Xylan-based nanocompartments orchestrate plant vessel wall patterning

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  • Hang Wang
  • Hanlei Yang
  • Zhao Wen
  • Chengxu Gao
  • Yihong Gao
  • Yanbao Tian
  • Zuopeng Xu
  • Xiangling Liu
  • Persson, Staffan
  • Baocai Zhang
  • Yihua Zhou

Nanoclustering of biomacromolecules allows cells to efficiently orchestrate biological processes. The plant cell wall is a highly organized polysaccharide network but is heterogeneous in chemistry and structure. However, polysaccharide-based nanocompartments remain ill-defined. Here, we identify a xylan-rich nanodomain at pit borders of xylem vessels. We show that these nanocompartments maintain distinct wall patterns by anchoring cellulosic nanofibrils at the pit borders, critically supporting vessel robustness, water transport and leaf transpiration. The nanocompartments are produced by the activity of IRREGULAR XYLEM (IRX)10 and its homologues, which we show are de novo xylan synthases. Our study hence outlines a mechanism of how xylans are synthesized, how they assemble into nanocompartments and how the nanocompartments sustain cell wall pit patterning to support efficient water transport throughout the plant body.

OriginalsprogEngelsk
TidsskriftNature Plants
Vol/bind8
Udgave nummer3
Sider (fra-til)295-306
Antal sider12
ISSN2055-026X
DOI
StatusUdgivet - 2022

Bibliografisk note

Funding Information:
We thank S. Zhang and L. Wang for the kind help with AFM, A. Wu for providing seeds of Arabidopsisirx mutants, X. Fu for help with examining transpiration potential of rice plants, X. He for help with VISUAL, Y. Wu for help with MST assay, Q. Qian and D. Zeng for providing the core rice accessions, Q. Liu and S. Tang for support with field trials and C. Zheng for help with the model drawing. The super-resolution microscopy analysis was performed at the Bio-imaging Facility, Institute of Genetics and Developmental Biology, Chinese Academy of Science (CAS). This work was supported by the National Nature Science Foundation of China (grant nos. 32030077 and 31922006) to Y.Z. and B.Z., CAS grants no. XDA24010102 to Y.Z. and Youth Innovation Promotion Association CAS (Y202030) to B.Z., as well as the State Key Laboratory of Plant Genomics to Y.Z. S.P. acknowledges grants from the Australian Research Council (DP190101941), Velux (Villum Investigator grant no. 25915), Novo Nordisk (laureate grant no. NNF19OC0056076) and the Danish National Research Foundation (chair grant no. DNRF155).

Funding Information:
We thank S. Zhang and L. Wang for the kind help with AFM, A. Wu for providing seeds of Arabidopsis irx mutants, X. Fu for help with examining transpiration potential of rice plants, X. He for help with VISUAL, Y. Wu for help with MST assay, Q. Qian and D. Zeng for providing the core rice accessions, Q. Liu and S. Tang for support with field trials and C. Zheng for help with the model drawing. The super-resolution microscopy analysis was performed at the Bio-imaging Facility, Institute of Genetics and Developmental Biology, Chinese Academy of Science (CAS). This work was supported by the National Nature Science Foundation of China (grant nos. 32030077 and 31922006) to Y.Z. and B.Z., CAS grants no. XDA24010102 to Y.Z. and Youth Innovation Promotion Association CAS (Y202030) to B.Z., as well as the State Key Laboratory of Plant Genomics to Y.Z. S.P. acknowledges grants from the Australian Research Council (DP190101941), Velux (Villum Investigator grant no. 25915), Novo Nordisk (laureate grant no. NNF19OC0056076) and the Danish National Research Foundation (chair grant no. DNRF155).

Publisher Copyright:
© 2022, The Author(s), under exclusive licence to Springer Nature Limited.

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