Download The impact of abiotic factors on cellulose synthesis

Journal of Experimental Botany, Vol. 67, No. 2 pp. 543–552, 2016
doi:10.1093/jxb/erv488 Advance Access publication 9 November 2015
REVIEW PAPER
The impact of abiotic factors on cellulose synthesis
Ting Wang1, Heather E. McFarlane2,* and Staffan Persson3 1 Max Planck Institute of Molecular Plant Physiology, Am Muehlenberg 1, D-14476 Potsdam, Germany
School of Biosciences, University of Melbourne, 3010, Melbourne, Australia
3 ARC Centre of Excellence in Plant Cell Walls, School of Biosciences, University of Melbourne, 3010, Melbourne, Australia
2 * To whom correspondence should be addressed. E-mail: [email protected]
Received 20 August 2015; Revised 11 October 2015; Accepted 23 October 2015
Editor: Simon Turner, University of Manchester Abstract
As sessile organisms, plants require mechanisms to sense and respond to changes in their environment, including
both biotic and abiotic factors. One of the most common plant adaptations to environmental changes is differential
regulation of growth, which results in growth either away from adverse conditions or towards more favorable conditions. As cell walls shape plant growth, this differential growth response must be accompanied by alterations to the
plant cell wall. Here, we review the impact of four abiotic factors (osmotic conditions, ionic stress, light, and temperature) on the synthesis of cellulose, an important component of the plant cell wall. Understanding how different abiotic factors influence cellulose production and addressing key questions that remain in this field can provide crucial
information to cope with the need for increased crop production under the mounting pressures of a growing world
population and global climate change.
Key words: Abiotic stress, cellulose synthase, cellulose synthesis, cell wall, microtubule, salt stress.
Introduction
Extreme environmental conditions can have a negative
impact on plant growth. Much of this decline in production
may be explained by abiotic stresses (i.e. unfavorable environmental conditions), which potentially result in cell or tissue
damage and/or reduced growth. Considering current climate
projections, it is of immense importance to understand the
processes that underpin plant growth during changes in our
environment (Mickelbart et al., 2015). Traditionally, these
conditions include temperature (either cold or heat), drought,
osmotic, salinity, and other non-biotic environmental stresses
(Le Gall et al., 2015). In addition to these stresses, abiotic
changes at non-stress levels (e.g. light and temperature fluctuations between day and night conditions) can also influence plant growth. Because of their sessile nature, plants
must sense and respond to changes in their environment. One
of the most common plant adaptations to environmental
changes is differential regulation of growth, to grow either
away from adverse conditions or towards more favourable
conditions. Plant cells are surrounded by a protective and
supportive polysaccharide-based plant cell wall that sustains
differential growth during both cell division and cell expansion. Therefore, it is likely that cell wall changes are required
for differential growth responses to changing environmental
conditions.
Many studies have tracked gene expression patterns, protein levels, and metabolite changes in response to different
abiotic conditions in a variety of plants (for example, see
table 1 in Le Gall et al., 2015; Kosova et al., 2011). While
these reports have generated important information to better understand plant cellular responses to abiotic stresses,
we focus this review on potential mechanisms that control
plant cell wall changes, in particular the cell wall component
© The Author 2015. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved.
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544 | Wang et al.
cellulose, at the genetic and cell biology levels in the model
system Arabidopsis thaliana in response to abiotic stress.
Plant responses to abiotic stress
Different abiotic stresses lead to both general and specific
influences on plant growth and development. For example, at
elevated temperatures, many plants show altered architecture:
in Arabidopsis, hypocotyls and petioles elongate to resemble
the morphological response of shade avoidance (Hua, 2009;
Tian et al., 2009). Under high salinity conditions, damage
to plants includes reduced leaf expansion, stomatal closure,
and reduced photosynthesis, finally leading to biomass loss
due to osmotic imbalance (Zhang and Shi, 2013). In addition, overaccumulation of Na+ can induce K+ efflux, leading
to toxic effects (Mahajan and Tuteja, 2005; Maathuis et al.,
2014). Combinations of abiotic stress can further interact to
affect plant physiology (Suzuki et al., 2014). Drought, salinity, and low temperature can lead to turgor loss via changes in
osmotic conditions. Consequently, membranes may become
disorganized, proteins may denature, and reactive oxygen
species (ROS) can accumulate, leading to oxidative damage
(Krasensky and Jonak, 2012).
In addition to these physiological responses, many abiotic
stress conditions induce production of abscisic acid (ABA),
which is often referred to as the ‘stress hormone’. ABA functions as a key regulator in the activation of plant adaptation to
drought and salinity (Cutler et al., 2010; Golldack et al., 2014).
ABA production and ABA signaling have also been implicated in temperature stress signaling and responses to changes
in light conditions or carbon availability (Ljung et al., 2015),
and in non-stress physiological roles, such as stomatal regulation and seed dormancy (Finkelstein, 2013). Other signals are
likely also to play a role in plant responses to abiotic factors,
but these are less well characterized (Yoshida et al., 2014).
At the cellular level, ABA signaling perception and transduction pathways have been extensively reviewed elsewhere
(Cutler et al., 2010; Raghavendra et al., 2010; Finkelstein,
2013). Three different protein classes seem to constitute the
core signaling components, namely Pyrabactin Resistance 1
(PYR)/Regulatory Components of ABA Receptors (RCARs),
protein phosphatase 2C (PP2C) and PP2A family members,
and SNF1-related protein kinase 2s (SnRK2s). However,
a number of other proteins have also been implicated in
ABA signaling (Cutler et al., 2010). Other cellular responses
include a short-term increase in cytosolic Ca2+, production
of ROS (Pei et al., 2000), and activation of kinase cascades
and other signaling events. Similar to most other signal transduction pathways, ABA responses eventually lead to changes
in gene expression patterns via several well-characterized
regulatory elements. Microarray data have shown that many
ABA-responsive genes are also differentially regulated during
dehydration and salt tolerance. These include protein kinases
and phosphatases, regulatory proteins, cell wall proteins, and
enzymes that detoxify ROS; however, the specific changes
that occur in response to ABA can vary between organisms,
tissues, and developmental stages (Nemhauser et al., 2006;
Cutler et al., 2010).
The plant cell wall
Plant cell walls are primarily composed of polysaccharides,
but also include proteins and other compounds. Cell wall polysaccharides are grouped into three main classes, based on
their chemistry: cellulose (McFarlane et al., 2014), hemicelluloses (Scheller and Ulvskov, 2010), and pectins (Atmodjo
et al., 2013). The composition of the cell wall can differ
between species, organs, tissues, and even developmental
stages (Popper et al., 2011). However, in dicot primary cell
walls (i.e. the walls of growing cells that can respond to environmental factors), cellulose is the primary component by
weight and the main load-bearing structure (Zablackis et al.,
1995). Cellulose is synthesized at the plasma membrane–cell
wall interface by cellulose synthase (CesA) enzymes. The
CesAs are organized into a large, multiprotein complex,
called the cellulose synthase complex (CSC). The organization of the CSC allows for co-ordinated synthesis of cellulose
microfibrils, which are made up of many β-1,4-glucan chains.
In the model plant, A. thaliana, cellulose synthesis requires
at least three different plasma membrane-localized CesA
proteins. CesA1, CesA3, and one of the CesA6-like proteins
(CesA2, CesA5, CesA6, and CesA9) are required for cellulose
synthesis in primary cell walls, which are actively growing. In
contrast, CesA4, CesA7, and CesA8 are required for secondary cell wall synthesis (McFarlane et al., 2014).
Studies of fluorescent protein-conjugated CesAs have
revealed that they are localized to the plasma membrane, the
Golgi apparatus, and small subcellular compartments called
small CesA-containing compartments (SmaCCs) or microtubule-associated CesA compartments (MASCs) (Paredez
et al., 2006; Crowell et al., 2009; Gutierrez et al., 2009).
According to current models of cellulose synthesis, the biochemical activity of the CesAs propels the CSC through the
plasma membrane (McFarlane et al., 2014), and this movement is related to the speed and direction of cellulose microfibril synthesis (Paredez et al., 2006). Because of the close
spatial relationship between the trajectories of CesAs and
cortical microtubules, it is hypothezised that cellulose synthesis is guided by microtubules (Baskin, 2001; Paredez et al.,
2006). Indeed, several proteins have been identified that interact with both microtubules and CesAs, and that are required
for normal levels of cellulose synthesis (Bringmann et al.,
2012; Li et al., 2012). Presumably, the intracellular CesAs
(i.e. Golgi and SmaCC/MASC-localized CesAs) are inactive. These SmaCCS/MASCs may, together with the pH of
the trans-Golgi network, control the delivery and recycling of
CesAs to and from the plasma membrane (Luo et al., 2015).
Therefore, internalization of active, plasma membrane-localized CSCs might be one mechanism of regulating cellulose
synthesis.
As the main load-bearing component of the cell wall in
young, actively growing Arabidopsis tissues, cellulose is
an important component of cell wall changes required for
directional cell expansion in response to changing abiotic
conditions. Other cell wall components, such as lignin (CanoDelgado et al., 2003; Moura et al., 2010) and matrix polysaccharides (Sasidharan et al., 2011; Tenhaken, 2015), are clearly
The impact of abiotic factors on cellulose synthesis | 545
altered under biotic and abiotic stresses. Important changes
to the cell wall can also be driven by biotic and developmental factors; however, these have been reviewed elsewhere
(Sanchez-Rodriguez et al., 2010; Hamann, 2012; Bellincampi
et al., 2014).
Influences of water availability on cellulose
The plant cell wall provides mechanical strength to withstand turgor pressure and also acts as one of the front lines
to protect the cell against environmental change. Since turgor
pressure is one of the main driving forces for cell expansion
and plant growth, changes to osmotic pressure can directly
affect plant growth (Lockhart, 1965; Geitmann and Ortega,
2009). Additionally, changes to osmotic conditions can alter
cell expansion, especially of the roots, resulting in directional plant growth towards more favorable water conditions
or away from high salt conditions (Galvan-Ampudia and
Testerink, 2011). Both the orientation of cellulose microfibrils and the composition of the cell wall are important factors that govern the direction of cell expansion (Green, 1962;
Peaucelle et al., 2015), implying that cellulose may be directly
or indirectly regulated by water availability.
Under extreme osmotic stress, plasmolysis (the separation
of the plasma membrane from the cell wall) will necessarily disrupt cellulose synthesis. Mild osmotic or ionic stress
caused rapid internalization of CesAs from the plasma membrane into SmaCCs/MASCs (Crowell et al., 2009; Gutierrez
et al., 2009). However, the signals that induce CesA internalization under these conditions have not been characterized.
Interestingly, clathrin-mediated endocytosis also increased
under salt stress conditions (Konig et al., 2008; Zwiewka
et al., 2015), and clathrin-mediated internalization of CesAs
was recently substantiated in planta (Bashline et al., 2015).
Mutations in one of the 10 CesA genes in Arabidopsis,
CesA8, led to enhanced drought and osmotic stress tolerance
(Chen et al., 2005). The lew2-1 and lew2-2 alleles of CesA8
(originally from a forward genetic screen for a leaf wilting
phenotype) accumulated high levels of osmolytes and ABA.
Several stress-induced marker genes, including RD29A,
ABA2, and P5CS, were transcriptionally up-regulated in lew2
mutants compared with the wild type. Such physiological and
molecular changes may be primarily due to the collapsed
xylem in cesa8 mutants, which could impede water transport
(Chen et al., 2005). In this way, it is possible that changes to
cellulose can influence the water status of the whole plant.
Besides the 10 Arabidopsis CesA genes, there are a large
number of genes encoding cellulose synthase-like (CSL)
proteins. Among the CSL subfamilies, CSLDs are the most
similar to the CesAs (Favery et al., 2001). Indeed, domain
swap experiments demonstrated that when the predicted central catalytic domain of CSLD3 was replaced by the same
region from the cellulose synthase CesA6, this chimeric protein could rescue the root hair phenotype of csld3 mutants
(Park et al., 2011). These results imply that CSLDs may also
play some role in cellulose synthesis. Interestingly, CSLD1,
CSLD2, and CSLD3 genes were induced by increased NaCl
conditions, though none of their single T-DNA mutants displayed enhanced or decreased tolerance to ionic or osmotic
stress conditions (Zhu et al., 2010). In contrast, CSLD5 (also
known as SALT-OVERSENSITIVE6, SOS6) was identified from a forward genetic screen for hypersensitivity to salt
stress (Zhu et al., 2010). sos6 mutants were hypersensitive to
NaCl and KCl, but also to osmotic stress. Only small differences were observed in cell wall composition between the wild
type and sos6 mutants under normal conditions or under salt
stress (Zhu et al., 2010). Therefore, although the CSLDs have
been implicated in cellulose synthesis and cell wall deposition, the exact role of CSLD5/SOS6 in osmotic tolerance
remains unclear.
Salt stress and cellulose synthesis
Saline conditions can affect many aspects of plant growth.
Generally, salt stress can be subdivided into two pathways:
an early-occurring osmotic stress response, which is due to
salt outside of cells, and an ionic stress response due to accumulation of ions (e.g. Na+) inside of cells. These pathways
are, not surprisingly, closely related (Zhu, 2002), but, for the
purposes of this review, we will focus this section on ionicrelated responses, since water availability and osmotic stress
have already been examined in the section above.
In Arabidopsis, several CesA genes have been implicated in
salt stress responses via bioinformatic analyses of gene regulatory networks and gene ontology annotations (Heyndrickx
and Vandepoele, 2012), but direct experimental evidence is
lacking. Many non-CesA-encoding genes have also been
implicated in cellulose synthesis in primary cell walls via
co-expresssion analysis (Persson et al., 2005) and forward
genetic screens. For example, CTL1 encodes a chitinase-like
protein (Zhong et al., 2002; Hermans et al., 2010), which was
co-localized with CesAs in the Golgi apparatus and functionally affected cellulose synthesis (Sanchez-Rodriguez et al.,
2012). The hot2 mutant allele of CTL1 displayed hypersensitivity to salt stresses and osmotic stress (Kwon et al., 2007).
hot2 mutants accumulated high levels of Na+, under both
normal and high salt conditions, but it is unclear how this
is related to the role of CTL1 in cellulose deposition. sos5
mutants were hypersensitive to salt, but not to osmotic stress
(Shi et al., 2003). SOS5 encodes a fasciclin-like arabinogalactan protein, a cell wall-localized glycoprotein, which is
predicted to be linked to the plasma membrane by a glycosylphosphatidylinositol lipid anchor (Shi et al., 2003). SOS5
and a receptor-like kinase (FEI2) were both implicated in
seed coat mucilage production and/or release, and defects in
either of these genes could be phenocopied by cesa5 mutants
(Harpaz-Saad et al., 2011). Despite their similar mutant phenotypes in seeds, it remains to be determined how CesA5 and
SOS5 interact, especially with regards to the salt sensitivity of
sos5. Another indirect link between salt stress and cellulose
synthesis occurs via KOBITO (KOB), a glycosyltransferaselike protein that affects cellulose synthesis (Pagant et al.,
2002). An abi8 mutant allele of KOB was isolated in a screen
for ABA-resistant seed germination (Brocard-Gifford et al.,
546 | Wang et al.
2004), suggesting that KOB might be involved in this and
other ABA-related processes, such as abiotic stress responses.
Furthermore, KOB transcript was specifically down-regulated in the root epidermis and cortex in response to salt
treatment (Dinneny et al., 2008). Combined, these results
implicate several known effectors of cellulose synthesis in cellular responses to salt stress and ABA.
KORRIGAN (KOR) is an endoglucanase that directly
interacted with CesAs at the plasma membrane and potentially in intracellular compartments (Liebminger et al.,
2013; Vain et al., 2014). A temperature-sensitive allele of
KOR, rsw2-1, was hypersensitive to NaCl (Lane et al., 2001;
Kang et al., 2008). Interestingly, this rsw2-1 mutant genetically interacted with both complex glycan1 (cgl1) and staurosporin and temperature sensitive 3a (stt3a) mutants, which
are defective in the production of complex-type N-glycans
and in the unfolded protein response, respectively. Both
rsw2-1 cgl1 and rsw2-1 stt3a double mutants exhibited
growth defects at the permissive temperature. These resembled rsw2-1 single mutants at the restrictive temperature as
well as cgl1 and stt3a single mutants treated with salt, and
rsw1-1 rsw2-1 double mutants (defective in both KOR and
CesA1) (Kang et al., 2008). These results imply that KOR
(and possibly other aspects of cellulose synthesis) requires
complex N-glycans for its function and implicate the production of complex N-glycans and the unfolded protein response
in cellulose synthesis and in salt tolerance. Indeed, KOR is
heavily glycosylated in vivo, and various glycosylation sites
within the protein have been associated with KOR function
and localization (Liebminger et al., 2013; Rips et al., 2014).
Interestingly, N-glycan maturation was also crucial for cellulose synthesis in Oryza sativa (Fanata et al., 2013). Both salt
and herbicide treatment induced removal of CesAs from the
plasma membrane into internal SmaCCs/MASCs (Crowell
et al., 2009; Gutierrez et al., 2009). Although kor mutants
were hypersensitive to salt, they internalized lower levels of
CesAs in response to herbicide treatment (Vain et al., 2014),
suggesting that CesA internalization in the short term may
play a role in salt tolerance.
Salt treatment also resulted in microtubule destabilization (Wang et al., 2007), which may affect CesA trajectories
in the plasma membrane, and, therefore, cellulose deposition (Paredez et al., 2006). Recently, two plant-specific proteins (Companion of Cellulose Synthase 1 and 2; CC1 and
CC2) were characterized to interact with microtubules and
co-localize with CesAs (Endler et al., 2015). Double cc1 cc2
mutants were hypersensitive to both salt and cellulose synthesis inhibitors, but not to osmotic stress. Further functional
analysis revealed that the cytosolic N-terminal parts of the
CC proteins, which were essential for salt tolerance, interacted with microtubules and promoted microtubule dynamics. Time-lapse analysis of microtubule organization and
CesA dynamics revealed that in wild-type plants, salt treatment initially resulted in microtubule depolymerization and
removal of CesAs from the plasma membrane, which agreed
with previous reports (Paredez et al., 2006; Kang et al., 2008).
In wild-type plants, the cortical microtubule array and plasma
membrane-localized CesAs eventually recovered under salt
conditions (Wang et al., 2007; Endler et al., 2015). However,
cc1 cc2 double mutants failed to maintain a recovered microtubule array or CesA trajectories at the plasma membrane
under salt stress conditions (Endler et al., 2015). The authors
proposed a model in which the CC proteins interact with both
CesAs and microtubules and promote microtubule dynamics
in order to maintain cellulose production and plant growth
during sustained salt stress (Endler et al., 2015; Fig. 1).
Light regulation of cellulose synthesis
Because plants are photosynthetic organisms, their growth is
necessarily regulated by light. Through photomorphogenesis,
light signals can directly influence plant growth, allowing the
plant to grow towards optimal light conditions (Fankhauser
and Christie, 2015). Furthermore, plant growth is controlled
by the circadian clock, which can be regulated by light signals (Harmer, 2009). Through photosynthesis, light can also
influence carbon availability. Since synthesis of the polysaccharide-rich cell wall represents a major carbon sink, it seems
reasonable that cell wall synthesis might also be regulated
by the energy status of the cell (Delmer and Haigler, 2002).
Whether cellulose synthesis is regulated in a diurnal pattern
during day and night, and whether this is directly dependent
on components of the circadian clock or regulated by light/
energy sensing, remain open questions.
Photomorphogenesis is one of the oldest fields in plant science. From early studies that revealed that some plants grew
towards light sources, important discoveries were made in the
field of plant hormone signaling, cell expansion, and cell wall
synthesis (Fankhauser and Christie, 2015). The Arabidopsis
hypocotyl is a common model system for photomorphogenesis; under dark conditions (i.e. as if the seed had germinated
under a layer of soil), the hypocotyl underwent rapid elongation. This growth was almost 10 times faster than hypocotyl
growth in light and occurred with little or no cell division,
and therefore relies mostly upon cell elongation (Gendreau
et al., 1997). Although this elongation may be decoupled
from cell wall synthesis in the short term (Refregier et al.,
2004; Hematy et al., 2007), eventually new cell wall material
must be deposited before the cell wall becomes too thin. For
this reason, dark-grown hypocotyls have become a popular model system for understanding cellulose synthesis (e.g.
Paredez et al., 2006).
In addition to photomorphogenesis, light can also trigger
plant responses at the subcellular level. High light conditions,
for example, can trigger reorganization of chloroplasts via
changes to the actin cytoskeleton (Trojan and Gabrys, 1996).
While plastid light avoidance may not directly affect cellulose levels, changes to the actin cytoskeleton can also affect
the subcellular trafficking of CesAs. Mutants with defects
in actin subunits or drugs that inhibit actin dynamics both
displayed defects in the dynamics of SmaCCs/MASCs and
reduced CesA delivery to the plasma membrane, ultimately
resulting in decreased cellulose synthesis (Sampathkumar
et al., 2013). Light also affected the organization of cortical microtubules (Yuan et al., 1994; Lindeboom et al., 2013),
The impact of abiotic factors on cellulose synthesis | 547
- Salt
Primary CSC
Slow CSC
movement
Primary CSC
CESA5
Cell wall
Dark
Cellulose microfibril
Cellulose microfibril
PM
Cytoplasm
CC Protein
Cell wall
PM
Cytoplasm
MT
MT
Normal CSC
movement
Light
CESA5
+ Salt
P
Kinase?
PhyB
SmaCC
Nucleus
Red light
Fig. 1. Impacts of abiotic factors on cellulose synthesis. Under normal conditions (upper left panel), cellulose synthesis occurs at the plasma membrane
and is guided by cortical microtubules. Under salt stress conditions (lower left), microtubules rapidly depolymerize and CSCs are removed from the
plasma membrane. CC1/CC2 co-localize with CesAs and can interact with microtubules to promote microtubule dynamics. CC protein activity is required
for the reformation of cortical microtubules, remobilization of CSCs to the plasma membrane, and the sustained recovery of cellulose synthesis under
salt stress conditions (Endler et al., 2015). In dark-grown seedlings (upper right), CSCs that contain CesA5 move more slowly than CSCs that contain
CesA6. Light treatment (lower right), especially with red light, can alter the activity of CesA5 in a PhyB-dependent manner, probably through direct
phosphorylation of CesA5 via an unknown kinase (Bischoff et al., 2011).
which could influence CSC trajectories and cellulose synthesis (Paredez et al., 2006; Chan et al., 2010).
Despite the close relationship between light and cell wall
synthesis, the extent to which cellulose synthesis is directly
regulated by light signals remains partially unknown. At the
transcriptional level, different light conditions influenced
the expression of CesA genes and members of the cellulose
synthase-like families in both Arabidopsis and Zea mays
(Hamann et al., 2004; van Erp and Walton, 2009). However,
it remains unclear whether this is direct transcriptional regulation through light signaling pathways (i.e. phytochrome and
cryptochrome, reviewed by Chen and Chory, 2011) or indirect as a result of changes to the carbon status of the cell.
At the post-transcrioptional level, CesA phosphopeptides
have been detected in several proteomic studies (e.g. Nuhse
et al., 2004; Boex-Fontvieille et al., 2014). Individual point
mutations that mimicked constitutively phosphorylated
or dephosphorylated residues in CesA1 resulted in subtle
changes in CSC velocities, CSC–microtubule associations,
cellulose content, and hypocotyl morphology (Chen et al.,
2010). These results imply that the phosphorylation state
of CesAs within the CSC can affect cellulose synthesis.
Although the signals that regulate CesA1 phosphoproteins
remain unknown, there is substantial evidence that the CesA5
phosphorylation state and biosynthetic activity is light regulated. Both CesA5 and CesA6 sequences are highly similar,
but expression of CesA5 under the CesA6 promoter was
insufficient to rescue the strong phenotype of dark-grown
cesa6 mutants completely (Desprez et al., 2007; Persson
et al., 2007; Bischoff et al., 2011). However, light treatment
of cesa6 mutants restored CSC speed to wild-type levels. This
response required phytochrome B (PhyB), and activation of
PhyB with red light was sufficient (Bischoff et al., 2011). Sitedirected mutagenesis of four CesA5 residues that have been
detected in phosphoproteomics studies (Nuhse et al., 2004)
revealed that phosphomimetic (i.e. S→D) CesA5 mutants
could fully complement both hypocotyl growth and CSC
speed phenotypes of cesa6 mutants, while S→A/G mutants
were unable to complement (Bischoff et al., 2011). These data
are consistent with a model in which CesA5 phosphorylation
status and biochemical activity can be regulated by light signaling through PhyB (Fig. 1). Interestingly, mutants in several
light signaling pathways (phya, phyb, cry1, hy5, and cop1) all
displayed changes to CesA transcript levels and cellulose content, implying that other components of light signaling pathways may be involved in the regulation of cellulose synthesis
(Wang et al., 2015).
Despite the evidence that light signaling may directly regulate cellulose synthesis, there are also indications that the carbon status of the cell can regulate CesAs at the transcriptional
and post-transcriptional levels. This could provide a mechanism by which cellulose synthesis is indirectly regulated by
548 | Wang et al.
light, through the availability of photosynthetically derived
carbon and related signaling processes. Indeed, mutants with
changes to starch metabolism also displayed cellulose phenotypes and vice versa (Peng et al., 2000). Different photosynthetic conditions (both the concentration of CO2 and light
conditions) changed the metabolic flux of carbon into cellulose and altered the relative abundance of CesA phosphopeptides (Boex-Fontvieille et al., 2014). These results imply
that light and carbon availability signals may be integrated
to produce similar effects on cell wall synthesis enzymes.
Furthermore, after growing under limited carbon conditions,
CesA3 was phosphorylated within 3 min of exogenous supply
of sucrose in a SIRK1 kinase-dependent manner (Wu et al.,
2013), providing one possible mechanism via which CesAs
may be post-translationally modified in response to energy
signals, especially under low light or high light conditions,
both of which can result in decreased photosynthesis and low
energy stress (Ort, 2001).
Cellulose synthesis can also be post-translationally regulated at the level of CSC localization. Transfer of Arabidopsis
seedlings from media containing exogenous sucrose to
sucrose-free media resulted in a decrease in fluorescently
tagged CesA signal at the plasma membrane and an increase
in CesA signal in the Golgi apparatus (Fujimoto et al., 2015).
These results imply that carbon availability within the cell
might regulate cellulose synthesis by altering CesA localization, thereby reducing photosynthate assimilation into the
cell wall under low carbon stress.
Influence of temperature on cellulose
synthesis
Temperature signals are important regulators of plant
growth, especially in the context of diurnal growth regulation
and seasonal growth (e.g. winter dormancy or spring flowering) (Penfield, 2008). In many cases, both temperature and
light conditions can feed into the circadian clock (Harmer,
2009). The mechanisms responsible for temperature sensing
are less well known than other abiotic sensing mechanisms,
but many studies have characterized the influences of either
small temperature fluctuations or larger temperature changes
(i.e. heat and cold stress) on plant growth. These temperature
stress response pathways seem to converge on similar components to drought and/or salt stress at the subcellular level
and often result in similar physiological adaptations (Rizhsky
et al., 2004; Krasensky and Jonak, 2012). However, plants can
become somewhat acclimated to both high and low temperature stress by exposure to mild temperature changes prior to
major stress events, as in the case of cold-induced freezing
tolerance.
Changes in temperature can affect metabolic activities and
growth rates; for example, both hypocotyl elongation and the
speed of CesA movement in the plasma membrane increased
when Arabidopsis seedlings were grown at 29 °C compared
with 21 °C (Fujita et al., 2011). Interestingly, this increase
in temperature also resulted in a decrease in crystalline cellulose (Fujita et al., 2011), implying an inverse relationship
between the rate of cellulose synthesis and its crystallinity.
Furthermore, increasing the growth temperature of Medicago
sativa (alfalfa) plants increased the expression of several CesA
genes (Guerriero et al., 2014).
Once temperatures reach extremes for the plant, downstream cellular responses are similar to that of salt and
drought stress, and include production of ABA and ROS,
influx of calcium ions into the cytosol, and induction of the
unfolded protein response (Mittler et al., 2012). Interestingly,
temperature-sensitive point mutant alleles have been isolated
for both CesA1 and CesA3, as well as for the CSC-interacting
protein KOR (Arioli et al., 1998; Lane et al., 2001; Wang et al.,
2006). It is likely that the discovery of these temperature-sensitive alleles is simply the result of the type of screen used.
However, it is intriguing that several CSC components have
been isolated in temperature-sensitive screens since this may
imply that the complex is especially sensitive to temperature,
or to the effects of high temperature, such as protein misfolding or misglycosylation. Indeed, antisense mutants for CesA2
displayed slightly slower growth rates at higher temperatures
(31 °C compared with 22 °C), but showed no changes to the
height of mature plants or in other phenotypic characteristics (Burn et al., 2002), implying that the CSC might be more
sensitive to high temperature stress than other components
of the cell. Alternatively, it is possible that plants with compromised cell walls could be hypersensitive to abiotic stress.
Cold stress (or freezing stress) can affect CesA gene expression differently in different species. Cold treatments decreased
CesA expression in poplar and cotton, but increased CesA
expression in cold-tolerant rice (Ko et al., 2011; Zhang et al.,
2012; Zhu et al., 2013; J. Chen et al., 2014; X. Chen et al., 2014).
These results imply that the expression of individual CesA
genes may be fine-tuned depending on the level of cold treatment, and the species and developmental stage being studied.
For example, field trials of cotton planted late in the year (i.e.
decreased mean growing temperature) resulted in decreased
CesA expression and total cellulose, compared with cotton that
was planted earlier in the year (J. Chen et al., 2014).
Freezing-tolerant esk1 mutants displayed an irregular
xylem phenotype, and EKS1/TBL29 encodes a protein that
is involved in modification of hemicelluloses, suggesting a
relationship between cell wall synthesis and cold tolerance
(Bischoff et al., 2010; Lefebvre et al., 2011; Yuan et al., 2013).
Consistent with these data, in vitro grown cotton ovules that
were cultured with a constant supply of glucose but fluctuating temperatures had visible rings in their fibers, implying
changes to cellulose synthesis or crystallinity at different temperatures (Haigler et al., 1991). However, this may also be
the result of temperature sensitivity of glucose conversion
enzymes, rather than a direct effect of temperature on the
CSC (Martin and Haigler, 2004).
In addition to these relatively direct impacts on cellulose
synthesis, both high and low temperatures can have effects
on membrane fluidity and cytoskeletal organization, which
may result in an indirect influence on cellulose synthesis.
Changes in temperature can influence membrane fluidity, and
membrane remodeling is a common response to temperature
shifts (Penfield, 2008). Temperature-induced lipid changes
The impact of abiotic factors on cellulose synthesis | 549
are important for the photosynthetic complex in the plastid thylakoid membranes, but changes in plasma membrane
fluidity could affect cellulose synthesis (Fujita et al., 2012).
Interestingly, alteration of membrane phosphoinositide
phosphates by genetic or pharmacological methods changed
cell wall composition (Ischebeck et al., 2013; Fujimoto et al.,
2015), but this could be due to the important role that phosphoinositide phosphates play in membrane trafficking, and
possibly secretion and recycling of CesAs (Krishnamoorthy
et al., 2014), rather than any changes in fluidity. It has also
been suggested that microtubule polymer status may play a
role in integrating signals and initiating cellular responses,
including temperature sensing (Wasteneys, 2003; Nick, 2013).
Similar to salt treatment, low temperature treatments induced
microtubule depolymerization (Sangwan et al., 2001; Komis
et al., 2002), which could affect cellulose synthesis and deposition. Although cellulose synthesis could be maintained in the
absence of cortical microtubules (Himmelspach et al., 2003;
Sugimoto et al., 2003; Gutierrez et al., 2009), CesA trajectories and cellulose crystallinity were both affected (Gutierrez
et al., 2009; Fujita et al., 2011). Given the role that CC1 and
CC2 played in re-establishing microtubule polymer status
and maintaining cellulose synthesis under salt stress conditions (Endler et al., 2015), it will be interesting to determine
whether they play a similar role in cold tolerance.
Summary and future directions
An increasingly important global challenge is to utilize our
land and water resources as efficiently as possible to sustain
our growing population. Plants are essential primary producers, and the growth ranges of different plants are often
defined by abiotic factors, such as temperature, light, and
soil conditions. Therefore, understanding plant growth and
cell expansion under different abiotic conditions is a crucial
future challenge. Here, we have reviewed the evidence that
CesA enzymes, and therefore cellulose synthesis, may be
regulated by abiotic factors. Since cellulose is both a major
carbon sink and the main load-bearing component of growing plant cell walls, regulating cellulose synthesis would allow
plants to modulate cell expansion and resource utilization
simultaneously.
In reviewing the current literature regarding the abiotic
regulation of cell wall synthesis, especially of cellulose synthesis, we have encountered several outstanding questions
in this field. For example, does ABA signaling directly feed
into signals that control cellulose synthesis? Currently, the
signals that directly influence transcriptional and post-transcriptional regulation of CesAs are unknown. After identification of transcription factors that directly regulate CesA
transcript levels; or characterizing kinases, phosphatases,
and other post-transcriptional modifiers that can modulate
CesAs; or identifying the mechanisms that control CesA
secretion and recycling, it will be interesting to determine
whether known abiotic signaling pathways feed into these
processes. Furthermore, how do other abiotic factors influence cellulose production? While there is mounting evidence
that the abiotic factors discussed here can influence cellulose,
other abiotic conditions (e.g. soil pH, micronutrient conditions, atmospheric composition) remain relatively unstudied
in the context of cell wall synthesis. Finally, how do different
signaling pathways cross-talk to regulate cellulose synthesis?
It is well known that there is extensive cross-talk between abiotic response pathways and hormone signaling (Cutler et al.,
2010; Suzuki et al., 2014). It will be an interesting and complex job to dissect such cross-talk between signaling pathways
during the regulation of cellulose synthesis.
Acknowledgements
SP was funded in part from a R@MAP Professorship at University of
Melbourne and an ARC Discovery grant (DP150103495). HEM is supported by an EMBO Long Term Fellowship (ALTF-1246-2013) and an
NSERC Postdoctoral Fellowship (PDF-454454-2014). We apologize to colleagues whose work we could not cite due to length restrictions.
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