Published May 20, 2024 | Published
Journal Article Open

Xyloglucan deficiency leads to a reduction in turgor pressure and changes in cell wall properties, affecting early seedling establishment

Abstract

Xyloglucan is believed to play a significant role in cell wall mechanics of dicot plants. Surprisingly, Arabidopsis plants defective in xyloglucan biosynthesis exhibit nearly normal growth and development. We investigated a mutant line, cslc-Δ5, lacking activity in all five Arabidopsis cellulose synthase like-C (CSLC) genes responsible for xyloglucan backbone biosynthesis. We observed that this xyloglucan-deficient line exhibited reduced cellulose crystallinity and increased pectin levels, suggesting the existence of feedback mechanisms that regulate wall composition to compensate for the absence of xyloglucan. These alterations in cell wall composition in the xyloglucan-absent plants were further linked to a decrease in cell wall elastic modulus and rupture stress, as observed through atomic force microscopy (AFM) and extensometer-based techniques. This raised questions about how plants with such modified cell wall properties can maintain normal growth. Our investigation revealed two key factors contributing to this phenomenon. First, measurements of turgor pressure, a primary driver of plant growth, revealed that cslc-Δ5 plants have reduced turgor, preventing the compromised walls from bursting while still allowing growth to occur. Second, we discovered the conservation of elastic asymmetry (ratio of axial to transverse wall elasticity) in the mutant, suggesting an additional mechanism contributing to the maintenance of normal growth. This novel feedback mechanism between cell wall composition and mechanical properties, coupled with turgor pressure regulation, plays a central role in the control of plant growth and is critical for seedling establishment in a mechanically challenging environment by affecting shoot emergence and root penetration.

    Copyright and License

    © 2024 The Authors. Published by Elsevier Under a Creative Commons license.

    Acknowledgement

    This work was supported by grants from the National Institutes of Health (grants GM145298 and GM067203 to W.M.G.) and the Gatsby Charitable Trust (GAT3731/DAA to E.M.M.). The Meyerowitz Laboratory has funding from the Howard Hughes Medical Institute. S.R. is funded by the Royal Society URF URF\R1\180196 and the Gatsby Charitable Foundation GAT3731/GLJ. L.S. is funded by the Leverhulme Trust RPG-2022-111. H.J. is funded by the Gatsby Charitable Foundation GAT3395-PR4B. We gratefully acknowledge Professor Nigel Scrutton for generously providing the carbohydrate-binding modules essential for this research. We extend our appreciation to the University of Minnesota Imaging Center (UIC SCR_020997) and the Sainsbury Laboratory Cambridge University Microscopy Facility for their invaluable resources. Our gratitude also goes to Dr. Raymond Wightman for microscopy assistance. We are thankful to the Arabidopsis Biological Resource Center (ABRC) for supplying the T-DNA insertion mutants and Professor Olga Zabotina for providing the xxt1/xxt2 mutant line. Additionally, our heartfelt thanks go to Professor Kenneth Keegstra for his insightful feedback on the manuscript. This article is published under HHMI’s Open Access to Publications policy. The HHMI lab heads have previously granted a nonexclusive CC BY 4.0 license to the public and a sublicensable license to HHMI in their research articles. In accordance with these licenses, the author-accepted manuscript of this article can be freely accessed under a CC BY 4.0 license immediately upon publication.

    Contributions

    F.B., W.M.G., S.R., E.M.M., and H.J. were responsible for conceptualization. F.B., L.S., S.R., R.C., and W.M.G. performed research. H.J., S.R., E.M.M., and W.M.G. were responsible for supervision and funding acquisition. F.B. wrote the original draft. All authors reviewed and edited the manuscript.

    Data Availability

    Document S1. Figures S1–S5

    Conflict of Interest

    The authors declare no competing interests.

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    Additional details

    Created:
    May 30, 2024
    Modified:
    May 30, 2024