These affect physical
characteristics as well as the presence and accessibility of
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ligands, cell wall fragments and wall epitopes, which could be
involved in CWI maintenance by serving as indicators of the
state of the wall. The latter possibilities are of particular interest
in plants since a large number of RLK-encoding genes have been
identified in plant genomes, with several of them implicated in
CWI maintenance (Engelsdorf and Hamann 2014).
In yeast, three different stimulus perception and signal generation mechanisms are contributing to CWI maintenance and
interact to different degrees (Fig. 1; Levin 2011). Stimulus detection in the first one is mediated by a group of five plasma
membrane-localized proteins (WSC1–WSC3, MTL1 and MID2),
which exhibit structural but not sequence similarities
(Jendretzki et al. 2011). MTL1 and MID2 also exhibit partial
redundancy with each other, with loss-of-function alleles causing severe phenotypes (Rajavel et al. 1999). Whereas mutations
in WSC1 cause strong phenotypic effects, mutations in WSC2
and WSC3 have only mild phenotypic consequences and
double mutant strains exhibit additive phenotypes (Verna
et al. 1997, Ketela et al. 1999). These observations suggest
that the WSC proteins do not have identical functions, a limited
degree of functional redundancy exists and CWS sensing is redundantly organized in yeast. The probably most crucial and
best-characterized protein of the group is WSC1, which will be
discussed here in some detail to illustrate the mode of action of
a CWS sensor. The protein consists of a small cytoplasmic
domain, a transmembrane domain and a highly glycosylated
N-terminal domain, containing the so-called serine-threoninerich (STR) region and the cysteine-rich domain (CRD) (Rodicio
and Heinisch 2010). Recent functional studies involving single
molecule, atomic force microscopy have shown that combining
the highly O-glycosylated N-terminal area of WSC1 with the
STR domain generates sufficient mechanical stiffness to turn
the protein into a functional mechanosensor (Heinisch et al.
2010). Having transmembrane and STR/CRD domains ensures
that the WSC1 protein is anchored simultaneously in the
plasma membrane and the cell wall, meaning that any displacement of the wall in relation to the membrane leads to conformational changes of a protein. These conformational
changes represent the signal leading to activation of a signaling
cascade.
Fig. 1 Schematic, simplified overview of signaling cascades and genes
implicated in CWI maintenance in a yeast cell. The cell wall is colored
beige, the plasma membrane is represented by a green line, with the
intermediate space highlighted in gray. The nucleus is colored light
orange.
Plant Cell Physiol. 56(2): 215–223 (2015) doi:10.1093/pcp/pcu164
Signal translation from WSC1 to ROM1, a cytoplasmic,
plasma membrane-associated guanosine nucleotide exchange
factor (GEF), is mediated via the small cytoplasmic domain in
response to the previously mentioned conformational change
of the extracellular part of WSC1 (Levin 2011). ROM1 in turn
mediates the GTP/GDP exchange at the small GTPase RHO1.
RHO1 is a central integrator responding to different inputs,
whose activity is regulated both by GEFs (such asROM1/2
and TUS) and by GTPase-activating proteins (GAPs)
(Schmelzle et al. 2002, Yoshida et al. 2009). While ROM1 and
ROM2 are responsible for CWS-induced RHO1 activation, TUS
regulates the GTPase in a cell cycle-dependent manner. In contrast, the GAPs are regulating RHO1 activity in a target-specific
manner (Schmidt et al. 2002). RHO1 downstream targets are
the transcription factor SKN7, SEC3 (a component of the exocyst complex), b-1,3 and b-1,6 glucan synthases, BNI1/BNR1
(regulators of actin cytoskeleton organization) and protein
kinase C1 (PKC1) (Alberts et al. 1998, Ketela et al. 1999).
SKN7 is a transcription factor, which is also regulated incidentally by the HOG1 turgor sensing system (see below for more
details). Amongst the genes regulated by SKN7 are OCH1 and
NCA3, which encode proteins required for cell wall biogenesis
and septation (Nakayama et al. 1992, Shankarnarayan et al.
2008). The S. cerevisiae genome encodes only a single homolog
of the mammalian PKC, with deletion of PKC1 causing lethality
unless osmotic support is provided (Levin and BartlettHeubusch 1992, Paravicini et al. 1992). Signals from PKC1 are
relayed via a mitogen-activated protein kinase (MAPK) module
consisting of BCK1, MKK1/2, MPK1 and MLP1. They result in
transcriptional regulation of the response mediators RLM1 and
SBF (Jung et al. 2002, Bermejo et al. 2008, Kim et al. 2008). RLM1
in turn regulates the activity of at least 25 genes involved in cell
wall biogenesis (such as the b-1,3 glucan synthase FKS2) or
encoding proteins residing in the wall (Jung and Levin 1999).
This condensed overview illustrates how CWS perception is
mediated via mechanosensitive plasma membrane proteins
exemplified here by WSC1, highlights the cascades responsible
for signal translation and, by listing the cellular processes
(in)directly involved, indicates how influential CWI maintenance is in yeast metabolism and cell biology.
The second mechanism capable of detecting CWS involves a
stretch-activated, plasma membrane-localized channel complex consisting of CCH1 and MID1 and a signaling cascade
based on changes in cytoplasmic Ca2+ concentrations to activate downstream responses (Levin 2011). The complex is
involved in perception of different stresses such as cold,
hyper/hypo-osmotic and oxidative stress (Matsumoto et al.
2002, Peiter et al. 2005, Popa et al. 2010). The stretch-activated
MID1 channel protein is cation specific, connected to the membrane via a GPI (glycosylphosphatidylinositol) anchor, is found
only in the fungal kingdom and was originally identified
through a forward genetic screen aimed at identifying mutants
exhibiting mating pheromone-induced cell death (Iida et al.
1994, Rispail et al. 2009). CCH1, on the other hand, is a transmembrane Ca2+ channel, which exhibits similarity to the a1
subunit of voltage-gated channels found in animals
(Paidhungat and Garrett 1997). An example illustrating the
links between different signaling cascades perceiving CWS is
the regulation of CCH1 activity by the previously mentioned
MAPK MPK1 (Rispail et al. 2009). Influx of Ca2+ ions into the
cytoplasm activates yeast calmodulin, which in turn regulates
the activity of calcineurin, a heterodimer that has Ca2+- and
calmodulin-dependent phosphatase activity. One of the primary targets of calcineurin activity is CRZ1, a zinc finger transcription factor whose nuclear localization is dependent on
dephosphorylation by calcineurin (Yoshimoto et al. 2002).
Expression analysis has shown that CRZ1 regulates the activity
of different P-ATPases involved in ion homeostasis and of FKS2,
exemplifying how the activity of genes involved in cell wall
metabolism can be regulated by both CWS and CCH1–MID1mediated mechanoperception (Yoshimoto et al. 2002).
Hypo-osmotic stress perception is mediated by both the
CCH1–MID1 channel complex and the hybrid-histidine
kinase SLN1, with the kinase apparently detecting changes in
turgor pressure levels and hypo-osmotic shock (Batiza et al.
1996, Reiser et al. 2003). SLN1 forms an essential part of one
branch of the HOG1 system, which represents the main system
mediating osmoperception in yeast. It consists of two branches,
which detect hypo- (SLN1) and hyper- (SHO1) osmotic stress,
with the resulting signals being relayed via the MAPK kinase
PBS2 to HOG1 kinase, after which the system is named (Levin
2011). The SLN1 branch involves a histidine-phosphotransfer
protein (YPD1) and two downstream regulators (SSK1 and
SKN7) (Fassler and West 2010). While previous work has
shown that changes in turgor levels/hypo-osmotic shock initiate a phospho-transfer from a histidine in the kinase domain to
an aspartate within the receiver domain of SLN1, the specific
biophysical stimulus responsible still remains to be understood
(Saito and Posas 2012). The second transfer occurs then between the SLN1 receiver domain and YPD1, which permits
phospho-transfers to SSK1 and SKN7. While SSK1 is inactivated
through this modification, the transcription factor SKN7 is
activated and induces expression of target genes such as
OCH1 required for cell wall metabolism.
In contrast, under hyperosmotic conditions, the SLN1 signaling activity is reduced, thus allowing enhanced signaling via
the SHO1 branch (Kaserer et al. 2009). Perception of hyperosmotic stress requires plasma membrane-localized SHO1 as well
as HKR1, MSB2 and OPY2 (Saito and Posas 2012). HKR1 and
MSB2 encode mucin-like proteins, which contain STR and
transmembrane domains like WSC1 in addition to the approximately 200 amino acid long HKR1–MSB2 domain. Results from
genetic analysis suggest that the STR domain has an inhibitory
activity while HKR1–MSB2 is activating (Cullen et al. 2004,
Tatebayashi et al. 2007). Recently it was shown that the actin
cytoskeleton is an essential component for signal generation by
MSB2, which suggests that the actin cytoskeleton could contribute to turgor monitoring by acting as a highly efficient
sensor (Tanaka et al. 2014). Signals generated by the different
sensors are translated via a MAPK module involving
STE11/PBS2/HOG1 and lead to different types of responses
(Saito and Posas 2012). Responses range from very fast changes
(seconds to minutes) in ion and glycerol transport activity as
well as metabolic and translational changes to slower (nuclear)
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T. Hamann | Concepts for plant cell wall integrity maintenance
effects allowing long-term modulated adaptations including
changes in gene expression (around 500 transcript levels
change within 10 min after initial stress perception) and inhibition of cell cycle progression (Capaldi et al. 2008). Interestingly,
responses to hypo-osmotic stress lead primarily to transcript
level changes in genes required for cell wall metabolism, while
hyperosmotic stress primarily affects genes required for glycerol
and energy metabolism, hinting at qualitatively different responses required to adapt to hypo- vs. hyperosmotic stress.
To summarize, the available data from research into the
yeast CWI maintenance mechanism show that three different
sensor systems monitor the state of the wall. By combining
inputs from osmo-, mechano- and CWS perception, the yeast
cell constantly has very detailed information about the state of
its cell wall and can make adaptive changes in composition and
structure by modifying cell wall and/or cellular metabolism to
maintain CWI. This can involve direct regulation of cell wall
biosynthetic genes or cytoskeletal reorganization. In parallel,
CWI signaling is also influencing fundamental cellular processes
such as cell cycle progression, highlighting the importance of
CWI during developmental processes.
Plant Cell Wall Metabolism Involved in Cell
Wall Integrity Maintenance
In recent years, data supporting the existence of a dedicated
plant CWI mechanism have increased but have not yet led to
the same level of understanding as in yeast. However, enough
information has been generated to allow a discussion of possible organizational structures for the plant CWI maintenance
mechanism. Initially in this section there will be a brief introduction of plant cell wall components required for discussing
plant CWI maintenance. The second part will focus on experiments using manipulation of cellulose biosynthesis as a tool to
impair CWI and the data generated will be used to outline the
possible mode of action of the plant CWI maintenance mechanism. This will involve discussions of our current knowledge of
possible stimuli responsible for activating the response mechanism and whether turgor pressure is a passive element in plant
CWI maintenance or is actively participating.
The plant cell wall performs many different functions during
cell differentiation and in response to a changing environment.
This is possible because of the large number of different cell wall
polysaccharides and proteins in cell wall metabolism, which
enable it to adapt its characteristics to different requirements.
Here only cell wall components and processes directly relevant
for discussing the plant CWI maintenance mechanism (based
on the currently available data) will be covered. For in-depth
coverage of plant cell wall metabolism, several recently published, comprehensive reviews are recommended (Liepman
et al. 2010, McFarlane et al. 2014, Rennie and Scheller 2014,
Sénéchal et al. 2014). Primary (elastic) cell walls are formed
directly after cell division, whereas mechanically reinforced
walls (called secondary walls) can be formed later on during
differentiation. The main load-bearing element of plant cell
walls is cellulose, which consists of strands of b-1,4-linked
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glucose units organized in microfibrils that are produced by
plasma membrane-localized rosette complexes (McFarlane
et al. 2014). The composition of the rosette complexes active
during primary cell wall formation differs from that of those
active during secondary cell wall formation, which also results
in different sensitivities to cellulose biosynthesis inhibitors such
as isoxaben (Heim et al. 1990). Isoxaben is a frequently used tool
in plant CWI maintenance research to cause CWS (Manfield
et al. 2004, Hematy et al. 2007, Hamann et al. 2009, Tsang et al.
2011). It inhibits cellulose production during primary cell wall
formation by blocking the activity of CELLULOSE SYNTHASE A
(CESA) 3 and 6 based on data from mutations causing resistance
to the inhibitor (Heim et al. 1989, Scheible et al. 2001, Desprez
et al. 2002). Thus, isoxaben treatment probably causes CWS by
weakening the load-bearing element of the wall while (high)
turgor levels remain unchanged. Combining generation of
CWS in a highly specific way with availability of mutants causing
resistance makes isoxaben a convenient tool to study CWI maintenance in a controlled manner. To illustrate the effects of isoxaben treatment on a single-cell level, Fig. 2A–D shows cells in
the epidermis from mock-, sorbitol- and/or isoxaben-treated primary root tips of Arabidopsis seedlings expressing a plasma
membrane marker (M. Veerabagu and T. Hamann, unpublished).
While mock- (Fig. 2A) and sorbitol-treated (Fig. 2B) epidermal
cells do not exhibit dramatic distortion, cells in roots treated with
isoxaben (Fig. 2C) are bloated. Intriguingly, epidermal cells treated with a combination of isoxaben and sorbitol exhibit shapes
more similar to the mock control than the isoxaben-treated
roots (compare Fig. 2D and B). While these observations illustrate the effects of weakened cell walls vs. constant turgor pressure, the specific nature of the initial stimulus indicative of CWI
impairment remains to be determined and will be discussed
below in more detail.
Cellulose microfibrils are cross-linked with xyloglucans and
the resulting mesh is embedded in a matrix consisting of pectins in primary cell walls. Pectins consist mainly of galacturonic
acid and form some of the most complex wall polysaccharides
(Sénéchal et al. 2014). While the backbones of the pectic polysaccharides are fairly conserved and involve distinct domains
such as homogalacturonan, xylogalacturonan and rhamnogalacturonan I or II, the side chains exhibit significant diversity
with respect to the neutral cell wall sugars attached. In contrast
to cellulose, xyloglucans and pectins are synthesized in the
Golgi before being transported to the wall for integration.
During the integration process, pectins can also be de-esterified
or methylated, which influences wall characteristics such as
adhesion, porosity and rheological properties (Sénéchal et al.
2014). These modifications are mediated by members of large
gene families such as pectin methyl esterases or acetylesterases
(Wolf et al. 2009). This generates a highly redundantly organized system and provides a large number of options for dynamic modifications and cross-linking in a highly controlled
manner. These in turn will affect the availability of epitopes
for proteinaceous binding partners as well as physical and biological characteristics of the wall (Bethke et al. 2014). One of the
main differences between primary and secondary cell walls is
the deposition of lignin in secondary cell walls. Lignin is one of
Plant Cell Physiol. 56(2): 215–223 (2015) doi:10.1093/pcp/pcu164
Fig. 2 Effects of cellulose biosynthesis inhibition and sorbitol treatments on cell shape in Arabidopsis seedling root tips. Seedling root
tips were mock (A), 300 mM sorbitol (B), 600 nM isoxaben (C) or
sorbitol/isoxaben treated for 2 h. Expression of the WAVE131–
yellow fluorescent protein (YFP) plasma membrane marker was detected using a Leica SP5 laser confocal microscope. Cells of interest are
highlighted with white arrows.
the most abundant cell wall polymers and has different functions such as water proofing the walls of xylem cells or reinforcing cell walls in response to pathogen infection (Moura et al.
2010, Wang et al. 2013). Monolignols such as p-coumaryl, coniferyl and sinapyl-alcohols give rise to the main lignin units (phydroxyphenyl, guaiacyl and syringyl). After their synthesis,
monolignols are transported to the cell wall and transformed
into monolignol radicals through the activities of laccases and
peroxidases. These radicals form random cross-links, giving rise
to three-dimensional structures in which other cell wall components such as cellulose microfibrils are embedded. Callose is
another cell wall component consisting of b-1,3-linked glucose
units, which is frequently formed at the wall by callose synthases in response to biotic stress or as a wound response to
reinforce a damaged wall (Hardham et al. 2007).
Plant Cell Wall Integrity Maintenance
Responses
The first two reports postulating the existence of a plant CWI
maintenance mechanism elegantly illustrate its involvement in
plant development and defense. Cano-Delgado and colleagues
aimed to isolate genes required for cell morphogenesis during
Arabidopsis thaliana primary root development (Cano-Delgado
et al. 2000, Cano-Delgado et al. 2003). They isolated a novel
allele (ectopic lignification) for CESA3. While the mutation
caused, on the one hand, a reduction in cellulose production
in elongating cells, in seedling roots simultaneous ectopic production of lignin was observed. The authors showed that the
same effect can be achieved by using isoxaben and suggested
that a compensatory reaction was taking place where a missing
load-bearing element was replaced with another one. In parallel, Ellis and colleagues were interested in isolating novel signaling components required for jasmonic acid- (JA) mediated
responses to pathogen infection (Ellis and Turner 2001, Ellis
et al. 2002). They performed a reporter-based forward genetic
screen using the JA-inducible VEGETATIVE STORAGE
PROTEIN1 (VSP1) promoter to drive expression of a luciferase
reporter gene. They also isolated a mutant allele of CESA3 they
named constitutive expression of VSP1 (cev1), because it caused
activation of the JA-sensitive reporter construct. Their phenotypic characterization of the mutant plants detected increased
JA (lignin) production and resistance to Erisyphe orontii as well
as induction of defense gene expression. In the following years,
other groups used genetic and inhibitor-based methods to
assess the impacts of both short (minutes up to 36 h) and
long-term (days to weeks) cellulose biosynthesis inhibition in
Arabidopsis seedlings and callus cultures (Manfield et al. 2004,
Duval et al. 2005, Paredez et al. 2006, Duval and Beaudoin, 2009,
Hamann et al. 2009, Denness et al. 2011, Tsang et al. 2011,
Wormit et al. 2012). The results of these studies have provided
a global overview of the impact of CWS (here caused by isoxaben treatment) on cell signaling, as well as cellular and cell
wall metabolism. Previous work showed that cellulose biosynthesis inhibition affects cytoskeleton organization within
15 min after the start of treatment, reduces elongation of
root epidermal cells after 1 h, causes ectopic production of JA
and reactive oxygen species (ROS) after 3–4 h, lignification of
cells in the root elongation zone after 6 h, transient redistribution of soluble sugars after 8–10 h, inhibition of photosynthetic
activity, callose deposition and necrosis in cotyledons after 18 h
and later on changes in levels of cell wall components such as
arabinose, uronic acid and galactose. Interestingly, isoxabeninduced lignin, callose and JA production, necrosis and redistribution of soluble sugars can be suppressed by provision of
osmotic support similarly to the results obtained in yeast
(Hamann et al. 2009, Wormit et al. 2012). These observations
illustrate the wide range of responses and highlight the similarities to phenotypes observed when plants are exposed to biotic
or abiotic stress.
All the studies employed cellulose biosynthesis inhibition as
a tool, which has the advantage of causing a specific, standardized CWS and making results comparable. However, this is
only one possible type of CWS, so it remains to be determined
how generally applicable the results are since the responses
probably differ dependent on the type of CWS. For example,
mutations in CESA4, 7 and 8 required for secondary cell wall
formation activate ABA-mediated signaling cascades and affect
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resistance to different pathogens (Ralstonia solanacearum and
Plectosphaerella cucumerina) compared with mutations in the
genes required for primary cell wall formation (HernandezBlanco et al. 2007). This suggests that, for example, the pathogen infection mechanisms or the CWS responses could differ
between elongating and differentiated cells and highlights the
need for additional, detailed studies.
Stimuli Indicating Cell Wall Integrity
Impairment
Currently both the specific nature and whether one or several
qualitatively different types of stimuli are responsible for activating the CWI maintenance mechanism remain to be determined. Here three different options will be discussed to
illustrate possible scenarios taking place in planta upon exposure to CWI impairment. In the first scenario, the stimuli could
consist of fragments/ligands released, increased accessibility of
cell wall epitopes or a combination of these. These stimuli could
occur during cell wall degradation by invading pathogens,
wounding or cell elongation, and could activate the CWI maintenance mechanism via RLKs, which would bind to ligands/
fragments/epitopes becoming available. This consideration
also highlights the possibility that the CWI maintenance mechanism could form an essential component of plant immunity
such as responses to damage-associated molecular patterns
(DAMPs), since cell wall-derived fragments can be considered
to be DAMPs. Different RLKs have been implicated in CWI
maintenance. The available evidence suggests that THESEUS1,
which belongs to the CrRLK1L family of RLKs, has a key role in
the response to isoxaben-induced CWI impairment since it
suppresses cellulose deficiency phenotypes and THESEUS1overexpressing lines exhibit increased lignin deposition
(Hematy et al. 2007, Denness et al. 2011). An important question remaining to be addressed is whether THESEUS1 binds a
ligand released during CWI impairment or an epitope residing
in the cell wall that becomes (in)accessible. Wall-associated
kinases (WAKs) are also regularly discussed in this context,
since they have been shown to bind pectin and pectin-derived
epitopes as well as being implicated in turgor-sensitive processes with their signals being relayed via MAPKs to downstream response targets (Brutus et al. 2010, Kohorn and
Kohorn, 2012, Kohorn et al. 2014). Since other candidate
RLKs such as PEPR1/2, FERONIA, HERKULES1/2 and FEI1/2
have been discussed extensively in recent reviews they will
not be covered here again (Lindner et al. 2012, Engelsdorf and
Hamann 2014, Wolf and Hofte 2014). Signals generated by these
RLKs could be translated through established signaling cascades
involving ROS, JA, salicylic acid (SA), aminocyclopropane carboxylic acid (ACC) and ABA, leading to downstream responses
such as modification/adaptation of cell wall metabolism
(Malinovsky et al. 2014, Miedes et al. 2014).
A second scenario involves turgor pressure pushing outwards against a cell wall weakened due to active cell elongation,
metabolic defects or biotic/abiotic stress. All these processes
could cause distortion of the wall or displacement of the
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plasma membrane in relation to the wall. From a turgor
point of view, this could correspond to a hypo-osmotic shock
situation, with the available data supporting this view since
mild hyperosmotic shocks (support) suppress CWI impairment
in Arabidopsis seedlings and yeast (Fig. 2; Hamann et al. 2009,
Levin 2011). In this scenario, stimuli would be perceived by
(plasma membrane-localized) proteins, which are able to
sense displacement of the membrane vs. the wall (mechanosensitive) and/or changes in turgor pressure levels. Stimulus
perception could lead to conformational changes (analogous
to WSC1) or opening of membrane channels (MID1–CCH1),
which initiate signaling cascades. In recent years, different gene
families encoding mechano- (MCA) and turgor-sensitive (MSL,
OSCA and AHK) proteins have been discussed in this context,
with functional evidence implicating MID1 COMPLEMENTING
ACTIVITY1 (MCA1), Arabidopsis histidine kinase 4 (AHK4/
CRE1) and calcium-based signaling cascades in the response
to CWD caused by isoxaben (Denness et al. 2011, Wormit
et al. 2012, Kurusu et al. 2013, Monshausen and Haswell,
2013, Yuan et al. 2014).
While the available evidence supports both scenarios just
described, a third scenario combining them is theoretically possible as well. It is reasonable to assume that stimuli indicative of
CWI impairment encompass both chemical (ligands/epitopes)
and physical (displacement) signals. By detecting and integrating both types of signals, the plant cell would receive detailed qualitative and quantitative information regarding the
(functional) integrity of its wall, enabling it to modulate/
adapt the responses specifically to particular functional
requirements. Such a system design has the additional benefit
of generating a highly redundantly organized mechanism where
even if one type of sensor is inactivated the other ones would
still be able to detect CWI impairment. Since previous work has
implicated at least one RLK (THESEUS1) and a putative
mechanosensor (MCA1) in plant CWI maintenance, it should
be possible to test this hypothesis by combining relevant
genotypes.
With respect to the function of turgor pressure in plant CWI
maintenance, the available evidence is ambiguous. Data from
yeast suggest that turgor sensing is involved in CWI maintenance and regulates to some extent the activity of the same
target genes such as the WSC1 cell wall sensor and the
MID1–CCH1 complex. In Arabidopsis, turgor manipulation
suppresses all responses to isoxaben-induced CWS similar to
yeast (Hamann et al. 2009). In parallel, AHK4, which can complement the yeast turgor sensor (SLN1), is required to mediate
osmosensitive, isoxaben-induced metabolic changes (Wormit
et al. 2012). However, AHK4 is thought to function as a cytokinin receptor in plants, which does not help to clarify the
function of turgor sensing in CWI maintenance (Stolz et al.
2011). Bearing in mind the limited experimental evidence available, the logical next step has to be a systematic functional
analysis of genes possibly capable of detecting changes in
turgor pressure levels using standardized assays such as isoxaben-induced lignin and JA production to determine their respective contributions and make them comparable. Candidate
gene families of particular interest in this context are the AHKs,
Plant Cell Physiol. 56(2): 215–223 (2015) doi:10.1093/pcp/pcu164
MSLs and OSCA (Wilson et al. 2013, Kumar and Verslues 2014,
Yuan et al. 2014).
To summarize, currently it is an exciting time to work on the
plant CWI maintenance mechanism since enough evidence has
accumulated to support the notion that it is an important
component of plant developmental, stress response and cell
wall metabolic processes. Additionally the available functional
data provide sufficient guidance for targeted, hypothesis-driven
experiments to dissect its mode of action. In parallel it has been
suggested that understanding the mechanism may generate
novel options to overcome successfully the plasticity of plant
cell walls, which has slowed down previous attempts to manipulate biomass quality in a knowledge driven way to facilitate
bioenergy production from ligno-cellulosic feed stocks (Burton
and Fincher 2014).
Funding
Work in the author’s research group is supported by the DFG,
the Sather Centre, EMBO and the Norwegian University of
Science and Technology.
Acknowledgments
The author would like to thank the anonymous referees for
their comments and apologize to colleagues whose work
could not be discussed due to space limitations.
Disclosures
The authors have no conflicts of interest to declare.
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