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Control of secondary cell wall patterning involves xylan deacetylation by a GDSL esterase

Abstract

O-acetylation, a ubiquitous modification of cell wall polymers, has striking impacts on plant growth and biomass utilization and needs to be tightly controlled. However, the mechanisms that underpin the control of cell wall acetylation remain elusive. Here, we show a rice brittle leaf sheath1 (bs1) mutant, which contains a lesion in a Golgi-localized GDSL esterase that deacetylates the prominent hemicellulose xylan. Cell wall composition, detailed xylan structure characterization and enzyme kinetics and activity assays on acetylated sugars and xylooligosaccharides demonstrate that BS1 is an esterase that cleaves acetyl moieties from the xylan backbone at O-2 and O-3 positions of xylopyranosyl residues. BS1 thus plays an important role in the maintenance of proper acetylation level on the xylan backbone, which is crucial for secondary wall formation and patterning. Our findings outline a mechanism for how plants modulate wall acetylation and endow a plethora of uncharacterized GDSL esterases with surmisable activities.

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Figure 1: Map-based cloning of the BS1 gene.
Figure 2: BS1 is localized in the Golgi apparatus and has esterase activity.
Figure 3: The bs1 mutants have increased acetate level on xylan backbone.
Figure 4: Enzyme activity assays of BS1.
Figure 5: BS1 is expressed in vascular bundles.
Figure 6: BS1 affects secondary wall pattern in vessels and agronomic traits.

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (NSFC, 31530051) and the Ministry of Sciences and Technology of China (2013CB127001), NSFC (31571247), Chinese Academy of Sciences (CAS) grants for XDA08010103 and Youth Innovation Promotion Association CAS (2016094), as well as the State Key Laboratory of Plant Genomics. We thank K. Hu, L. Xu, X. Liu and S. Zang for technical support on NMR analyses, W. Yang for help with laser microdissection and S. Persson and V. Chiang for comments on the manuscript.

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Authors and Affiliations

Authors

Contributions

Y.Z. and C.C. conceived the study; F.L. performed map-based cloning and complementary assays; B.Z. and L.Z. performed all the chemical and biochemical assays in the study and analysed the data; D.Z. performed subcellular localization experiments; H.W. performed western blotting and polyacrylamide gel electrophoresis analyses; X.L. and Z.X. performed gene transformation and field observation; Y.Z. and B.Z. wrote the article. B.Z., L.Z. and F.L. share equal first authorship.

Corresponding authors

Correspondence to Chengcai Chu or Yihua Zhou.

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The authors declare no competing financial interests.

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Supplementary Figures 1–11, Supplementary Tables 1 and 2. (PDF 2230 kb)

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Zhang, B., Zhang, L., Li, F. et al. Control of secondary cell wall patterning involves xylan deacetylation by a GDSL esterase. Nature Plants 3, 17017 (2017). https://doi.org/10.1038/nplants.2017.17

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