Article

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

Received:
Accepted:
Published online:

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.

  • Subscribe to Nature Plants for full access:

    $62

    Subscribe
  • Purchase article full text and PDF:

    $32

    Buy now

Additional access options:

Already a subscriber? Log in now or Register for online access.

References

  1. 1.

    et al. Toward a systems approach to understanding plant cell walls. Science 306, 2206–2211 (2004).

  2. 2.

    & O-acetylation of plant cell wall polysaccharides. Front. Plant Sci. 3, 12 (2012).

  3. 3.

    et al. O-acetylation of Arabidopsis hemicellulose xyloglucan requires AXY4 or AXY4L, proteins with a TBL and DUF231 domain. Plant Cell 23, 4041–4053 (2011).

  4. 4.

    , , & The four Arabidopsis reduced wall acetylation genes are expressed in secondary wall-containing cells and required for the acetylation of xylan. Plant Cell Physiol. 52, 1289–1301 (2011).

  5. 5.

    et al. Loss-of-function mutation of REDUCED WALL ACETYLATION2 in Arabidopsis leads to reduced cell wall acetylation and increased resistance to Botrytis cinerea. Plant Physiol. 155, 1068–1078 (2011).

  6. 6.

    , & Xylan O-acetylation impacts xylem development and enzymatic recalcitrance as indicated by the Arabidopsis mutant tbl29. Mol. Plant 6, 1373–1375 (2013).

  7. 7.

    , , & The role of the plant-specific ALTERED XYLOGLUCAN9 protein in Arabidopsis cell wall polysaccharide O-acetylation. Plant Physiol. 167, 1271–1283 (2015).

  8. 8.

    & Plant cell wall polymers as precursors for biofuels. Curr. Opin. Plant Biol. 13, 305–312 (2010).

  9. 9.

    et al. The Arabidopsis IRX10 and IRX10-LIKE glycosyltransferases are critical for glucuronoxylan biosynthesis during secondary cell wall formation. Plant J. 57, 718–731 (2009).

  10. 10.

    et al. Comparison of five xylan synthesis mutants reveals new insight into the mechanisms of xylan synthesis. Plant J. 52, 1154–1168 (2007).

  11. 11.

    , , , & Characterization of IRX10 and IRX10-like reveals an essential role in glucuronoxylan biosynthesis in Arabidopsis. Plant J. 57, 732–746 (2009).

  12. 12.

    , , , & Two Arabidopsis proteins synthesize acetylated xylan in vitro. Plant J. 80, 197–206 (2014).

  13. 13.

    et al. The pattern of xylan acetylation suggests xylan may interact with cellulose microfibrils as a twofold helical screw in the secondary plant cell wall of Arabidopsis thaliana. Plant J. 79, 492–506 (2014).

  14. 14.

    et al. Acetylesterase-mediated deacetylation of pectin impairs cell elongation, pollen germination, and plant reproduction. Plant Cell 24, 50–65 (2012).

  15. 15.

    , , , & GDSL family of serine esterases/lipases. Prog. Lipid Res. 43, 534–552 (2004).

  16. 16.

    , , & Combining comparative sequence and genomic data to ascertain phylogenetic relationships and explore the evolution of the large GDSL-lipase family in land plants. Mol. Biol. Evol. 28, 551–565 (2011).

  17. 17.

    , , & Crystal structure of Escherichia coli thioesterase I/protease I/lysophospholipase L1: consensus sequence blocks constitute the catalytic center of SGNH-hydrolases through a conserved hydrogen bond network. J. Mol. Biol. 330, 539–551 (2003).

  18. 18.

    et al. Structure of a novel enzyme that catalyzes acyl transfer to alcohols in aqueous conditions. Biochem. J. 46, 8969–8979 (2007).

  19. 19.

    , , , & Role of a GDSL lipase-like protein as sinapine esterase in Brassicaceae. Plant J. 53, 802–813 (2008).

  20. 20.

    et al. Identification and characterization of a GDSL lipase-like protein that catalyzes the ester-forming reaction for pyrethrin biosynthesis in Tanacetum cinerariifolium- a new target for plant protection. Plant J. 71, 183–193 (2012).

  21. 21.

    & Lipase-catalysed preparation of acetates of 4-nitrophenyl β-D-xylopyranoside and their use in kinetic studies of acetyl migration. Carbohydr. Res. 339, 1353–1360 (2004).

  22. 22.

    et al. Action of xylan deacetylating enzymes on monoacetyl derivatives of 4-nitrophenyl glycosides of β-D-xylopyranose and α-L-arabinofuranose. J. Biotech. 151, 137–142 (2011).

  23. 23.

    et al. Three novel rice genes closely related to the Arabidopsis IRX9, IRX9L, and IRX14 genes and their roles in xylan biosynthesis. Front. Plant Sci. 4, 83 (2013).

  24. 24.

    et al. VASCULAR-RELATED NAC-DOMAIN6 and VASCULAR-RELATED NAC-DOMAIN7 effectively induce transdifferentiation into xylem vessel elements under control of an induction system. Plant Physiol. 153, 906–914 (2010).

  25. 25.

    Microbial carbohydrate esterases deacetylating plant polysaccharides. Biotechnol. Adv. 30, 1575–1588 (2012).

  26. 26.

    & Secondary cell wall patterning during xylem differentiation. Curr. Opin. Plant Biol. 15, 38–44 (2012).

  27. 27.

    & Initiation of cell wall pattern by a Rho- and microtubule-driven symmetry breaking. Science 337, 1333–1336 (2012).

  28. 28.

    et al. GUX1 and GUX2 glucuronyltransferases decorate distinct domains of glucuronoxylan with different substitution patterns. Plant J. 74, 423–434 (2013).

  29. 29.

    et al. Variation in NRT1.1B contributes to nitrate-use divergence between rice subspecies. Nat. Genet. 47, 834–838 (2015).

  30. 30.

    , , , & MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725–2729 (2013).

  31. 31.

    et al. Plant N-glycan processing enzymes employ different targeting mechanisms for their spatial arrangement along the secretory pathway. Plant Cell 18, 3182–3200 (2006).

  32. 32.

    et al. Golgi nucleotide sugar transporter modulates cell wall biosynthesis and plant growth in rice. Proc. Natl Acad. Sci. USA 108, 5110–5115 (2011).

  33. 33.

    et al. AtABCA9 transporter supplies fatty acids for lipid synthesis to the endoplasmic reticulum. Proc. Natl Acad. Sci. USA 110, 773–778 (2013).

  34. 34.

    et al. Two trichome birefringence-like proteins mediate xylan acetylation, which is essential for leaf blight resistance in rice. Plant Physiol. 173, 470–481 (2017).

  35. 35.

    & Preparation of plant cells for transmission electron microscopy to optimize immunogold labeling of carbohydrate and protein epitopes. Nat. Protoc. 7, 1716–1727 (2012).

  36. 36.

    Semimicro determination of cellulose in biological materials. Anal. Biochem. 32, 420–424 (1969).

  37. 37.

    , , & Identification and functional characterization of the distinct plant pectin esterases PAE8 and PAE9 and their deletion mutants. Planta 240, 1123–1138 (2014).

  38. 38.

    , , & Whole plant cell wall characterization using solution-state 2D NMR. Nat. Protoc. 7, 1579–1589 (2012).

  39. 39.

    et al. Glycosyl transferases in family 61 mediate arabinofuranosyl transfer onto xylan in grasses. Proc. Natl Acad. Sci. USA 109, 989–993 (2012).

  40. 40.

    et al. A gibberellin-mediated DELLA-NAC signaling cascade regulates cellulose synthesis in rice. Plant Cell 27, 1681–1696 (2015).

Download references

Author information

Author notes

    • Feng Li

    Present address: Shanghai Center for Plant Stress Biology, Chinese Academy of Sciences, Shanghai 201602, China

    • Baocai Zhang
    • , Lanjun Zhang
    •  & Feng Li

    These authors contributed equally to this work

Affiliations

  1. State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China

    • Baocai Zhang
    • , Lanjun Zhang
    • , Feng Li
    • , Dongmei Zhang
    • , Xiangling Liu
    • , Hang Wang
    • , Zuopeng Xu
    • , Chengcai Chu
    •  & Yihua Zhou
  2. University of Chinese Academy of Sciences, Beijing 100049, China

    • Lanjun Zhang
    • , Dongmei Zhang
    • , Hang Wang
    • , Chengcai Chu
    •  & Yihua Zhou

Authors

  1. Search for Baocai Zhang in:

  2. Search for Lanjun Zhang in:

  3. Search for Feng Li in:

  4. Search for Dongmei Zhang in:

  5. Search for Xiangling Liu in:

  6. Search for Hang Wang in:

  7. Search for Zuopeng Xu in:

  8. Search for Chengcai Chu in:

  9. Search for Yihua Zhou in:

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.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Chengcai Chu or Yihua Zhou.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    Supplementary Figures 1–11, Supplementary Tables 1 and 2.