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Structural diversity of xylans in the cell walls of monocots

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Abstract

Main conclusion

Xylans in the cell walls of monocots are structurally diverse. Arabinofuranose-containing glucuronoxylans are characteristic of commelinids. However, other structural features are not correlated with the major transitions in monocot evolution.

Most studies of xylan structure in monocot cell walls have emphasized members of the Poaceae (grasses). Thus, there is a paucity of information regarding xylan structure in other commelinid and in non-commelinid monocot walls. Here, we describe the major structural features of the xylans produced by plants selected from ten of the twelve monocot orders. Glucuronoxylans comparable to eudicot secondary wall glucuronoxylans are abundant in non-commelinid walls. However, the α-d-glucuronic acid/4-O-methyl-α-d-glucuronic acid is often substituted at O-2 by an α-l-arabinopyranose residue in Alismatales and Asparagales glucuronoxylans. Glucuronoarabinoxylans were the only xylans detected in the cell walls of five different members of the Poaceae family (grasses). By contrast, both glucuronoxylan and glucuronoarabinoxylan are formed by the Zingiberales and Commelinales (commelinids). At least one species of each monocot order, including the Poales, forms xylan with the reducing end sequence -4)-β-d-Xylp-(1,3)-α-l-Rhap-(1,2)-α-d-GalpA-(1,4)-d-Xyl first identified in eudicot and gymnosperm glucuronoxylans. This sequence was not discernible in the arabinopyranose-containing glucuronoxylans of the Alismatales and Asparagales or the glucuronoarabinoxylans of the Poaceae. Rather, our data provide additional evidence that in Poaceae glucuronoarabinoxylan, the reducing end xylose residue is often substituted at O-2 with 4-O-methyl glucuronic acid or at O-3 with arabinofuranose. The variations in xylan structure and their implications for the evolution and biosynthesis of monocot cell walls are discussed.

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Abbreviations

AGX:

Arabinoglucuronoxylan

AIR:

Alcohol-insoluble residue

Araf :

Arabinofuranose

Arap :

Arabinopyranose

2AB:

2-Aminobenzamide

GlcpA:

Glucuronic acid

MeGlcpA:

4-O-Methyl glucuronic acid

13C NMR:

Carbon nuclear magnetic resonance spectroscopy

GAX:

Glucuronoarabinoxylan

GX:

Glucuronoxylan

1H NMR:

Proton nuclear magnetic resonance spectroscopy

MALDI-TOF:

MS matrix-assisted laser desorption time-of-flight mass spectrometry

Xylp :

Xylopyranose

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Acknowledgments

This research was funded by the BioEnergy Science Center (BESC). BESC is a U.S. Department of Energy Bioenergy Research Center supported by the Office of Biological and Environmental Research in the DOE Office of Science. We also acknowledge the U.S. Department of Energy-funded Center for Plant and Microbial Complex Carbohydrates (Grant DE-FG02-93ER20097) for equipment support.

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Author notes

  1. Ameya R. Kulkarni

    Present address: Incyte Corporation, Wilmington, DE, 19803, USA

Authors and Affiliations

  1. Complex Carbohydrate Research Center and US Department of Energy Bioenergy Science Center, University of Georgia, Athens, GA, 30602, USA

    Maria J. Peña, Ameya R. Kulkarni, Jason Backe, Malcolm A. O’Neill & William S. York

  2. Department of Plant Biology, University of Georgia, Athens, GA, 30602, USA

    Michael Boyd

  3. Department of Biochemistry and Molecular Biology, University of Georgia, Athens, GA, 30602, USA

    William S. York

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  1. Maria J. Peña
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Correspondence to William S. York.

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M. J. Peña and A. R. Kulkarni contributed equally to this study.

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Peña, M.J., Kulkarni, A.R., Backe, J. et al. Structural diversity of xylans in the cell walls of monocots. Planta 244, 589–606 (2016). https://doi.org/10.1007/s00425-016-2527-1

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