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Structural Diversity of Xylans in the Cell Walls of Monocots

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Structural Diversity of Xylans in the Cell Walls of Monocots Planta DOI 10.1007/s00425-016-2527-1 ORIGINAL ARTICLE Structural diversity of xylans in the cell walls of monocots 1 1,4 1 2 Maria J. Pen˜a • Ameya R. Kulkarni • Jason Backe • Michael Boyd • 1 1,3 Malcolm A. O’Neill • William S. York Received: 10 February 2016 / Accepted: 8 April 2016 Ó Springer-Verlag Berlin Heidelberg 2016 Abstract Asparagales glucuronoxylans. Glucuronoarabinoxylans Main conclusion Xylans in the cell walls of monocots were the only xylans detected in the cell walls of five are structurally diverse. Arabinofuranose-containing different members of the Poaceae family (grasses). By glucuronoxylans are characteristic of commelinids. contrast, both glucuronoxylan and glucuronoarabinoxylan However, other structural features are not correlated are formed by the Zingiberales and Commelinales (com- with the major transitions in monocot evolution. melinids). At least one species of each monocot order, including the Poales, forms xylan with the reducing end Most studies of xylan structure in monocot cell walls have sequence -4)-b-D-Xylp-(1,3)-a-L-Rhap-(1,2)-a-D-GalpA- emphasized members of the Poaceae (grasses). Thus, there (1,4)-D-Xyl first identified in eudicot and gymnosperm is a paucity of information regarding xylan structure in glucuronoxylans. This sequence was not discernible in the other commelinid and in non-commelinid monocot walls. arabinopyranose-containing glucuronoxylans of the Alis- Here, we describe the major structural features of the matales and Asparagales or the glucuronoarabinoxylans of xylans produced by plants selected from ten of the twelve the Poaceae. Rather, our data provide additional evidence monocot orders. Glucuronoxylans comparable to eudicot that in Poaceae glucuronoarabinoxylan, the reducing end secondary wall glucuronoxylans are abundant in non- xylose residue is often substituted at O-2 with 4-O-methyl commelinid walls. However, the a-D-glucuronic acid/4-O- glucuronic acid or at O-3 with arabinofuranose. The vari- methyl-a-D-glucuronic acid is often substituted at O-2 by ations in xylan structure and their implications for the an a-L-arabinopyranose residue in Alismatales and evolution and biosynthesis of monocot cell walls are discussed. M. J. Pen˜a and A. R. Kulkarni contributed equally to this study. Keywords Monocot Á Cell wall Á Electronic supplementary material The online version of this Glucuronoarabinoxylan Á Glucuronoxylan article (doi:10.1007/s00425-016-2527-1) contains supplementary material, which is available to authorized users. Abbreviations & William S. York AGX Arabinoglucuronoxylan [email protected] AIR Alcohol-insoluble residue Araf Arabinofuranose 1 Complex Carbohydrate Research Center and US Department of Energy Bioenergy Science Center, University of Georgia, Arap Arabinopyranose Athens, GA 30602, USA 2AB 2-Aminobenzamide 2 Department of Plant Biology, University of Georgia, Athens, GlcpA Glucuronic acid GA 30602, USA MeGlcpA4-O-Methyl glucuronic acid 13 3 Department of Biochemistry and Molecular Biology, C NMR Carbon nuclear magnetic resonance University of Georgia, Athens, GA 30602, USA spectroscopy 4 Present Address: Incyte Corporation, Wilmington, DE 19803, GAX Glucuronoarabinoxylan USA GX Glucuronoxylan 123 Planta 1H NMR Proton nuclear magnetic resonance Herve´ et al. 2009). By contrast, glucuronoarabinoxylan spectroscopy (GAX) is the predominant non-cellulosic polysaccharide in MALDI-TOF MS matrix-assisted laser desorption time- the type II primary walls of the Poaceae (commelinids), of-flight mass spectrometry which contain relatively small amounts of pectin and Xylp Xylopyranose xyloglucan (Smith and Harris 1999; Gibeaut et al. 2005). The walls of the Poaceae are further distinguished by the presence of variable amounts of (1-3,1-4)-linked b-glucans (Carpita and Gibeaut 1993; Smith and Harris 1999). The limited data available suggest that the primary cell walls of Introduction other commelinids have characteristics of both type I and type II walls. Plant cells are enclosed in a polysaccharide-rich Xylans are the major hemicellulosic polysaccharide macrostructure referred to as the cell wall. The composi- present in the secondary (lignified) cell walls of flowering tion of these walls varies considerably depending on the plants. These xylans are classified according to the type type and developmental stage of the cell that they sur- and abundance of the substituents on the 1,4-linked b-D- rounded (Fangel et al. 2012). Cells in growing tissues have Xylp residues of the polysaccharide backbone (Fig. 1a). non-lignified primary walls with a polysaccharide compo- Glucuronoxylans (GX), which are major components of the sition that differs from the lignified secondary walls of secondary walls of woody and herbaceous eudicots, have vascular and woody tissues. Additional diversity in cell a-D-glucuronic acid (GlcpA) or 4-O-methyl a-D-glucuronic wall composition also exists between different taxonomic acid (MeGlcpA) substituents at O-2 (Ebringerova et al. groups, most notably in the monocots. This diverse group 2005). The secondary wall GAX of the Poaceae and other of land plants, which includes species of economic and commelinids contains a-L-Araf residues at O-3, which ecological importance, is comprised of approximately account for the bulk of the backbone substituents, along 65,000 species that are distributed in 12 orders (Bremer with a small number of GlcpA or MeGlcpA substituents at et al. 2009; Givnish et al. 2010). Studies by Harris and O-2. The a-L-Araf residues may be further substituted at O- Hartley showed that the monocots could be divided into 2 with a a-L-Araf or a b-D-Xylp residues (Saulnier et al. two groups based on the presence or absence of ester- 1995). The GAX in the primary walls of Poaceae typically linked ferulic and coumaric acid in their primary walls contains more Araf substituents. The Araf residues of GAX (Harris and Hartley 1980). Monocots with primary walls in Poaceae primary and secondary cells walls are often that contain ferulate/coumarate comprise the commelinid esterified with ferulic or coumaric acids (Buanafina 2009). clade (Chase et al. 1993). This clade consists of the Poales, The GX and AGX in the secondary walls of eudicots which includes the Poaceae (grasses), Cyperaceae (sedges), and gymnosperms have a well-defined glycosyl sequence - and Bromeliaceae (bromeliads), together with the Zingib- 4)-b-D-Xylp-(1,3)-a-L-Rhap-(1,2)-a-D-GalpA-(1,4)-D- erales, Commelinales, and the basal Arecales (palms) Xylp (sequence 1 in Fig. 1b) at their reducing end (Jo- (Givnish et al. 2010). The Dasypogonaceae are also con- hansson and Samuelson 1977; Pen˜a et al. 2007). This sidered to be commelinids but their relationship to other sequence is required for normal GX synthesis during sec- members of the clade has not been resolved (Chase et al. ondary cell wall formation and has been proposed to have a 2006). Ferulic acid esters are absent in the primary cell role in regulating xylan chain length (Pen˜a et al. 2007; walls of the non-commelinid monocots, which are a para- York and O’Neill 2008). However, no sequence 1 has been phyletic group consisting of the Asparagales, Liliales, detected at reducing end of Poaceae GAX (Kulkarni et al. Pandanales, Dioscoreales, Petrosaviales, Alismatales, and 2012a). Rather, in wheat endosperm GAX, the reducing Acorales. The Acorales are believed to be sister to all the end xylose has been reported to be often substituted at O-3 monocots (Bremer et al. 2009; Givnish et al. 2010). with an a-L-Araf residue or at O-2 with a a-D-GlcpA Commelinid and non-commelinid primary cell walls residue (Ratnayake et al. 2014). It is not known whether also differ in the type and abundance of their non-cellulosic sequence 1 is conserved in other commelinid and non- polysaccharides. These differences led to the recognition of commelinid monocot heteroxylans. at least two types of primary wall (Bacic et al. 1988; Most studies of the composition and structure of Carpita and Gibeaut 1993; Carpita 1996; Harris et al. monocot cell walls have emphasized model plants or plants 1997). In the so-called type I primary walls of eudicots and of economic importance rather than phylogenetic diversity. non-commelinid monocots, pectin and xyloglucan account Here, we describe the major structural features of xylans for the bulk of the non-cellulosic polysaccharides. Small isolated from the cell walls of plants representing 10 of the amounts of xylan have also been reported to be present in 12 monocot orders. Cell walls were isolated from the entire these walls (Darvill et al. 1980; Zablackis et al. 1995; actively growing aerial portions of each plant with a major 123 Planta Fig. 1 Structural features of a Side chains identified in monocot xylans monocot xylans. a (i) GlcA- and MeGlcA-containing acidic side chains are present in the xylans (i) α-D-GlcpA-(1→2) 4-O-Methyl-α-D-GlcpA-(1→2)- of all monocots. (ii) Side chains containing Arap are most (ii) α-L-Arap-(1→2)-α-GlcpA-(1→2)- α-L-Arap-(1→2)-4-O-Methyl-α-D-GlcpA-(1→2)- abundant in the xylan of the Asparagales and Alismatales. (iii) α-L-Araf-(1→3)- The GlcA is 4-O-methylated in the Asparagales and Eucalyptus grandis xylans. (iii) (iv) α-L-Araf-(1→2)-α-L-Araf-(1→3)- β-D-Xylp-(1→2)-α-L-Araf-(1→3)- Monoglycosyl Araf side chains are present in GAX from b Reducing end sequences in identified in monocot xylans commelinids. (iv) Side chains in which the Araf is substituted were detected only in the Poales (v) R1→4)-β-D-Xylp-(1→4)-β-D-Xylp-(1→3)-α-LRhap- (1→2)-α-D-GalpA-(1→4)-D-Xyl~OH GAX. b Reducing end glycosyl sequences. (v) Sequence 1 has Sequence 1 been detected in the xylans from numerous seed plants, except (vi) R →4)-β-D-Xylp-(1→4)-β-D-Xylp-(1→4)-D-Xyl~OH the Poaceae.
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