Antibody-based screening of cell wall matrix glycans in ferns reveals taxon, tissue and cell-type specific distribution patterns
© Leroux et al.; licensee BioMed Central. 2015
Received: 16 September 2014
Accepted: 1 December 2014
Published: 18 February 2015
While it is kno3wn that complex tissues with specialized functions emerged during land plant evolution, it is not clear how cell wall polymers and their structural variants are associated with specific tissues or cell types. Moreover, due to the economic importance of many flowering plants, ferns have been largely neglected in cell wall comparative studies.
To explore fern cell wall diversity sets of monoclonal antibodies directed to matrix glycans of angiosperm cell walls have been used in glycan microarray and in situ analyses with 76 fern species and four species of lycophytes. All major matrix glycans were present as indicated by epitope detection with some variations in abundance. Pectic HG epitopes were of low abundance in lycophytes and the CCRC-M1 fucosylated xyloglucan epitope was largely absent from the Aspleniaceae. The LM15 XXXG epitope was detected widely across the ferns and specifically associated with phloem cell walls and similarly the LM11 xylan epitope was associated with xylem cell walls. The LM5 galactan and LM6 arabinan epitopes, linked to pectic supramolecules in angiosperms, were associated with vascular structures with only limited detection in ground tissues. Mannan epitopes were found to be associated with the development of mechanical tissues. We provided the first evidence for the presence of MLG in leptosporangiate ferns.
The data sets indicate that cell wall diversity in land plants is multifaceted and that matrix glycan epitopes display complex spatio-temporal and phylogenetic distribution patterns that are likely to relate to the evolution of land plant body plans.
KeywordsCell wall evolution Homogalacturonan Arabinan Galactan Xyloglucan Xylan Mannan Mixed-linkage glucan Sclerenchyma
The colonisation of land was a major event in the history of plants. Subsequent widespread ecological radiation and diversification was directed by complex interactions involving the interplay between morpho-anatomical and physiological adaptations of plants and the physical and chemical changes in their environment. Many adaptations facilitated terrestrial colonisation and survival, including anchorage and water uptake, mechanical support, water transport, protection against desiccation and UV-irradiance, as well as reproduction in absence of water . Specialised tissues and cell types, especially in the vegetative body, emerged and contributed to the structural complexity of plants. As the architecture and properties of cell walls largely determine tissue/organ structure and function and consequently overall morphology, they must have played a fundamental role in the evolution and differentiation of complex body plans.
By the end of the 19th century, the combined efforts of many plant anatomists led to an increased knowledge of the anatomical complexity of land plants, resulting in the distinction of tissues and cell types that are still recognised today . These tissues are composed of cells with walls that are classed as either primary cell walls that prevent cell bursting and regulate cell expansion, or non-extendable secondary cell walls, restricted to certain cell types, which have mechanical properties resisting external forces that would lead to cell collapse. Both types of walls are structurally complex composites. In most primary cell walls a load bearing network of cellulose microfibrils is cross-linked and interspersed with complex sets of matrix glycans including those classed as hemicelluloses (xyloglucans, heteroxylans, heteromannans and mixed-linkage glucans) and the multi-domain pectic supramolecular polysaccharides [3,4]. Secondary cell walls are often reinforced with lignin and contain low amounts of pectins. Many cell wall components may display considerable heterogeneity, either in their molecular structure or in their spatio-temporal distribution in plant organs, tissues, cell-types and individual walls [3,5]. As wall components may be present in variable amounts in different cell walls at specific developmental stages, there is not always a clear distinction in molecular composition between primary and secondary cell walls . Moreover, walls may be modified in response to environmental stress or pathogen attack  and even after cell death (e.g. postmortem lignification ).
Cell walls also display remarkable diversity at the taxonomical level as the presence and/or abundance of specific wall components may vary between the major plant lineages (e.g. [9-17]; see  for a brief overview). Analysis of the early diverging fern (s.l., monilophyta) Equisetum [19,20] has indicated structurally distinct cell walls that do not fit within either the type I or type II classification that had been developed for angiosperm cell walls [21,22]. Recently, a third mannan-rich (primary) cell wall type (cell wall type III), typical of ferns was reported . Although broadly useful in reflecting major taxonomic distinctions in global compositional differences, classifications of cell wall types neglects variation in wall components between cell types within organs and most notably may not relate to all land plant species. In addition, little is known of how the range of polysaccharides found in primary and secondary cell walls relates to the evolution of specific cell wall functions and cell types.
Results and discussion
Variation in the dataset may reflect differences in developmental stage and health between plants, but also differences in extractability of specific components (e.g. lignification might hinder extraction of wall components) and tissue- and cell-type specific differences in cell wall composition. In several cases no binding of specific monoclonal antibodies (mAbs) above background was detected neither in the glycan microarray analysis, nor in the immunofluorescence analyses, indicating that the epitopes were not extracted, absent, or of (relatively) low-abundance. Therefore, if epitopes were not positively identified (indicated with “0” in the heatmaps) one cannot conclude that they are absent. Moreover, as we did not sample all organs and structures (including roots, rhizomes and laminae but also meristems and differentiating tissues) for each of the species studied, we can by no means state that certain epitopes are absent in the plant.
To understand the variation in epitope abundance we performed in situ immunolabelling experiments using the same antibodies as used for probing the glycan microarrays. As mAbs are epitope-specific and not polymer-specific, and, some epitopes might be masked by other wall components , we cannot draw any firm conclusions on general fern cell wall composition. However, immunofluorescence (IF) is a powerful tool to explore spatial patterns in glycan-epitope distribution, which is the main aim of this study.
Broad themes that became apparent in the glycan epitope analysis included the observation that the majority of the epitopes characterized in angiosperms were generally present across the assessed fern species. While we found no evidence for the presence of some epitopes including the LM7 homogalacturonan epitope that occurs at corners of intercellular spaces in angiosperms, the LM8 xylogalacturonan epitope that is detected in detaching cells and the LM9 feruloylated galactan epitope of Amaranthaceae cell walls, all other epitopes of cell wall matrix components were detected in variable (relative) amounts, and these are discussed below. As we can only show a selection of images, we chose to represent variation by selecting those images that provide most clarity with respect to general or very specific labelling patterns. In most cases we show magnifications of vascular bundles (typically xylem surrounded by phloem, pericycle and endodermis) or mechanical tissues (either sclerenchymatous or collenchymatous).
Differential occurrence of pectic homogalacturonan (HG) epitopes in ferns
Homogalacturonan (HG) is the major pectic polysaccharide in angiosperms and a range of mAbs (e.g. JIM5, JIM7, LM19 and LM20) are available that recognize subtly different methyl-esterification patterns of this polymer [25-27]. HG is an abundant component of the primary cell walls of most angiosperms, except in the grasses where the total pectic content is low . Studies have provided evidence for the presence of HGs in gymnosperms, ferns, lycophytes and charophycean green algae [9,28-30].
1,5-arabinan and 1,4-galactan epitopes associated with specific tissues and/or cell types
Analysis of the pectic component rhamnogalacturan-I (RG-I) was performed by means of the arabinan and galactan-directed mAbs LM6 and LM5, respectively. Although 1,5-arabinans and 1,4-galactans are present in the complex heterogeneous pectic polymer RG-I , 1,5-arabinan may also be a constituent of arabinogalactan proteins . RG-I is highly variable both in structure and occurrence within cell walls [34-37] and many have suggested that RG-I side chains exhibit developmentally-linked structural variation [33,38,39]. Both epitopes have been immunodetected in mature tissues of green algae , ferns [29,41] and angiosperms [37,42].
Xyloglucan epitopes associated with phloem tissues and, after unmasking, primary cell walls
Xyloglucans have a backbone of (1 → 4)-β-d-glucan units, some of which are substituted with short side chains [31,48]. The structure of xyloglucan can be highly complex, and often shows variation in different taxonomic orders in different plant groups [49,50]. LM15, binding to the XXXG-motif of xyloglucan (although it also binds to tobacco xyloglucan with a XXGG motif ), and CCRC-M1, binding to fucosylated xyloglucan were employed in this study. Xyloglucans are the most abundant hemicelluloses in primary walls of seed plants, except for grasses and other commelinid monocotyledons except for palms, where (glucurono)arabinoxylans are the major hemicelluloses [12,21,48]. They have also been detected in primary cell walls of bryophytes [9,10,51,52], lycophytes, ferns and gymnosperms [9,10,19,50] and immunolabelling experiments indicated their presence in some charophycean green algae [30,40,53].
The CCRC-M1 fucosylated xyloglucan epitope was detected in the NaOH-extracts of most leptosporangiate and eusporangiate ferns studied, but, with the exception of a very weak signal in two species, not found in the Aspleniaceae (Figures 2 and 4). Within the lycophytes, the CCRC-M1 epitope was only detected in the heterosporous Selaginella. IF confirmed these observations as CCRC-M1 was not detected in Aspleniaceae (Figure 8w, x) and widely immunodetected in other leptosporangiate ferns such as Blechnum (Figure 8y, z), treated or untreated with pectate lyase. In non-asplenioid leptosporangiate ferns, CCRC-M1 bound to phloem cell walls (Figure 8y-z), which further suggests that xyloglucan might have been important for the evolution of phloem tissues. The absence of this epitope in most asplenioid ferns indicates that its abundance or detectability is variable at family level. Although high relative amounts (compared to LM15) of the CCRC-M1 epitope were detected in our glycan array analysis, IF only revealed weak binding, even after pectate lyase pretreatment, suggesting that CCRC-M1 epitopes might be masked by other polymers than HG or are soluble and lost during antibody-incubation procedures. As the epitope was found in two out of 36 species belonging to Aspleniaceae, it is probably only present in very low amounts or in a configuration that hinders epitope access or alters extractability.
Xylan epitopes are associated with secondary cell walls but also display some distinct distribution patterns
The mAbs LM10 and LM11 both recognise unsubstituted (1 → 4)-β-xylan, but LM11 can also bind to substituted arabinoxylans . Xylans are the major cellulose-linking polysaccharides in secondary cell walls of higher plants [12,48] and are the major non-cellulosic polysaccharides in primary cell walls of commelinid monocots [12,48]. In ferns, xylans have been reported to occur in secondary cell walls [55,56]. Evidence for the presence of xylans in charophycean green algae, chlorophytes, and red algae has also been published (e.g. [53,57]). In angiosperms, LM10 and LM11 bind strongly to secondary cell walls, and pectate lyase pretreatment unmasked xylan epitopes in parenchyma, including distinct regions of collenchyma cell wall thickenings .
Mannan-epitopes are associated with sclerified secondary cell walls and are unmasked in primary cell walls after pectate lyase treatment
Mannans are mannose-rich complex heteroglycans that can occur as storage polymers, particularly in the leguminosae , or fulfil structural functions . In this study we used the LM21 antibody which is known to bind to heteromannans including glucomannan and galactomannan . Mannans appear to be very abundant in the primary cell walls of the earliest land plants such as bryophytes, lycophytes, and early-diverging ferns, and less abundant in those of leptosporangiate ferns, gymnosperms and angiosperms [9,10,60-63]. A mannan-rich primary cell wall type was proposed for ferns, based on analysis of fern laminae . Mannans have also been detected in algal species , including some of which completely lack cellulose in their cell walls [64,65]. In angiosperms, mannans (mainly glucomannans and galactoglucomannans) are usually found at low levels in secondary cell walls [12,66,67], whereas they are the major hemicelluloses in secondary cell walls of gymnosperms [12,66]. Glucomannans, in particular, give extremely tough physical characteristics to some cell walls .
Mixed-linkage glucan is detected in cell walls of fully elongated cells
The molecular probes used in this analysis have been developed to study angiosperm taxa but are clearly applicable to an analysis of fern cell walls indicating that at least some of the cell wall structures present in angiosperm cell wall polysaccharides are conserved. As cell walls are highly dynamic with their chemical composition depending on developmental and environmental cues, it is not surprising that the glycan array data set displayed variation in glycan epitope-distribution among ferns but also within Aspleniaceae. However, IF of selected species enabled identification of glycan epitopes that were recurrently detected in cell walls of specific tissues and tissue types, indicating that changes in cell wall architecture, including structural elaboration of specific polymers, are linked to the emergence and/or differentiation of specialised tissues and cell types in land plants. In all species studied we detected xyloglucan LM15 and xylan LM11 epitopes in phloem and xylem tracheid walls, respectively. The RG-I-related LM5- (galactan) and LM6-epitopes (arabinan) were found in cell walls of specific cell-types in vascular bundles in all leptosporangiate ferns. The LM21 heteromannan epitope was generally detected in cell walls of mechanical tissues that are impregnated with yellowish-brown pigments, but was also found in primary cell walls, typically after pectate lyase pretreatments. To the best of our knowledge we provided the first evidence of MLG occurrence in leptosporangiate ferns, in which we detected the highest abundance of the BS-400-3 MLG epitope in petioles with immature but fully elongated sclerenchyma tissues.
Our results also provided further evidence indicating the distinctive nature of Equisetum cell walls and indicated that only low amounts of pectic HG epitopes were detected in CDTA extracts of lycophytes. We showed that while the fucosylated xyloglucan epitope CCRC-M1, except for low amounts in two species, was not detected in the fern family Aspleniaceae, high relative amounts were found in other leptosporangiate fern species. In the same way, the CCRC-M1 epitope was detected in the heterosporous Selaginella species but not in the homosporous lycophyte Huperzia. These few examples further emphasize the complexity cell wall diversity as cell wall polysaccharides not only vary in their fine-structural details but also may display intricate spatio-temporal and phylogenetic distribution patterns.
Implications for screening cell wall diversity
The variation in cell wall composition at lower taxonomic levels raises the question which criteria should be used to select species that are representative of specific plant lineages.
An approach that combines high-throughput screening with detailed analysis of selected species, as adopted here and discussed elsewhere , partly solves this problem, allowing investigation of large numbers of samples. However, while covering as much diversity as possible is important, one also needs to take into account other sources of variation. The position of a cell wall in the plant, organ or tissue at any given developmental stage, as well as the environment in which the plant occurs all have an impact on cell wall architecture. The extent of and susceptibility to variation may be substantial as, in contrast to most animals, plants have a sedentary lifestyle. Hence, they display plastic phenotypes, resulting in often dramatic differences between conspecifics or even among organs produced by the same plant as we highlighted in this study. IF is one of the best methods to unravel such complexity allowing fine mapping of cell wall composition at different levels of organisation, from organs to cell wall microdomains at any given developmental stage. Several of our results emphasize the merits of including antibody-based techniques in cell wall comparative studies. We found that differences in epitope abundance are frequently related to the relative proportions of specific tissues with distinct cell wall composition. In addition, some components may have spatially restricted distributions and may be present in amounts that are below the detection limit of some analytical techniques. We also demonstrated variation in cell wall composition within heterogeneous tissues as well as in individual cell walls, information that is often lost during fractionation of plant cell walls for polysaccharide isolation. However, to fully understand cell wall diversity and evolution a multi-modal/-scale approach is necessary, and while in situ labelling experiments clearly have some advantages, they should ideally be complemented with biochemical analysis of fractionated cell walls to provide conclusive information on polymer structure and presence.
Seventy six fern species from 20 families and 4 species of lycophytes growing in the fern collection at the Ghent University Botanical Garden were sampled for material that was used in our glycan microarray analysis with 15 cell wall directed molecular probes (Figure 1, Supplementary information Additional file 1). In order to explore infrageneric variation a larger number of species belonging to the family Aspleniaceae (36 species) were collected.
For glycan microarray analysis of organs and tissues of Asplenium elliottii (root, rhizome, petiole, lamina, vascular bundles, sclerenchyma and cortex parenchyma parenchyma) we sampled base- mid and top section of petioles and manually isolated tissues from the petioles with single edge razor blades. First petioles were dissected longitudinally and the vascular bundles were pulled out. Second, the soft epidermis and cortical parenchyma tissues were removed by scraping them off the hard and brown-coloured sclerenchyma tissue. In a second glycan microarray analysis we sampled petioles bases only (or stems in the case of Huperzia, Selaginella, Psilotum and Equisetum) of mature plants as these organs contain ground, vascular and mechanical tissues, and their rigidity allows easy vibratome sectioning. We primarily collected material from plants cultivated in plant beds or large containers as small container size may inhibit plant growth and, hence, affect differentiation of mechanical tissues, which may influence overall cell wall composition. Material was also fixed for sectioning (see further below).
Alcohol Insoluble Residue (AIR)
Material was suspended in liquid nitrogen and homogenized to a fine powder using a mortar and pestle. Five volumes of aqueous 70% ethanol were added and the suspension samples incubated for 1 h at 4°C on a rotator, centrifuged (10,000 × g for 10 minutes) and the supernatant discarded. This procedure was repeated 5 times, before a final wash with acetone for 2 min. The AIR was then air dried.
Glycan microarray analysis
Glycan microarray profiling was performed on AIR samples as previously described . Pectins, and polymers associated with pectins, were extracted by vortexing three sample replicates, consisting of 5 mg of AIR each, with 150 μl 50 mM CDTA (1,2-Diaminocyclohexane-N,N,N’,N’-tetraacetic acid), pH 7.5 in a TissueLyser (Qiagen MM 200) at 6 shakes s-1 for 2h. After centrifuging at 12,000 × g, supernatants (CDTA-extracts) were removed and stored at 4°C. After washing the pellets with de-ionized water, they were incubated with 150 μl of 4M NaOH with 0.1% v/v NaBH4 in the TissueLyser at 6 shakes s-1 for 2h to extract hemicelluloses. After centrifuging at 12,000 × g, supernatants (NaOH-extracts) were removed again and kept at 4°C. Extracts were spotted onto nitrocellulose membranes using a Sprint microarrayer (ArrayJet, Roslin, Scotland, UK). The original extracts, plus two dilutions (1:2 and 1:5) were printed in triplicate (printing replicates). Arrays were air-dried and probed with mAbs. Briefly, after blocking with 5% w/v milk protein in PBS, arrays were incubated in primary mAbs (1:10 dilution for CCRC-M1 and LM mAbs, 1:100 for BS-400-3 mAb) for 2h at room temperature. After washing, arrays were probed with secondary antibodies conjugated to alkaline phosphatase for 1.5 h before washing and developing in a BCIP/NBT (5-bromo-4-chloro-3-indolyphosphate/nitro-blue tetrazolium chloride) substrate. Arrays were then scanned and uploaded into ImaGene 6.0 microarray analysis software (BioDiscovery, http://www.biodiscovery.com). Mean spot signals (spot signals corresponding to just one dilution value on the array were used) from the three independent experiments are presented as a heatmap with the values normalized to the highest value of the entire dataset (set to equal 100). A cut off of 5% of the highest mean signal value was imposed and values below this are represented as 0.
Indirect immunofluorescence analysis of cell wall epitopes
Materials were fixed in 4% (w/v) paraformaldehyde in 50 mM PIPES (1,4-piperazinediethanesulfonic acid), 5 mM MgSO4, and 5 mM EGTA (ethylene glycol tetraacetic acid), pH 6.9. After washing in phosphate-buffered saline (PBS), transverse 40–60 μm thick sections were cut from unembedded material using a Microm HM650V vibration microtome (Thermo Fisher Scientific, Walldorf, Germany).
List of monoclonal antibodies used in this study
partially or demethyl-esterified HG
partially methyl-esterified HG
partially or demethyl-esterified HG
non-blockwise partially methyl-esterified HG
(1 → 4)-β-galactan
(1 → 5)-α-arabinan
feruloylated (1 → 4)-β-D-galactan
XXXG-motif of xyloglucan
(1 → 4)-β-d-xylan
(1 → 4)-β-d-xylan / arabinoxylan
(1 → 3, 1 → 4)-β-d-glucan
This study was supported by grants 1515710N00 and 1524914N from the Fund for Scientific Research — Flanders, Belgium (F.W.O. — Vlaanderen). We thank Prof. Dr. M. Espeel for providing access to vibratome facilities.
- Bateman RM, Crane PR, SiMichele WA, Kenrick PR, Rowe NP, Speck T, et al. Early evolution of land plants: phylogeny, physiology, and ecology of the primary terrestrial radiation. Ann Rev Ecol System. 1998;29:263–92.View ArticleGoogle Scholar
- Evert RF. Esau's plant anatomy. Meristems, cells, and tissues of the plant body: their structure, function, and development. New Jersey: John Wiley and Sons, Inc; 2006.View ArticleGoogle Scholar
- Burton RA, Gidley MJ, Fincher GB. Heterogeneity in the chemistry, structure and function of plant cell walls. Nat Chem Biol. 2010;6:724–32.View ArticlePubMedGoogle Scholar
- Cosgrove DJ. Growth of the plant cell wall. Nat Rev Mol Cell Biol. 2005;6:850–61.View ArticlePubMedGoogle Scholar
- Knox JP. Revealing the structural and functional diversity of plant cell walls. Curr Opin Plant Biol. 2008;11:308–13.View ArticlePubMedGoogle Scholar
- Lee KJD, Marcus SE, Knox JP. Plant cell wall biology: perspectives from cell wall imaging. Mol Plant. 2011;4:212–9.View ArticlePubMedGoogle Scholar
- Knox JP. Revealing the structural and functional diversity of plant cell walls. Curr Opin Plant Biol. 2008;11:308–13.View ArticlePubMedGoogle Scholar
- Pesquet E, Zhang B, Gorzás A, Puhakainen T, Serk H, Escamez S, et al. Non-cell-autonomous postmortem lignification of tracheary elements in Zinnia elegans. Plant Cell. 2013;24:1314–28.View ArticleGoogle Scholar
- Popper ZA, Fry SC. Primary cell wall composition of bryophytes and charophytes. Ann Bot. 2003;91:1–12.View ArticlePubMed CentralPubMedGoogle Scholar
- Popper ZA, Fry SC. Primary cell wall composition of pteridophytes and spermatophytes. New Phytol. 2004;164:165–74.View ArticleGoogle Scholar
- Popper ZA, Sadler IH, Fry SC. 3-O-Methylrhamnose in lower land plant primary cell walls. Biochem Syst Ecol. 2004;32:279–89.View ArticleGoogle Scholar
- Harris PJ. Diversity in plant cell walls. In: Henry RJ, editor. Plant diversity and evolution: genotypic and phenotypic variation in higher plants. Wallingford, Oxon, UK: CAB International Publishing; 2005. p. 201–27.View ArticleGoogle Scholar
- Popper ZA. The cell walls of pteridophytes and other green plants - a review. Fern Gaz. 2006;17:315–32.Google Scholar
- Popper ZA. Evolution and diversity of green plant cell walls (invited review). Curr Opin Plant Biol. 2008;11:286–92.View ArticlePubMedGoogle Scholar
- Popper ZA, Tuohy MG. Beyond the green: understanding the evolutionary puzzle of plant and algal cell walls. Plant Physiol. 2010;153:373–83.View ArticlePubMed CentralPubMedGoogle Scholar
- Sørensen I, Domozych D, Willats WGT. How have plant cell walls evolved? Plant Physiol. 2010;153:366–72.View ArticlePubMed CentralPubMedGoogle Scholar
- Popper A, Michel G, Hervé C, Domozych D, Willats WGT, Tuohy MG, et al. Evolution and diversity of plant cell walls: from algae to flowering plants. Ann Rev Plant Biol. 2011;62:567–90.View ArticleGoogle Scholar
- Fangel JU, Ulvskov P, Knox JP, Mikkelsen MD, Harholt J, Popper ZA, Willats WG. Cell wall evolution and diversity. Front Plant Sci. 2012. doi: 10.3389/fpls.2012.00152Google Scholar
- Sørensen I, Pettolino FA, Wilson SM, Doblin MS, Johansen B, Bacic A, et al. Mixed-linkage (1 → 3), (1 → 4)-β-d-glucan is not unique to the poales and is an abundant component of Equisetum arvense cell walls. Plant J. 2008;54:510–21.View ArticlePubMedGoogle Scholar
- Fry SC, Nesselrode BHW, Miller JG, Mewburn BR. Mixed-linkage (1 → 3,1 → 4)-β-d-glucan is a major hemicellulose of Equisetum (horsetail) cell walls. New Phytol. 2008;179:104–15.View ArticlePubMedGoogle Scholar
- Carpita NC, Gibeaut DM. Structural models of primary cell walls in flowering land plants – consistency of molecular structure with the physical properties of the walls during growth. Plant J. 1993;3:1–30.View ArticlePubMedGoogle Scholar
- Carpita NC. Structure and biogenesis of the cell walls of grasses. Annu Rev Plant Physiol Plant Mol Biol. 1996;47:445–76.View ArticlePubMedGoogle Scholar
- Silva GB, Ionashiro M, Carrara TB, Crivellari AC, Tiné MAS, Prado J, et al. Cell wall polysaccharides from fern leaves: evidence for a mannan-rich Type III cell wall in Adiantum raddianum. Phytochem. 2011;72:2352–60.View ArticleGoogle Scholar
- Marcus SE, Verhertbruggen Y, Hervé C, Ordaz-Ortiz JJ, Farkas V, Pedersen HL, et al. Pectic homogalacturonan masks abundant sets of xyloglucan epitopes in plant cell walls. BMC Plant Biol. 2008;8:60. doi:https://doi.org/10.1186/1471-2229-8-60.View ArticlePubMed CentralPubMedGoogle Scholar
- Willats WGT, Orfila C, Limberg G, Buchholt HC, van Alebeek G-JWM, Voragen AGJ, et al. Modulation of the degree and pattern of methyl-esterification of pectic homogalacturonan in plant cell walls: implications for pectin methyl esterase action, matrix properties and cell adhesion. J Biol Chem. 2001;276:19404–13.View ArticlePubMedGoogle Scholar
- Clausen MH, Willats WGT, Knox JP. Synthetic methyl hexagalacturonate hapten inhibitors of anti-homogalacturonan monoclonal antibodies LM7, JIM5 and JIM7. Carb Res. 2003;338:1797–800.View ArticleGoogle Scholar
- Verhertbruggen Y, Marcus SE, Haeger A, Ordaz-Ortiz JJ, Knox JP. An extended set of monoclonal antibodies to pectic homogalacturonan. Carb Res. 2009;344:1858–62.View ArticleGoogle Scholar
- Domozych DS, Serfis A, Kiemle SN, Gretz MR. The structure and biochemistry of charophycean cell walls: I. Pectins of Penium margaritaceum. Protoplasma. 2007;230:99–115.View ArticlePubMedGoogle Scholar
- Leroux O, Knox JP, Leroux F, Vrijdaghs A, Bellefroid E, Borgonie G, et al. Intercellular pectic protuberances in Asplenium: new data on their composition and origin. Ann Bot. 2007;100:1165–73.View ArticlePubMed CentralPubMedGoogle Scholar
- Sørensen I, Pettolino FA, Bacic A, Ralph J, Lu F, O’Neill MA, et al. The charophycean green algae provide insights into the early origins of plant cell walls. Plant J. 2011;68:201–11.View ArticlePubMedGoogle Scholar
- Albersheim P, Darvill A, Roberts K, Sederoff R, Staehelin A. Plant cell walls: from chemistry to biology. New York: Garland Science; 2010.Google Scholar
- Caffel KH, Mohnen D. The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carb Res. 2009;344:1879–900.View ArticleGoogle Scholar
- Lee KJD, Sakata Y, Mau S-L, Pettolino F, Bacic A, Quatrano RS, et al. Arabinogalactan-proteins are required for apical cell extension in the moss Physcomitrella patens. Plant Cell. 2005;17:3051–65.View ArticlePubMed CentralPubMedGoogle Scholar
- Willats WGT, Marcus SE, Knox JP. Generation of a monoclonal antibody specific to (1 → 5)-β-L-arabinan. Carb Res. 1998;308:149–52.View ArticleGoogle Scholar
- Willats WGT, Steele-King CG, Marcus SE, Knox JP. Side chains of pectic polysaccharides are regulated in relation to cell proliferation and cell differentiation. Plant J. 1999;20:619–28.View ArticlePubMedGoogle Scholar
- Bush MS, McCann MC. Pectic epitopes are differentially distributed in the cell walls of potato (Solanum tuberosum) tubers. Plant Physiol. 1999;107:201–13.View ArticleGoogle Scholar
- Verhertbruggen Y, Marcus SE, Haeger A, Verhoef R, Schols A, McCleary BV, et al. Developmental complexity of arabinan polysaccharides and their processing in plant cell walls. Plant J. 2009;59:413–25.View ArticlePubMedGoogle Scholar
- Skjot M, Pauly M, Bush MS, Borkhardt B, McCann MC, Ulvskov P. Direct interference with rhamnogalacturonan I biosynthesis in Golgi vesicles. Plant Physiol. 2002;129:95–102.View ArticlePubMed CentralPubMedGoogle Scholar
- Cankar K, Kortstee A, Toonen MAJ, Wolters-Arts M, Houbein R, Mariani C, et al. Pectic arabinan side chains are essential for pollen cell wall integrity during pollen development. Plant Biotech J. 2014;12:492–502.View ArticleGoogle Scholar
- Domozych DS, Sorensen I, Pettolino A, Bacic A, Willats WGGT. The cell wall polymers of the charophycean green algae Chara corallina: Immunobinding and biochemical screening. Int J Plant Sci. 2010;171:345–61.View ArticleGoogle Scholar
- Leroux O, Knox JP, Masschaele B, Bagniewska-Zadworna A, Marcus SE, Claeys M, et al. An extensin-rich matrix lines the carinal canals in Equisetum ramosissimum, which may function as water-conducting channels. Ann Bot. 2011;108:307–19.View ArticlePubMed CentralPubMedGoogle Scholar
- Jones L, Milne JL, Ashford D, McQueen-Mason SJ. Cell wall arabinan is essential for guard cell function. Proc Natl Acad Sci U S A. 2003;100:11783–8.View ArticlePubMed CentralPubMedGoogle Scholar
- Pryer KM, Schuettpelz E, Wolf PG, Schneider H, Smith AR, Cranfill R. Phylogeny and evolution of ferns (monilophytes) with a focus on the early leptosporangiate divergences. Am J Bot. 2004;91:1582–98.View ArticlePubMedGoogle Scholar
- McCartney L, Ormerod AP, Gidley MJ, Knox JP. Temporal and spatial regulation of pectic (1 → 4)-β-d-galactan in cell walls of developing pea cotyledons: implications for mechanical properties. Plant J. 2000;22:105–13.View ArticlePubMedGoogle Scholar
- Ulvskov P, Wium H, Bruce D, Jorgensen B, Qvist KB, Skjot M, et al. Biophysical consequences of remodeling the neutral side chains of rhamnogalacturonan I in tubers of transgenic potatoes. Planta. 2005;220:609–20.View ArticlePubMedGoogle Scholar
- Verhertbruggen Y, Marcus SE, Chen J, Knox JP. Cell wall pectic arabinans influence the mechanical properties of Arabidopsis thaliana inflorescence stems and their response to mechanical stress. Plant Cell Physiol. 2013;54:1278–88.View ArticlePubMedGoogle Scholar
- McCartney L, Steele-King CG, Jordan E, Knox JP. Cell wall pectic (1 → 4)-β-d-galactan marks the acceleration of cell elongation in the Arabidopsis seedling root meristem. Plant J. 2003;33:447–54.View ArticlePubMedGoogle Scholar
- Scheller HV, Ulvskov P. Hemicelluloses. Ann Rev Plant Biol. 2010;61:263–89.View ArticleGoogle Scholar
- Hoffman M, Jia Z, Peña MJ, Cash M, Harper A, Blackburn AR, et al. Structural analysis of xyloglucans in the primary cell walls of plants in the subclass Asteridae. Carb Res. 2005;15:1826–40.View ArticleGoogle Scholar
- Hsieh Y, Harris PJ. Structures of xyloglucans in primary cell walls of gymnosperms, monilophytes (ferns sensu lato) and lycophytes. Phytochem. 2012;79:87–101.View ArticleGoogle Scholar
- Ligrone R, Vaughn KC, Renzaglia KS, Knox JP, Duckett JG. Diversity in the distribution of polysaccharide and glycoprotein epitopes in the cell walls of bryophytes: new evidence for the multiple evolution of water-conducting cells. New Phytol. 2002;156:491–508.View ArticleGoogle Scholar
- Kremer C, Pettolino F, Bacic A, Drinnan A. Distribution of cell wall components in Sphagnum hyaline cells and in liverwort and hornwort elaters. Planta. 2004;219:1023–35.View ArticlePubMedGoogle Scholar
- Domozych DS, Sorensen I, Willats WGGT. The distribution of cell wall polymers during antheridium development and spermatogenesis in the Charophycean green alga, Chara coralline. Ann Bot. 2009;104:1045–56.View ArticlePubMed CentralPubMedGoogle Scholar
- McCartney L, Marcus SE, Knox JP. Monoclonal antibodies to plant cell wall xylans and arabinoxylans. J Histochem Cytochem. 2005;53:543–6.View ArticlePubMedGoogle Scholar
- Timell TE. Studies on ferns (Filicineae). 1. The constitution of a xylan from cinnamon fern (Osmunda cinnamomea). Svensk Papperstidning. 1962;65:122–5.Google Scholar
- Carafa A, Duckett JG, Knox JP, Ligrone R. Distribution of cell-wall xylans in bryophytes and tracheophytes: new insights into basal interrelationships of land plants. New Phytol. 2005;168:231–40.View ArticlePubMedGoogle Scholar
- Lahaye M, Rondeau-Mouro C, Deniaud E, Buleon A. Solid-state C-13 NMR spectroscopy studies of xylans in the cell wall of Palmaria palmata (L. Kuntze, Rhodophyta). Carb Res. 2003;338:1559–69.View ArticleGoogle Scholar
- Hervé C, Rogowski A, Gilbert HJ, Knox JP. Enzymatic treatments reveal differential capacities for xylan recognition and degradation in primary and secondary plant cell walls. Plant J. 2009;58:413–22.View ArticlePubMedGoogle Scholar
- Buckeridge MS. Seed cell wall storage polysaccharides: models to understand cell wall biosynthesis and degradation. Plant Physiol. 2010;154:1017–23.View ArticlePubMed CentralPubMedGoogle Scholar
- Marcus SE, Blake AW, Benians TAS, Lee KJD, Poyser C, Donaldson L, et al. Restricted access of proteins to mannan polysaccharides in intact plant cell walls. Plant J. 2010;64:191–203.View ArticlePubMedGoogle Scholar
- Bailey RW, Pain V. Polysaccharide mannose in New Zealand ferns. Phytochem. 1971;10:1065–73.View ArticleGoogle Scholar
- Bremner I, Wilkie KCB. The hemicelluloses of bracken. II. A galactoglucomannan. Carb Res. 1971;20:193–203.View ArticleGoogle Scholar
- Nothnagel AL, Nothnagel AE. Primary wall structure in the evolution of land plants. J Integr Plant Biol. 2007;49:1271–8.View ArticleGoogle Scholar
- Frei E, Preston RD. Non-cellulosic structural polysaccharides in algal cell walls. III. Mannan in siphoneous green algae. Proc Roy Soc London B Biol Sci. 1968;169:127–45.View ArticleGoogle Scholar
- Preston RD. Plants without cellulose. Sci Am. 1968;216:102–8.View ArticleGoogle Scholar
- Bacic A, Harris PJ, Stone BA. Structure and function of plant cell walls. In: Preiss J, editor. The Biochemistry of Plants: A Comprehensive Treatise, vol. 14. New York: Academic Press; 1988. p. 297–371.View ArticleGoogle Scholar
- Carpita NC, McCann MC. The functions of cell wall polysaccharides in composition and architecture revealed through mutations. Plant Soil. 2002;247:71–80.View ArticleGoogle Scholar
- Harholt J, Sørensen I, Fangel J, Roberts A, Willats WGT, Scheller HV, et al. The glycosyltransferase repertoire of the spikemoss Selaginella moellendorffii and a comparative study of its cell wall. Plos One. 2012. Doi: 10.1371/journal.pone.0035846l.Google Scholar
- Xue X, Fry SC. Evolution of mixed-linkage (1 → 3,1 → 4)-β-D-glucan (MLG) and xyloglucan in Equisetum (horsetails) and other monilophytes. Ann Bot. 2012;109:873–86.View ArticlePubMed CentralPubMedGoogle Scholar
- Tretheway JA, Harris PJ. Location of (1 → 3)- and (1 → 3), (1 → 4)-β- d -glucans in vegetative cell walls of barley (Hordeum vulgare) using immunogold labelling. New Phytol. 2002;154:347–58.View ArticleGoogle Scholar
- Tretheway JA, Campbell LM, Harris PJ. (1 → 3), (1 → 4)- β-d-glucans in the cell walls of the Poales (sensu lato): an immunogold labelling study using a monoclonal antibody. Am J Bot. 2005;92:1660–74.View ArticleGoogle Scholar
- Vega-Sánchez ME, Verhertbruggen Y, Scheller HV, Ronald PC. Abundance of mixed linkage glucan in mature tissues and secondary cell walls of grasses. Plant Signal Behav. 2012;8(2):e23143.View ArticleGoogle Scholar
- Moller I, Sorensen I, Bernal AJ, Blaukopf C, Lee K, Obro J, et al. High-throughput mapping of cell-wall polymers within and between plants using novel microarrays. Plant J. 2007;50:1118–28.View ArticlePubMedGoogle Scholar
- Smith AR, Pryer KM, Schuettpelz E, Korall P, Schneider H, Wolf P. A classification for extant ferns. Taxon. 2006;55:705–31.View ArticleGoogle Scholar
- Qiu YL, Li L, Wang B, Chen Z, Dombrovska O, Lee J, et al. A nonflowering land plant phylogeny from nucleotide sequences of seven chloroplast, mitochondrial, and nuclear genes. Int J Plant Sci. 2007;168:691–708.View ArticleGoogle Scholar
- Jones L, Seymour GB, Knox JP. Localization of pectic galactan in tomato cell walls using a monoclonal antibody specific to (1 → 4)-β-D-galactan. Plant Physiol. 1997;113:1405–12.PubMed CentralPubMedGoogle Scholar
- Willats WGT, McCartney L, Steele-King CG, Marcus SE, Mort A, Huisman M, et al. A xylogalacturonan epitope is specifically associated with plant cell detachment. Planta. 2004;218:673–81.View ArticlePubMedGoogle Scholar
- Clausen MH, Ralet M-C, Willats WGT, McCartney L, Marcus SE, Thibault J-F, et al. A monoclonal antibody to feruloylated-(1 → 4)-b-d-galactan. Planta. 2004;219:1036–41.View ArticlePubMedGoogle Scholar
- Puhlmann J, Bucheli E, Swain MJ, Dunning N, Albersheim P, Darvill AG, et al. Generation of monoclonal antibodies against plant cell wall polysaccharides. I. Characterization of a monoclonal antibody to a terminal α-(1,2)-linked fucosyl-containing epitope. Plant Physiol. 1994;104:699–710.View ArticlePubMed CentralPubMedGoogle Scholar
- Meikle PJ, Hoogenraad NJ, Bonig I, Clarke AE, Stone BA. A (1 → 3,1 → 4)-β-glucan-specific monoclonal antibody and its use in the quantitation and immunocytochemical location of (1 → 3,1 → 4)-β-glucans. Plant J. 1994;5:1–9.View ArticlePubMedGoogle Scholar
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