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Complete substitution of a secondary cell wall with a primary cell wall in Arabidopsis

Nature Plants volume 4, pages 777–783 (2018)Cite this article

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Abstract

The bulk of a plant’s biomass, termed secondary cell walls, accumulates in woody xylem tissues and is largely recalcitrant to biochemical degradation and saccharification1. By contrast, primary cell walls, which are chemically distinct, flexible and generally unlignified2, are easier to deconstruct. Thus, engineering certain primary wall characteristics into xylem secondary walls would be interesting to readily exploit biomass for industrial processing. Here, we demonstrated that by expressing AP2/ERF transcription factors from group IIId and IIIe in xylem fibre cells of mutants lacking secondary walls, we could generate plants with thickened cell wall characteristics of primary cell walls in the place of secondary cell walls. These unique, newly formed walls displayed physicochemical and ultrastructural features consistent with primary walls and had gene expression profiles illustrative of primary wall synthesis. These data indicate that the group IIId and IIIe AP2/ERFs are transcription factors regulating primary cell wall deposition and could form the foundation for exchanging one cell wall type for another in plants.

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Fig. 1: Accumulation of lignin-deficient cell walls by ERF035-VP16 plants.
Fig. 2: ERF035 is sufficient to activate primary cell wall formation.
Fig. 3: Induced cell walls in nst1 nst3 NST3pro::ERF035-VP16 plant stems are similar to primary cell walls.
Fig. 4: Typical primary cell wall structures are deposited in induced fibre cell walls of nst1 nst3 NST3pro::ERF035-VP16 plants.

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Data availability

The microarray data in this study were deposited to the NCBI GEO under the accession number GSE81039. Other data that support the findings of this study are available from the corresponding author upon reasonable request. Figures 1l–o, 2b,d and 3a,b,d–f and Supplementary Figs. 3, 4, 7c, 10, 11, 14–18, 21 and 22 have associated raw data.

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Acknowledgements

We thank A. Hosaka, A. Kuwazawa, F. Tobe, M. Yamada, Y. Sugimoto and Y. Takiguchi for their technical support. This work was supported by the JST ALCA program (grant no. JPMJAL1107) (to N.M.), a postdoctoral fellowship from the German Research Foundation (DFG, project 344523413) (to M.S.), University of Melbourne R@MAP Professorship, an ARC Future Fellowship grant (FT160100218) and a UoM IRRTF RNC grant (501892) (to S.P.) and an NSERC Discovery Grant (to S.D.M.).

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Authors and Affiliations

  1. Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Ibaraki, Japan

    Shingo Sakamoto, Miyuki T. Nakata & Nobutaka Mitsuda

  2. School of Biosciences, University of Melbourne, Parkville, Melbourne, Victoria, Australia

    Marc Somssich & Staffan Persson

  3. Department of Wood Science, Faculty of Forestry, University of British Columbia, Vancouver, British Columbia, Canada

    Faride Unda & Shawn D. Mansfield

  4. Graduate School of Science and Engineering, Saitama University, Saitama, Japan

    Kimie Atsuzawa & Yasuko Kaneko

  5. Max-Planck Institute for Molecular Plant Physiology, Potsdam, Germany

    Ting Wang

  6. Department of Plant Biology and Genome Center, University of California, Davis, Davis, CA, USA

    Anne-Maarit Bågman, Allison Gaudinier & Siobhan M. Brady

  7. Technology Center, Taisei Corporation, Yokohama, Japan

    Kouki Yoshida

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  1. Shingo Sakamoto
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Contributions

N.M. conceived and executed the project as principal investigator. N.M. and S.S. designed the experimental plans. K.Y. performed the tensile test and microarray data analysis. S.P. and S.D.M. designed the experiment related to CoMPP and cellulose analyses. S.S. performed all of the experiments except for CoMPP, cellulose analyses, TEM imaging and the yeast one-hybrid assay. M.S. performed the CoMPP analysis with the supervision of S.P. M.T.N. observed the root of the 35Spro::ERF035 plant. F.U. and S.D.M. performed the cellulose analyses. T.W., A.-M.B. and A.G. performed the yeast one-hybrid assay and its preparation. S.M.B. and S.P. designed and supervised the yeast one-hybrid assay. K.A. and Y.K. performed the TEM imaging, preparation of the thin section and the analysis of images. S.S., S.P. and N.M. mainly wrote the manuscript, with all other authors contributing to revisions.

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Correspondence to Nobutaka Mitsuda.

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The authors declare no competing interests.

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Supplementary information

Supplementary Information

Supplementary Methods, Supplementary References and Supplementary Figures 1–25.

Reporting Summary

Supplementary Table 1

Over-represented cell-wall-related GO terms in up-regulated genes in nst1 nst3 NST3pro:ERF035-VP16 plants.

Supplementary Table 2

Fold changes of cell wall-related genes in NST3p:ERF035-VP16 nst1 nst3 as per nst1 nst3.

Supplementary Table 3

Fold changes of cell wall-related genes in NST3p:ERF035-VP16 nst1 nst3 as per nst1 nst3 and in wt as per nst1 nst3.

Supplementary Table 4

List of upregulated genes related to cell wall biosynthesis in the nst1 nst3 NST3pro:ERF035-VP16 transgenic plants.

Supplementary Table 5

Over-represented cell-wall-related GO terms in putative target genes of group IIId and IIIe ERFs.

Supplementary Table 6

Primers in this study.

Supplementary Table 7

All transcription factor genes focused in this study.

Supplementary Table 8

Amino acid sequences of conserved domain used for constructing phylogenetic tree shown in Supplementary Fig. 25.

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Sakamoto, S., Somssich, M., Nakata, M.T. et al. Complete substitution of a secondary cell wall with a primary cell wall in Arabidopsis. Nature Plants 4, 777–783 (2018). https://doi.org/10.1038/s41477-018-0260-4

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