monitoring polysaccharide dynamics in the plant cell wall · 1 update review 2 3 monitoring...

Update review 1

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Monitoring Polysaccharide Dynamics in the Plant Cell Wall 3

Catalin Voiniciuc1, Markus Pauly

1, Björn Usadel

2,3* 4

5 1 Institute for Plant Cell Biology and Biotechnology and Cluster of Excellence on Plant Sciences 6

(CEPLAS), Heinrich Heine University, Düsseldorf, 40225, Germany 7 2 Institute for Biology I, BioSC, RWTH Aachen University, Worringer Weg 3, 52074 Aachen, 8

Germany 9 3 Forschungszentum Jülich, IBG-2 Plant Sciences, Wilhelm Johnen Strasse, 52428 Jülich, 10

Germany. 11

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* Address correspondence to [email protected] 13

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Running title: Plant Cell Wall Dynamics 16

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One-sentence summary: 19

New technologies reveal the deposition and remodeling of plant cell wall polysaccharides, and 20

their impact on plant development. 21

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Authors’ contributions: 25

CV, MP and BU drafted and wrote the article. 26

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Funding information: 30

The authors want to acknowledge support by the DFG project CASOM US98/13-1 and the 31

Ministry of Innovation, Science and Research within the framework of the NRW 32

Strategieprojekt BioSC (No. 613 313/323‐400‐002 13), the Excellence Cluster CEPLAS (EXC 33

1028) and the BMBF project “Cornwall” (031B0193A/B). 34

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Plant Physiology Preview. Published on February 27, 2018, as DOI:10.1104/pp.17.01776

Copyright 2018 by the American Society of Plant Biologists

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Monitoring Polysaccharide Dynamics in the Plant Cell Wall 36

Introduction 37

All plant cells are surrounded by complex walls that play a role in growth and 38

differentiation of tissues. Walls provide mechanical integrity and structure to each cell, and 39

represent an interface with neighboring cells and the environment (Somerville et al., 2004). Cell 40

walls are composed primarily of multiple polysaccharides that can be grouped into three major 41

classes: cellulose, pectins, and hemicelluloses. While cellulose fibrils are synthesized by the 42

plant cells directly at the plasma membrane (PM), the matrix polysaccharides are produced in the 43

Golgi apparatus by membrane-bound enzymes from multiple glycosyltransferase families 44

(Oikawa et al., 2013). After secretion to the wall via exocytosis, the structures of the non-45

cellulosic polysaccharides are modified by various apoplastic enzymes. In addition to 46

polysaccharides, most plant cell walls contain small amounts of structural proteins such as 47

extensins and arabinogalactan proteins. 48

Cell walls are dynamic entities, rather than rigid and recalcitrant shells, that can be 49

remodeled during plant development and in response to abiotic or biotic stresses. Cell expansion 50

requires the deposition of additional material in the surrounding primary walls, as well as the 51

reorganization and loosening of existing polymers to allow for wall relaxation and controlled 52

expansion (Cosgrove, 2005). The latest model of the primary wall structure proposes that 53

cellulose-cellulose junctions only occur at a limited number of “biomechanical hotspots”, where 54

protein catalysts must selectively act to initiate wall loosening (Cosgrove, 2018). In tissues 55

undergoing growth, recycling of polysaccharides via a suite of enzymes can contribute to the 56

construction of elongating walls (Barnes and Anderson, 2017). Once elongation ceases, some 57



2

cells deposit thick secondary walls that incorporate additional polysaccharides. Many secondary 58

walls are impregnated with the polyphenol lignin and thereby become relatively fixed structures 59

that exclude water and resist hydrolysis. 60

The dynamics of plant cell walls have traditionally been challenging to characterize in 61

muro due to technical limitations and the structural complexity of their components. As an 62

example of structural complexity, pectins can incorporate 12 different sugars in at least 25 63

glycosidic linkages, and can be further decorated with methyl, acetyl or phenolic groups 64

(Atmodjo et al., 2013). While analyses of extracted carbohydrates have been instrumental for 65

characterizing walls (Foster et al., 2010; Pettolino et al., 2012; Carpita and McCann, 2015), they 66

do not reveal how polysaccharides are distributed across different cell layers or within a 67

particular wall. Historically, only a few techniques were available to detect polysaccharides in 68

living plant cells, and many of the wall-directed probes had a broad specificity and/or poorly 69

characterized targets (Wallace and Anderson, 2012). For instance, the Calcofluor White dye has 70

been frequently used to stain cell walls, but fluoresces in the presence of β-glucan structures 71

from all three major polysaccharide classes (Anderson et al., 2010). Recent technical 72

developments, such as the identification of more specific probes, have helped elucidate the 73

components of the plant cell wall. 74

In this review, we focus on current and emerging techniques for monitoring the dynamics 75

of polysaccharides in the cell wall (Table 1). We highlight recent biological insights gained from 76

these methods, discuss the limitations of each approach, and provide a summary of specific 77

probes that may be used to identify different polysaccharide structures in situ (Figure 1, Table 2). 78



3

Cellulose 79

Visualization of Crystalline Cellulose Microfibrils 80

Cellulose microfibrils are aggregates of linear β-1,4-linked glucan chains, which are 81

stabilized by intra- and intermolecular hydrogen bonds in the walls (Notley et al., 2004; 82

McNamara et al., 2015). Several types of methods have been used to visualize the microfibrils in 83

the wall (Table 1). Primary wall cellulose fibrils have been estimated to be 3 nm in diameter by 84

spectroscopic and diffraction techniques (Thomas et al., 2013), whereas larger aggregates of 85

microfibrils in the 5-10 nm diameter range have been found in conifer wood (Fernandes et al., 86

2011). Even fibrils with diameters of up to 40 nm were observed by electron microscopy 87

utilizing freeze-fracture techniques (McCann et al., 1990). Currently, it is not clear how much 88

interspersed matrix polymer material contributes to these aggregate estimates. Due to this size 89

range, microfibrils can be observed by both atomic force microscopy (AFM) and scanning 90

electron microscopy (Zhang et al., 2016), and their angles and distances can be determined 91

(Marga et al., 2005). Crystalline cellulose is initially oriented randomly in meristematic cells 92

(McCann et al., 1990), but is later aligned as parallel fibrils, transverse to the axis of elongation 93

(Sugimoto et al., 2000). The orientation of microfibrils is hypothesized to mechanically restrict 94

the direction of cell extension, leading to anisotropic growth. Parallel cellulose microfibrils are 95

separated during cell expansion (Marga et al., 2005), presumably yielding to internal turgor 96

pressure and being loosened via enzymatic modification of adjoining matrix polysaccharides 97

(Wolf and Greiner, 2012; Cosgrove, 2016). Since microfibril diameters do not appear to decrease 98

during the elongation process, the fibrils are likely not modified directly. 99

100

Monitoring Cellulose Structure with Molecular Probes 101



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In addition to cellulose found in a crystalline microfibril form, some walls are estimated 102

to be composed of ~40% “amorphous” cellulose (Marga et al., 2005). This substantial proportion 103

of cellulose cannot be determined by the aforementioned microscopy tools, and can only be 104

roughly estimated by spectroscopic methods. Carbohydrate-binding modules (CBMs) are 105

powerful probes for detecting the presence and dynamics of amorphous cellulose (McLean et al., 106

2002). CBMs are non-catalytic domains of carbohydrate-active enzymes, and are thought to 107

facilitate binding to specific substrates (Hall et al., 1995). Multiple cellulose-directed CBMs 108

have been identified that bind either crystalline or amorphous structures (Table 2; McLean et al., 109

2002). Indirect immunolabeling of plant sections with His-tagged versions of these CBMs (see 110

Figure 1A for a detailed mechanism) has revealed the diversity of cellulose forms in various cell 111

walls using fluorescence (Blake et al., 2006) or electron microscopy (Ruel et al., 2012). For 112

example, collenchyma cells contain primary walls with a larger abundance of amorphous 113

cellulose compared to microfibril-rich secondary walls. CBMs also provided hints about polymer 114

interactions, as partial enzymatic removal of pectic polysaccharides in plant sections leads to a 115

more intensive labelling of crystalline cellulose. This indicates a close spatial proximity of these 116

two polymer classes (Blake et al., 2006), and has been independently demonstrated by solid state 117

NMR (Dick-Perez et al., 2012). However, certain probes may have broader specificities than 118

expected. For instance, CBM3a is a common label for crystalline cellulose that can also bind 119

xyloglucan (XyG), a xylose-substituted glucan (Hernandez-Gomez et al., 2015). This issue could 120

be mitigated by imaging walls before and after treatment with xyloglucanase, or by using 121

alternative probes (Table 2). 122

Fluorescent proteins (FPs) can be tagged to CBM domains to directly analyze 123

polysaccharide structure without the secondary or tertiary reagents shown in Figure 1A. For 124



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instance, two fluorescently-tagged CBMs enabled the dual-labeling of crystalline and amorphous 125

cellulose at the surface of plant fibers following biomass deconstruction (Gourlay et al., 2015). 126

Such chimeric protein constructs could potentially be transformed into plants to monitor 127

polysaccharides without any incubation steps. While in vivo fluorescent CBM probes may 128

provide greater insights into polysaccharide dynamics in growing cells, caution is necessary. For 129

example, direct expression of fluorescent CBM proteins in plants would have to be carefully 130

tested and optimized to ensure that the target polymer is visualized without altering its native 131

architecture or plant development. Another potential disadvantage is that the FP domain may 132

interfere with the ligand binding site of the CBM (Knox, 2012). Regardless of the presence of FP 133

tags, binding of a CBM or any other polysaccharide-directed monoclonal antibodies (mAbs) 134

provide limited quantitative information; an epitope may be found in multiple polymers, it could 135

be masked by its neighbors, or hidden by an altered conformation of the target polysaccharide 136

(Pattathil et al., 2015). Despite these issues, proteinaceous probes such as CBMs provide an 137

unprecedented view of the occurrence of wall polysaccharides. Alternatively, crystalline 138

cellulose in living cells can be fluorescently stained with Pontamine S4B (Figure 1E, Table 2; 139

available as Direct Red 23) to monitor microfibril reorientation in real-time (Anderson et al., 140

2010). In contrast to Calcofluor White, S4B is highly specific to cellulose. 141

142

Cellulose microfibrils are generated at the PM (Figure 1C) by rosette structures harboring 143

complexes of multiple cellulose synthase (CESA) enzymes and other proteinaceous components 144

(Hill et al., 2014; McFarlane et al., 2014). It is believed that the synthesis of glucan chains by the 145

CESAs propels the complex through the PM, depositing cellulose microfibrils in its wake 146

(McFarlane et al., 2014). The estimated size of cellulose microfibrils suggests that they are 147

produced by CESA rosettes containing a total of 18 CESA proteins, which was validated in the 148



6

moss Physcomitrella patens using an improved method for electron microscopy (Nixon et al., 149

2016). FP-tagged CESA enzymes have also been visualized in the PM of living cells from the 150

model plant Arabidopsis thaliana (Paredez et al., 2006). Their movement has been used as a 151

powerful proxy to assess the speed and orientation of microfibril formation in planta. By this 152

technique, the synthesis of cellulose in secondary walls has been estimated to be significantly 153

faster than in primary walls (Paredez et al., 2006; Wightman et al., 2009; Watanabe et al., 2015). 154

Since specific elements of the cytoskeleton can also be visualized with mAbs or FP probes, 155

numerous elegant studies have shown that the direction of cellulose deposition is coupled to 156

microtubule orientation (McFarlane et al., 2014). 157

Fluorescently-labeled CESAs are not only localized in the PM but also in intracellular 158

compartments such as the Golgi apparatus and other small bodies (Crowell et al., 2009). These 159

could represent proteins that are in transit through the secretory system: from the endoplasmatic 160

reticulum where they are synthesized, to the outer membrane of the cell. Alternatively, the 161

intracellular CESA-containing compartments could be the result of endocytosis presumably for 162

protein recycling purposes, or are destined to be reinserted into the PM under specific conditions, 163

such as salt stress (Gutierrez et al., 2009). Therefore, endomembrane trafficking is likely a key 164

regulator of when and where cellulose can be generated at the cell surface. This also highlights 165

the major limitation of FP probes as a proxy for assessing cellulose microfibril orientation, 166

direction, and synthesis. Even though CESAs can be observed in real-time, it is not certain when 167

the proteins are actually producing cellulose. This may be overcome by monitoring cellulose 168

deposition with several probes, ideally at the same time. A combined analysis of FP-CESA 169

localization, CBM3a immunolabeling, and S4B staining in Arabidopsis roots revealed that 170

cellulose is deposited at the cell plate earlier than previously thought (Miart et al., 2014). 171



7

Surprisingly, FP-tagged CESAs are not localized at the tip of elongating root hairs, where S4B 172

and CBM3a signals are detected (Park et al., 2011). Hence, other proteins are likely to be 173

responsible for the formation of these -glucans (Park et al., 2011), and new probes are needed 174

to further characterize their structure and to identify how they are produced. 175

Matrix Polysaccharides 176

In contrast to the simple, linear cellulose polymers, matrix polysaccharides (such as pectins 177

or hemicelluloses) can be branched and substituted and are thought to be synthesized in the 178

Golgi (Figure 1B). Once secreted to the wall, matrix polysaccharides are structurally modified by 179

various apoplastic enzymes, including glycosyl hydrolases and carbohydrate esterases. 180

Pectins are structurally complex polysaccharides that are rich in α-1,4-linked galacturonic 181

acid (GalA) subunits (Atmodjo et al., 2013), such as homogalacturonan (HG), 182

rhamnogalacturonan I (RG I) and II (RG II), and xylogalacturonan. Hemicellulose encompasses 183

matrix polysaccharides that can be extracted using only alkali as a chaotropic agent (Scheller and 184

Ulskov, 2010), and thus includes XyG, xylans, mannans, and mixed-linkage glucans. In contrast 185

to the current dogma for hemicellulose biosynthesis in the Golgi, mAbs and FP probes indicate 186

that mixed-linkage glucans are assembled at the PM (Wilson et al., 2015). Therefore, the 187

production of matrix polysaccharides and their subsequent remodeling in the wall are only 188

starting to be understood. The molecular architecture of matrix polysaccharides has been 189

revealed by the development of enhanced methods (Table 1) and the identification of probes with 190

specific target epitopes (Table 2). 191

192

Monitoring Pectic Structures 193



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HG is the most abundant pectin in primary walls, and can be modified in planta via 194

methylesterification and acetylation. Two other major pectic domains, rhamnogalacturonan I 195

(RG I) and II (RG II) contain rhamnose, and are covalently linked by HG (Atmodjo et al., 2013). 196

The Arabidopsis genome contains more than 170 HG-related enzymes (Sénéchal et al., 2014), 197

although the precise roles of only a few have been characterized to date. HG methylesterification 198

status plays important roles in various developmental processes, and is tightly controlled by 199

pectin methylesterases (PMEs), PME inhibitors (PMEIs), subtilisin-type serine proteases (SBTs), 200

and at least one E3 ubiquitin ligase (Levesque-Tremblay et al., 2015). Mutants with altered 201

expression of these players have been characterized using mAbs directed against HG domains 202

with different degrees of methylesterification. Several mAbs (e.g. LM19, 2F4; Table 2) 203

preferentially bind unesterified or sparsely methylated HG, whereas other mAbs (e.g. LM20, 204

JIM7; Table 2) recognize methylesterified pectin. Utilizing these probes has been instrumental in 205

observing the state of HG methylesterification in cell walls. Immunolabeling coupled with 206

transmission electron microscopy revealed that HG is synthesized in the plant Golgi apparatus in 207

a highly methylesterified state labeled by JIM7, whereas unesterified GalA epitopes are barely 208

detected without chemical de-esterification (Zhang and Staehelin, 1992). After deposition in the 209

wall, pectin can be de-esterified by PMEs in a specific spatiotemporal manner that results in one 210

of two contrasting roles (Levesque-Tremblay et al., 2015). Regions of unesterified GalA residues 211

can be cross-linked via Ca2+

ions (forming “egg-boxes”) to increase wall stiffness, or cleaved by 212

pectin-degrading enzymes (e.g. polygalacturonases) to promote wall loosening. 213

The impact of HG methylesterification on cell wall architecture can be conveniently 214

examined in the mucilage capsules that coat Arabidopsis seeds (Figure 1D to 1G). This 215

specialized cell wall contains more than 90% pectin, and only minor amounts of cellulose and 216



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hemicellulose (Voiniciuc et al., 2015b). Thick, hydrophillic capsules of mucilage can be 217

indirectly immunolabeled with the CCRC-M36 mAb (Figure 1F; Table 2) or quickly visualized 218

with Ruthenium Red (RR; Table 2), a dye that selectively binds to negatively charged molecules 219

such as unesterified GalA regions and is compatible with both light and electron microscopy 220

(Hanke and Northcote, 1975). The RR dye was a convenient probe for identifying chemically-221

mutagenized Arabidopsis mucilage-modified (mum) mutants (Western et al., 2001), and a large 222

number of natural Arabidopsis variants with altered mucilage architecture (Voiniciuc et al., 223

2016). The presence of Ca2+

ions, which can be manipulated by distinct chemical treatments, 224

negatively regulates the size of RR-stained mucilage capsules. For instance, flying saucer1 (fly1) 225

mutant seeds release smaller RR-stained mucilage capsules when hydrated in water, due to a 226

lower degree of pectin methylesterification and an increased abundance of HG egg-boxes 227

detected with the 2F4 mAb (Voiniciuc et al., 2013). The exogenous addition of Ca2+

ions further 228

blocks the ability of fly1 mucilage to expand, consistent with the model that unesterified HG 229

regions can form stiff gels. In stark contrast, the impaired wall architecture of the fly1 mutant 230

was largely rescued by treating seeds with cation chelators (Voiniciuc et al., 2013) that disrupt 231

the Ca2+

cross-links between unesterified HG chains to facilitate loosening of matrix 232

polysaccharides. Similar calcium-dependent phenotypes, consistent with the HG egg-box model, 233

have been observed for two additional mucilage mutants involved in HG methylation status: 234

sbt1.7 (Rautengarten et al., 2008) and pmei6 (Saez-Aguayo et al., 2013). While FLY1 regulates 235

the HG methylesterification status via protein ubiquitination in the endomembrane system, 236

SBT1.7 and PMEI6 inhibit PME activity directly in the extracellular matrix where HG is present. 237

Nevertheless, a new model for the role of HG in cell expansion postulates that Ca2+

-238

bridged pectins are not as prevalent in planta as previously thought (Hocq et al., 2017). The 239



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frequency of HG egg-boxes in cell walls may have been overestimated by certain 240

immunolabeling procedures, highlighting the need to still apply caution when using these 241

powerful tools. For instance, 2F4 immunolabeling of egg-box crosslinks requires addition of 242

Ca2+

ions (Liners and Cutsem, 1992), at concentrations that are several fold greater than 243

physiological levels (Hocq et al., 2017). Therefore, the effects of HG de-methylesterification on 244

cell walls should also be monitored with other techniques. AFM (Table 1) has been used to 245

quantify the elasticity of walls in living meristems of Arabidopsis wild type plants, as well as 246

transgenic lines overexpressing a PME gene or an antagonistic PMEI gene (Peaucelle et al., 247

2011). While the egg-box model predicts that PME activity increases the stiffness of the pectic 248

matrix, the AFM experiments found that de-methylesterification of HG promoted wall loosening 249

and was a prerequisite for organ initiation (Peaucelle et al., 2011). Therefore, unesterified HG in 250

growing cells is likely targeted by pectin-cleaving enzymes such as the recently identified 251

POLYGALACTURONANSES INVOLVED IN CELL EXPANSION (PGX1, PGX2, and 252

PGX3), which are required for the development of multiple Arabidopsis organs (Xiao et al., 253

2014; Rui et al., 2017; Xiao et al., 2017). 254

While the HG structure is typically visualized using mAbs, these relatively large probes 255

may have limited permeability and require multiple incubation steps that render them unsuitable 256

for real-time imaging of pectin dynamics (Figure 1A). Probes with considerably smaller 257

molecular weights have recently emerged for monitoring HG properties. Propidium iodide (PI) is 258

a membrane-impermeable stain that competes with Ca2+

ions to bind to demethylesterified 259

pectins. When used at low concentrations, PI enables imaging in Arabidopsis root hairs and 260

pollen tubes without altering cell growth (Rounds et al., 2011). Mutant pollen tubes with 261

impaired exocytosis show repetitive bursts of growing tips at cell wall regions that accumulate 262



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PI-stained demethylesterified HG (Synek et al., 2017). Alternatively, sparsely methylated HG 263

can be labelled in real-time with fluorescently-tagged chitosan oligosaccharides (COS; Table 2), 264

and the specificity of this labelling was tested using carbohydrate microarrays (Mravec et al., 265

2014). Sequential use of COS probes coupled to two distinct fluorophores revealed how cells in 266

Arabidopsis root caps accumulate de-esterified HG over time. Recently, another oligosaccharide 267

probe consisting only of GalA units was used to continuously monitor the distribution of 268

calcium-crosslinked HG in elongating pollen tubes (Mravec et al., 2017). Throughout pollen tube 269

growth, tightly-linked HG was only detected outside of the tip-growing region, consistent with 270

the polar localization of PMEI proteins (Röckel et al., 2008). Both PI and the oligosaccharide 271

probes can label HG in less than 20 minutes to provide an unprecedented resolution of HG 272

dynamics in living cells. Recently, HG dynamics were visualized using COS conjugated with 273

Alexa Fluor 488 (COS488

) and PI probes in guard cells lacking or overexpressing the PGX3 274

polygalacturonase (Rui et al., 2017). Although COS488

and PI labelled only partially overlapping 275

regions of the wall, they both supported an inverse relationship between the presence of PGX3 276

and unesterified HG. Additionally, COS488

and PI were more sensitive for quantifying GalA 277

epitopes in three dimensions, compared with indirect labeling of fixed cells with mAbs (LM19, 278

LM20 and 2F4) (Rui et al., 2017). Therefore, these new probes are compelling alternatives to 279

mAbs and should be further exploited. 280

Following the use of click chemistry to image polymers in animals, fungi and bacteria, 281

modified sugars can be metabolically incorporated into plant cell walls to visualize pectin 282

dynamics (Anderson and Wallace, 2012). Although fucose is part of several wall components, 283

Arabidopsis roots were shown to primarily incorporate an alkynylated fucose analog into a high 284

molecular-weight pectic polymer that is most likely RG-I (Anderson et al., 2012). Since the 285



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alkynylated fucose analog sugar can be fluorescently labelled with a membrane-impermeable 286

compound (Figure 1A), it can be used to identify proteins required to maintain the delivery of 287

pectin to the cell wall. This probe showed that elongating root epidermal cells lacking the 288

FRAGILE FIBER1 (FRA1) kinesin incorporate less RG I and in an uneven pattern, compared to 289

the wild type (Zhu et al., 2015). In addition, the synthesis and redistribution of another pectic 290

polymer can now be visualized using a clickable analogue of 3-deoxy-D-manno-oct-2-ulosonic 291

acid (Kdo), a monosaccharide unique to RG II (Dumont et al., 2016). The Kdo-derived probe is 292

compatible with other probes (e.g. the alkynylated fucose analog) to simultaneously image 293

multiple matrix polysaccharides during root growth. The RG I and RG II probes have been 294

detected via copper-catalyzed click reactions, which are toxic to Arabidopsis seedlings and may 295

damage the wall. However, two alternative methods to detect click-compatible analogs not 296

requiring copper were recently developed and could be used to study the long-term dynamics of 297

extracellular glycans (Hoogenboom et al., 2016). 298

299

Hemicellulose Dynamics in the Primary Cell Wall 300

XyG is a ubiquitous matrix polysaccharide in land plants, and represents the most abundant 301

hemicellulose in the primary wall (Pauly and Keegstra, 2016). Since XyG cross-links cellulose 302

microfibrils, it was thought that this network forms the major load-bearing structure in growing 303

cells and that its metabolism plays a major role in cell expansion. However, the Arabidopsis xxt1 304

xxt2 mutant lacking detectable XyG displays only minor morphological changes and vegetative 305

growth defects (Cavalier et al., 2008). These observations question the role of XyG in extension 306

growth. Nevertheless, the xxt1 xxt2 mutant plants exhibit burst root hairs (Cavalier et al., 2008), 307

indicating that XyG plays an important role in tip growth. 308



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The side-chain substitution pattern of XyG can vary depending on the plant species 309

(Schultink et al., 2014). However, recent analyses revealed that XyG structures can be tissue 310

specific (Liu, 2015; Lampugnani et al., 2013; Dardelle et al., 2015). Based on chemical analyses 311

of ground plant tissue samples, fucogalactoXyG is generally found in many eudicots, but not in 312

plant vegetative tissues from phylogenetically younger species of the Solanaceae and the grasses 313

(Poaceae). An alternative approach to identify fucogalactoXyG on a cellular level is the use of 314

the mAb CCRC-M1 (Table 2), which was the first wall-directed mAb with a thoroughly 315

characterized epitope specificity (Puhlmann et al., 1994). FucogalactoXyG labeled by CCRC-M1 316

has been visualized in specialized tissues in the grasses (Brennan and Harris, 2011), in the pollen 317

tubes of tomato (Solanum lycopersicum; Dardelle et al., 2015) and tobacco (Nicotiana alata; 318

Lampugnani et al., 2013), and in root hairs of rice (Oryza sativa; Liu et al., 2015). The presence 319

of this particular form of XyG in tip-growing tissues suggests that its structure and/or 320

metabolism is important for tip growth or at the interface between the plant and the environment. 321

Recently, the role of XyG in stomatal guard cell function was examined through live-cell 322

spinning disk confocal microscopy of xxt1 xxt2 mutant cell walls (Rui and Anderson, 2016). 323

XyG-deficient guard cell walls are less capable of longitudinal expansion during stomatal 324

movement, and show impaired organization of S4B-stained cellulose. Mutants containing point 325

mutations in CESA genes show similar defects as well as aberrant distribution of GFP-tagged 326

CESA proteins during stomatal movements (Rui and Anderson, 2016). While the cellulose 327

structure was visualized with two distinct tools (S4B dye and FP-CESA), the dynamics of XyG 328

polymers as stomata open and close have yet to be investigated. 329

The development of specific probes compatible with live-cell microscopy is essential for 330

monitoring the structure of XyG in dynamic contexts, such as stomatal movements. 331



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Sulphorhodamine-labeled XyG oligosaccharides have been used to visualize XyG 332

transglucosylase/hydrolase enzymes that act specifically in elongating walls of root epidermal 333

cells in Arabidopsis and tobacco root epidermal cells (Vissenberg et al., 2005). Since 334

fluorescently-labelled XyG was incorporated into the cell wall, this approach could be applied in 335

other biological contexts. In addition, multiple azido or alkynyl sugar analogues of glucose and 336

xylose have been synthesized as potential reporters for XyG (Zhu et al., 2016), but none of them 337

were metabolically incorporated into Arabidopsis roots. Although another study found a glucose 338

derivative (6dAG) that is specifically incorporated at root hair tips, this probe co-localizes with 339

callose, inhibits root growth, and leads to stunted root hairs (McClosky et al., 2016). Therefore, 340

no suitable clickable analogues are currently available to label hemicelluloses. Even though most 341

of the wall fucose is present in fucogalactoXyG (Zablackis et al., 1996), an alkynylated fucose 342

analog only labelled RG I (Anderson et al., 2012). Apparently, the corresponding 343

XyG:fucosyltransferase is not able to accept the fucose analog as a donor substrate (Perrin et al., 344

1999; Rocha et al., 2016), while the RG-I:fucosyltransferase does. These experiments highlight 345

one of the current limitations of using click chemistry or other sugar analogs to monitor wall 346

dynamics. Hopefully future research with different sugar analogs will overcome the exclusion 347

from wall polymer metabolic enzymes. 348

349

Xylan Dynamics in Secondary Cell Walls 350

Xylans and mannans are the two major classes of hemicelluloses that accumulate in plant 351

secondary walls (Scheller and Ulvskov, 2010), and have backbones composed primarily of 352

xylose and mannose, respectively. The dynamics of mannan have yet to be explored in great 353

detail, although new insights into their structural roles were gained in recent years (Yu et al., 354



15

2014; Voiniciuc et al., 2015a). Several mAb probes are available (e.g. LM21, LM22; Table 2), 355

but they cannot bind acetylated forms of mannan and are not sensitive to the presence of glucose 356

in the polymer backbone (Marcus et al., 2010), which varies in nature. A major limitation of 357

these proteinaceous probes is that their access to target epitopes can be heavily masked by pectic 358

HG (Marcus et al., 2010). Although the masking HG could be enzymatically removed prior to 359

immunolabeling, it would be advantageous to develop probes that surmount these challenges. 360

In the last two years, important tools for studying xylan dynamics have been developed. 361

De novo synthesis of various oligosaccharides has enabled the characterization of xylan-directed 362

mAbs (Schmidt et al., 2015). While microarrays with plant polysaccharides (Moller et al., 2008) 363

or oligosaccharides (Pedersen et al., 2012) have been previously probed with mAbs (Pattathil et 364

al., 2010), arrays of synthetic glycans have an exceptional purity and facilitate the precise 365

mapping of the epitopes recognized by molecular probes. A comprehensive screen of 209 wall-366

directed mAbs against 88 synthetic glycans, including 22 xylan oligosaccharides, identified 367

specific epitopes for 78 probes that were previously uncharacterized (Ruprecht et al., 2017). This 368

study also confirmed the epitopes of a few mAbs that were already characterized in detail (Table 369

2), such as the specificity of LM28 for xylan substituted with glucuronic acid (Cornuault et al., 370

2015). Since neither synthetic glycans nor specific mAbs are currently available for acetylated 371

xylan (Ruprecht et al., 2017), the current toolbox must be expanded to detect the full diversity of 372

hemicellulose structures found in nature. For instance, xylans can also be directly imaged using 373

CBMs. FP-tagged CBM15 (named OC15; Table 2) was developed as a sensitive probe for 374

monitoring xylan polymers during lignocellulosic biomass conversion (Khatri et al., 2016), but 375

could also be used in planta. 376



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To overcome the limitation of probes and to gain greater insight into polymer interactions, 377

solid state NMR has emerged as a powerful technique to monitor the molecular architecture of 378

the plant cell wall. Xylans were found to have a flattened conformation and were bound closely 379

to cellulose microfibrils in wild-type Arabidopsis stems, but not in a cellulose-deficient mutant 380

(Simmons et al., 2016). Moreover, solid state NMR revealed that an even pattern of substitution 381

is essential for xylan to bind to cellulose in the two-fold screw conformation (Grantham et al., 382

2017). The role of these regular motifs is also supported by mass spectrometric sequencing and 383

molecular dynamics simulations of xylan oligomers (Martínez-Abad et al., 2017). The 384

substitution of xylans can also be observed using MALDI mass spectrometry imaging, an 385

emerging technique that employs specific glycosyl hydrolases to map variations in 386

polysaccharide localization and structure. So far, this promising method was only used to track 387

the composition and distribution of arabinoxylan and mixed-linkage glucans during endosperm 388

maturation in wheat (Triticum aestivum) (Veličković et al., 2014). However, MALDI mass 389

spectrometry can detect all major classes of cell wall polysaccharides (Westphal et al., 2010), 390

and was successfully used to screen for Arabidopsis axy mutants with altered XyG structures 391

(Gille et al., 2011; Günl et al., 2011a; Günl and Pauly, 2011; Günl et al., 2011b; Schultink et al., 392

2015). Hence, MALDI when coupled with microscopy offers the possibility to i) enhance the 393

chemical wall structural resolution down to a cellular level and ii) image the dynamics of 394

multiple polysaccharides in situ. This will be particularly advantageous for detecting wall 395

polymers (e.g. acetylated hemicelluloses) that cannot currently be detected with existing probes 396

(Table 2). 397



17

Concluding Remarks 398

Advanced techniques to monitor polysaccharides (Table 1), along with the genomics era of the 399

last decade, have delivered an avalanche of new data pertaining to the mechanisms of plant cell 400

wall synthesis and metabolism. Many genes involved in these processes have now been 401

characterized. However, the spatiotemporal organization and regulation of wall polymer 402

synthesis and degradation, the assembly of polymer networks, and the dynamics of wall 403

assemblies during cell growth and differentiation remains a challenge (see Outstanding 404

Questions box). Identification and characterization of novel polysaccharide-specific probes, 405

coupled with sensitive techniques, will shed light on these unresolved issues. Even classic probes 406

(e.g. S4B and FP-tagged proteins; Table 2) can be visualized with increased precision by clearing 407

plant tissues using new techniques that forgo costly and time-consuming embedding and 408

sectioning steps (Ursache et al., 2018). Although the resolution of confocal microscopes was 409

historically limited by diffraction to >200 nm (Hell, 2007), this barrier has been surpassed in the 410

last decade to enable the imaging of living plant cells at the nanoscale level (Komis et al., 2018). 411

With the advent of super-resolution fluorescence microscopy, polysaccharide-binding probes 412

such as S4B can potentially be visualized in the walls of living plant cells at a resolution 413

approaching more invasive methods such as AFM and electron microscopy (Table 1; Liesche et 414

al., 2013). Indeed, novel membrane probes can now reveal the dynamics of organelles at a spatial 415

resolution of 50 nm, and over tens of minutes instead of tens of seconds for FP-tagged probes 416

(Takakura et al., 2017). Label-free in situ imaging of plant cell wall polysaccharides would be 417

ideal, and could be facilitated by further developments in techniques such as MALDI mass 418

spectrometry imaging. Other components of the wall not covered in this review, such as lignin 419

and structural proteins, could or have already been monitored using similar techniques. 420



18

Therefore, there has never been a better time to explore the dynamics of a diverse range of plant 421

cell wall polymers. 422

423

424

Tables 425

Table 1. Comparison of advanced techniques for monitoring polysaccharide dynamics. 426

A summary of technical advantages and limitations, along with key biological observations, which are discussed in 427 the text. For the electron microscope column, TEM or SEM indicate points specific to either transmission or 428 scanning electron microscopy, respectively. R denotes the relative resolution of a technique and ranges from the 429 diffraction limit of light (+) to atomic-resolution (+++). S denotes the relative speed of a technique (including the 430 typical sample preparation time) and ranges from multiple days (+) to mere seconds (+++). 431 432

Light

Microscopy Electron

Microscopy Atomic Force

Microscopy Solid state

NMR X-ray

Diffraction

Ad

van

tag

es • Live-cell

imaging • Many probes

(see Table 2)

• TEM: mAb-

compatible • Organelle

resolution

• Measurement

of elasticity • Near-native cell

walls

• Atomic-scale

chemical

information • Intact tissues

• Highest spatial

resolution

Vis

ual

izat

ion

• CESA

dynamics • Polymers

across tissues

• SEM: CESA

rosette size • TEM: Polymers

within a cell

• Pattern of

polymers • Stiffness of cell

wall

• Cellulose-

matrix polymer

location

• Cellulose

microfibril

dimensions

Lim

itat

ion

s • Epitope

masking • Probe

specificity

• TEM: Long

preparation • Fixation

artifacts

• Uncertain

polymer

identity

• Analysis of

biomass as a

whole (no cell

specificity)

• Works only for

crystal

structures

R + ++ ++ +++ +++ S +++ + ++ + +

433

434



19

Table 2. Selected probes to investigate the dynamics of different plant wall polysaccharides. 435

Additional antibodies with known targets that are not listed here are available from PlantProbes 436 (http://plantprobes.net) and CarboSource (https://www.ccrc.uga.edu/~carbosource/CSS_home.html). Abbreviations: 437 CBMs, carbohydrate-binding modules; mAb, monoclonal antibody; Kdo, 3-deoxy-D-manno-oct-2-ulosonic acid. 438 439 Probe Target Reference

Cellulose

Calcofluor White Various β-glucan structures (Anderson et al., 2010)

Pontamine Scarlet 4B (S4B) Specific for crystalline cellulose (Anderson et al., 2010)

FP-tagged CESA proteins Proxy for cellulose synthesis (Paredez et al., 2006)

CBM3a Crystalline cellulose (Blake et al., 2006)

CBM28 Amorphous cellulose (Blake et al., 2006)

Pectin

Ruthenium Red (RR) Pectin with de-esterified GalA (Hanke and Northcote, 1975)

LM19 mAb HG, particularly de-esterified

forms

(Verhertbruggen et al., 2009)

2F4 mAb Unesterified HG cross-linked by

Ca2+

(Liners and Cutsem, 1992)

LM20 mAb Methylesterified HG (Verhertbruggen et al., 2009)

JIM7 mAb Methyl-esterified epitopes of

HG

(Knox et al., 1990)

CCRC-M36 mAb Rhamnogalacturonan I

backbone

(Ruprecht et al., 2017)

Chitosan oligosaccharides (COS) De-esterified GalA regions (Mravec et al., 2014)

Oligogalacturonides (OG) Unesterified HG cross-linked by

Ca2+

(Mravec et al., 2017)

Propidium iodide (PI) Unesterified GalA units (Rounds et al., 2011)

Alkyne derivative of fucose Rhamnogalacturonan I (Anderson et al., 2012)

Azido derivative of Kdo Rhamnogalacturonan II (Dumont et al., 2016)

Xyloglucan Sulphorhodamine labelling Xyloglucan oligosaccharides (Vissenberg et al., 2005)

CCRC-M1 mAb FucogalatoXyG (Puhlmann et al., 1994)

Mannan

LM21 mAb Branched and unbrached

mannans

(Marcus et al., 2010)

LM22 mAb Unbranched mannans (Marcus et al., 2010)

Xylan

CBM15 - mOrange2 (OC15) Xylan (xylohexaose) (Khatri et al., 2016)

LM10 mAb Unbranched xylan (McCartney et al., 2005)

LM11 mAb Branched xylan (e.g. with

arabinose)

(McCartney et al., 2005)

LM28 mAb Glucuronosyl substituted xylans (Cornuault et al., 2015)

440

441

Figure Legends 442



20

Figure 1. Major classes of probes and key steps to image cell wall polysaccharides. 443

(A) Illustration of the steps required prior to microscopy (represented by a magnifying glass) for 444

different types of probes. Secondary antibodies (2° mAb) are commercially available and should 445

be selected based on the final application (electron versus light microscopy) and the available 446

equipment (e.g. fluorescence filters). Probes in colored boxes are exemplified in panels (B to G). 447

(B and C) Sites of wall polysaccharide synthesis in Arabidopsis cotyledons expressing the 448

yellow FP markers wave_22Y and wave_138Y, respectively (Geldner et al., 2009). FP signal 449

and chloroplast intrinsic fluorescence are shown using Orange Hot and Cyan Hot look-up tables 450

in Fiji (Schindelin et al., 2012). (D to G) Mucilage architecture of an S4B-stained and mAb-451

labeled (CCRC-M36 and AlexaFluor 488 2° mAb) Arabidopsis seed. (D) shows a segment of a 452

whole seed (black) that has been brought into contact with water. The only clearly visible 453

structure are columellae labeled by c. S4B staining reveals cellulosic rays in (E) and the antibody 454

CCRC-M36 shows deposition of rhamnogalacturonan (F). The comparison of the overlay (G) 455

with (D) exemplifies the usefulness of dyes and labels. Scale bars = 25 µm in (B to G). 456

457

458

459

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777



ADVANCES

• The advancement of spectroscopic and microscopic techniques, along with the discovery of multiple diverse proteinacious probes, has allowed the monitoring of polysaccharide dynamics in muro.

• “Click chemistry” enables the imaging of matrix polysaccharide deposition at an unprecedented resolution and is compatible with fluorescent probes directed against other wall components.

• Synthetic glycan arrays can help to identify the target epitopes of existing cell wall probes.

• Solid-state NMR provides molecular insights into the spatial localization of polysaccharides in intact plant tissues.

• Fine-tuning of polysaccharide structures in a spatiotemporal manner is essential to control the architecture of plant cell walls and can lead to distinct developmental fates.



OUTSTANDING QUESTIONS

• What relationships between morphological development and wall dynamics will be unraveled by applying the state-of-the-art imaging approaches in different biological contexts?

• How do polysaccharide structures visualized with specific techniques and probes influence cell wall architecture and properties?

• How does a cell decide to allocate carbon for the synthesis of a particular wall polymer?

• Which probes can label structurally defined motifs of individual polysaccharides, as well as of polymer complexes that occur in the plant cell wall?

• How do polysaccharides from different classes interact in the wall and how does their interplay affect polymer synthesis and assembly?

• What technical developments will overcome the current spatiotemporal limits for the in vivo monitoring of polysaccharide dynamics during cell elongation and differentiation?



Parsed CitationsAnderson CT, Carroll A, Akhmetova L, Somerville CR (2010) Real-time imaging of cellulose reorientation during cell wall expansion inArabidopsis roots. Plant Physiol 152: 787–96

Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Anderson CT, Wallace IS (2012) Illuminating the wall: using click chemistry to image pectins in Arabidopsis cell walls. Plant SignalBehav 7: 661–3


Anderson CT, Wallace IS, Somerville CR (2012) Metabolic click-labeling with a fucose analog reveals pectin delivery, architecture, anddynamics in Arabidopsis cell walls. Proc Natl Acad Sci U S A 109: 1329–1334


Atmodjo MA, Hao Z, Mohnen D (2013) Evolving Views of Pectin Biosynthesis. Annu Rev Plant Biol 64: 747–779Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Barnes WJ, Anderson CT (2017) Release, Recycle, Rebuild: Cell-Wall Remodeling, Autodegradation, and Sugar Salvage for New WallBiosynthesis during Plant Development. Mol Plant. doi: 10.1016/j.molp.2017.08.011


Blake AW, McCartney L, Flint JE, Bolam DN, Boraston AB, Gilbert HJ, Knox JP (2006) Understanding the biological rationale for thediversity of cellulose-directed carbohydrate-binding modules in prokaryotic enzymes. J Biol Chem 281: 29321–9


Brennan M, Harris PJ (2011) Distribution of fucosylated xyloglucans among the walls of different cell types in monocotyledonsdetermined by immunofluorescence microscopy. Mol Plant 4: 144–156


Carpita NC, McCann MC (2015) Characterizing visible and invisible cell wall mutant phenotypes. J Exp Bot 66: 4146–4163Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Cavalier DM, Lerouxel O, Neumetzler L, Yamauchi K, Reinecke A, Freshour G, Zabotina OA, Hahn MG, Burgert I, Pauly M, et al (2008)Disrupting two Arabidopsis thaliana xylosyltransferase genes results in plants deficient in xyloglucan, a major primary cell wallcomponent. Plant Cell 20: 1519–37


Cornuault V, Buffetto F, Rydahl MG, Marcus SE, Torode TA, Xue J, Crépeau M-JJ, Faria-Blanc N, Willats WGT, Dupree P, et al (2015)Monoclonal antibodies indicate low-abundance links between heteroxylan and other glycans of plant cell walls. Planta 242: 1321–1334


Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6: 850–61Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Cosgrove DJ (2018) Diffuse Growth of Plant Cell Walls. Plant Physiol 176: 16–27Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Cosgrove DJ (2016) Catalysts of plant cell wall loosening. F1000Research. doi: 10.12688/f1000research.7180.1Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title www.plantphysiol.orgon June 6, 2020 - Published by Downloaded from

Copyright © 2018 American Society of Plant Biologists. All rights reserved.

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http://scholar.google.com/scholar?as_q=Multidimensional solid-state NMR studies of the structure and dynamics of pectic polysaccharides in uniformly 13C-labeled Arabidopsis primary cell walls.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Dick-Perez&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Dumont M%2C Lehner A%2C Vauzeilles B%2C Malassis J%2C Marchant A%2C Smyth K%2C Linclau B%2C Baron A%2C Mas Pons J%2C Anderson CT%2C et al %282016%29 Plant cell wall imaging by metabolic click%2Dmediated labelling of rhamnogalacturonan II using azido 3%2Ddeoxy%2D d %2Dmanno%2Doct%2D2%2Dulosonic acid%2E Plant J 85%3A 437�??447&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Mravec J%2C Kracun SK%2C Rydahl MG%2C Westereng B%2C Miart F%2C Clausen MH%2C Fangel JU%2C Daugaard M%2C Van Cutsem P%2C De Fine Licht HH%2C et al %282014%29 Tracking developmentally regulated post%2Dsynthetic processing of homogalacturonan and chitin using reciprocal oligosaccharide probes%2E Development 141%3A 4841�??4850&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Mravec J%2C Kračun SK%2C Rydahl MG%2C Westereng B%2C Pontiggia D%2C De Lorenzo G%2C Domozych DS%2C Willats WGT %282017%29 An oligogalacturonide%2Dderived molecular probe demonstrates the dynamics of calcium%2Dmediated pectin complexation in cell walls of tip%2Dgrowing structures%2E Plant J 91%3A 534�??546&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Nixon BT%2C Mansouri K%2C Singh A%2C Du J%2C Davis JK%2C Lee J%2C Slabaugh E%2C Vandavasi VG%2C O�??Neill H%2C Roberts EM%2C et al %282016%29 Comparative Structural and Computational Analysis Supports Eighteen Cellulose Synthases in the Plant Cellulose Synthesis Complex%2E Sci Rep 6%3A 28696&dopt=abstract

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Rautengarten C, Usadel B, Neumetzler L, Hartmann J, Büssis D, Altmann T (2008) A subtilisin-like serine protease essential formucilage release from Arabidopsis seed coats. Plant J 54: 466–80


Rocha J, Cicéron F, de Sanctis D, Lelimousin M, Chazalet V, Lerouxel O, Breton C (2016) Structure of Arabidopsis thaliana FUT1reveals a variant of the GT-B class fold and provides insight into xyloglucan fucosylation. Plant Cell 28: 2352–2364


Röckel N, Wolf S, Kost B, Rausch T, Greiner S (2008) Elaborate spatial patterning of cell-wall PME and PMEI at the pollen tube tipinvolves PMEI endocytosis, and reflects the distribution of esterified and de-esterified pectins. Plant J 53: 133–143


Rounds CM, Lubeck E, Hepler PK, Winship LJ (2011) Propidium Iodide Competes with Ca 2+ to Label Pectin in Pollen Tubes andArabidopsis Root Hairs. Plant Physiol 157: 175–187


Ruel K, Nishiyama Y, Joseleau JP (2012) Crystalline and amorphous cellulose in the secondary walls of Arabidopsis. Plant Sci 193–194:48–61


Rui Y, Anderson CT (2016) Functional Analysis of Cellulose and Xyloglucan in the Walls of Stomatal Guard Cells of Arabidopsis. PlantPhysiol 170: 1398–419


Rui Y, Xiao C, Yi H, Kandemir B, Wang JZ, Puri VM, Anderson CT (2017) POLYGALACTURONASE INVOLVED IN EXPANSION3 Functionsin Seedling Development, Rosette Growth, and Stomatal Dynamics in Arabidopsis thaliana. Plant Cell 29: 2413–2432

Pubmed: Author and Title www.plantphysiol.orgon June 6, 2020 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

http://www.ncbi.nlm.nih.gov/pubmed?term=Pauly M%2C Keegstra K %282016%29 Biosynthesis of the Plant Cell Wall Matrix Polysaccharide Xyloglucan%2E Annu Rev Plant Biol 67%3A 235�??59&dopt=abstract

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http://search.crossref.org/?page=1&rows=2&q=Perrin RM, DeRocher AE, Bar-Peled M, Zeng W, Norambuena L, Orellana A, Raikhel N V, Keegstra K (1999) Xyloglucan fucosyltransferase, an enzyme involved in plant cell wall biosynthesis. Science (80- ) 284: 1976?9

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http://www.ncbi.nlm.nih.gov/pubmed?term=Puhlmann J%2C Bucheli E%2C Swain MJ%2C Dunning N%2C Albersheim P%2C Darvill AG%2C Hahn MG %281994%29 Generation of monoclonal antibodies against plant cell%2Dwall polysaccharides%2E I%2E Characterization of a monoclonal antibody to a terminal alpha%2D%281%2D%2D%3E2%29%2Dlinked fucosyl%2Dcontaining epitope%2E Plant Physiol 104%3A 699�??710&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Rounds CM%2C Lubeck E%2C Hepler PK%2C Winship LJ %282011%29 Propidium Iodide Competes with Ca 2%2B to Label Pectin in Pollen Tubes and Arabidopsis Root Hairs%2E Plant Physiol 157%3A 175�??187&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Rui Y%2C Xiao C%2C Yi H%2C Kandemir B%2C Wang JZ%2C Puri VM%2C Anderson CT %282017%29 POLYGALACTURONASE INVOLVED IN EXPANSION3 Functions in Seedling Development%2C Rosette Growth%2C and Stomatal Dynamics in Arabidopsis thaliana%2E Plant Cell 29%3A 2413�??2432&dopt=abstract


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monitoring polysaccharide dynamics in the plant cell wall · 1 update review 2 3 monitoring...

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