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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. For permissions, please email: [email protected] 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? 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