Verger, Stéphane – Mechanics and Dynamics of Cell-Cell Adhesion in Plants

Research

Stéphane Verger in the UPSC Growth FacilityPhoto: Johan Gunséus

Cell-cell adhesion is one of the most fundamental features of multicellular organisms. We are studying the mechanisms involved in cell-cell adhesion in both Arabidopsis and Poplar using novel and interdisciplinary approaches, including biophysical tools, confocal microscopy and computational modeling.

All living organisms experience physical stress, and notably tensions, as tissues grow. Adhesion between cells provides resistance to such forces and maintains the integrity of the organism. In turn, adhesion can be modulated, e.g. to promote cell migration in animals or organ shedding in plants. The relation between tension and adhesion is a fundamental question in the development of multicellular organisms, yet it remains largely under-studied in plants.

Cell-cell adhesion in plants largely relies on a layered structure composed of a pectin-rich middle lamella located between the walls of adjacent cells (Fig. 1). Conversely, cell separation events such as organ abscission, usually require an active degradation of the middle lamella by cell wall remodeling enzymes such as pectin methylesterases and polygalacturonases. Interestingly, such enzymes are also required for loosening the cell wall and allowing growth. In addition, turgor pressure puts the cell walls under tension; differential growth or patterns of tension can generate mechanical conflicts between adjacent cells, thus threatening cell adhesion (Fig. 1). How cell adhesion is maintained is thus not trivial when considering the coupling between forces and wall chemistry in a growing tissue.

The figure illustrates tension and adhesion in plant tissues.Fig 1: Tension and adhesion in plants. Plant cells adhere through their cell wall, while tissue scale tension tends to pull the cells apart.

Several mutants display cell adhesion defects. Among them, quasimodo1 and quasimodo2 (Fig. 2) are mutated in enzymes involved in the synthesis of the homogalacturonans (HG), the main component of the pectins and constituent of the middle lamella. However, the regulation of cell adhesion is more complex: We have previously identified suppressors of these mutants and revealed that the decrease in HG content is not the sole cause of the loss of cell adhesion in these mutants and that a feedback signal from the wall contributes to this phenotype. Beyond pectins, mutants affected in actin filament nucleation, mechanosensing and epidermal identity show cell adhesion defects, which strongly suggest that cell adhesion is under a complex, biochemical and biomechanical, control in plants.

Microscope images comparing cell adhesion defects in quasimodo mutants with wildtype plants. Fig 2: Cell adhesion defects in quasimodo2-1 cotyledon pavement cell (bottom Left) and quasimodo 1-1 dark-grown hypocotyl (bottom right), as compared to wildtype (top panels). Images are z-projection (maximal intensity) of 3D confocal stack from propidium iodide stained samples.

So far the topic has remained very challenging to study in plants, notably because the physical parameters related to cell adhesion are difficult to quantify (e.g. tensile stress at the cell-cell connections and adhesion strength). However, tools usually designed for material sciences are increasingly adapted to biophysics and living samples. For example Atomic Force Microscopy (AFM, Fig. 3) and micro-mechanical tools to deform and measure cells and tissues mechanical properties in a quantitative way, as well as mechanical models to predict tension patterns in tissues, can now be used to study cell-cell adhesion in plants.

Atomic Force Microscopy images from 4-day old wild type (A-C) and qua1-1 (D-F) cotyledons. Fig 3: Atomic Force Microscopy (AFM) images from 4-day old wild type (A-C) and qua1-1 (D-F) cotyledons. (A and D) 3D rendering of the epidermis topography. Lighter regions are more elevated than darker ones. (B and E) Topography map. (C and F) Stiffness map of the outer walls, ranging from 5.5 MPa (black) to 7 MPa (white). While for the wild type, the cell-cell connections form a clearly defined “valley” and are stiffer, in qua1-1 these regions are flatter and softer. The red arrow in panel M points to holes in the flat and soft region, suggesting that this zone may be a sheet of outer wall detached from the underlying cell. Scale bars, 10 μm.

Taking advantage of these recent developments, our aim is to unravel the mechanics and dynamics of cell adhesion in plants at unprecedented resolution. More precisely our goal is:

  • To identify the mechanisms through which plants dynamically control cell-cell adhesion, focusing on the role of mechanosensing, cytoskeleton dynamics and the cell wall secretion.
  • To study the dynamic control of cell adhesion taking place during wood fiber cell elongation, and its importance for the chemical and mechanical properties of Poplar wood.

For this purpose we combine the use of genetic, chemical and mechanical perturbations together with quantitative live imaging, micromechanical and cell wall analyses, and computational modeling.

While part of our work is carried out on the model species Arabidospis thaliana, providing basic knowledge on the questions of cell-cell adhesion in plants, in the long term our research may lead to the generation of improved trees for traits such as wood mechanical strength and biomass conversion.


Key Publications

  • Demes E & Verger S (2023). High-throughput characterization of cortical microtubule arrays response to anisotropic tensile stress. BMC Biology, 21 (1), 1-13. https://doi.org/10.1186/s12915-023-01654-7
  • Atakhani A, Bogdziewiez L, Verger S (2022) Characterising the mechanics of cell–cell adhesion in plants. Quantitative Plant Biology. 3, 2022, e2. https://doi.org/10.1017/qpb.2021.16
  • Malivert A, Erguvan Ö, Chevallier A, Dehem A, Friaud R, Liu M, Martin M, Peyraud T, Hamant O, Verger S (2021) FERONIA and microtubules independently contribute to mechanical integrity in the Arabidopsis shoot. PLoS Biology. 19, 11, e3001454. https://doi.org/10.1371/journal.pbio.3001454
  • Erguvan Ö, Louveaux M, Hamant O, Verger S (2019). ImageJ SurfCut: a user-friendly pipeline for high-throughput extraction of cell contours from 3D image stacks. BMC Biol. 17(1):38. https://doi.org/10.1186/s12915-019-0657-1
  • Verger, S., Long, Y., Boudaoud, A., Hamant, O. (2018). A tension-adhesion feedback loop in plant epidermis. eLife. 7, e34460. https://elifesciences.org/articles/34460
  • Verger, S., Chabout, S., Gineau, E., Mouille, G. (2016). Cell adhesion in plants is under the control of putative O-fucosyltransferases. Development. 143, 2536-2540. http://dev.biologists.org/content/143/14/2536.long