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

Research

Stéphane Verger in the UPSC Growth Facility

Photo: 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

Atakhani A, Bogdziewiez L, Verger S (2022) Characterising the mechanics of cell–cell adhesion in plants. Quantitative Plant Biology. In press.
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.
Fruleux A, Verger S, Boudaoud A (2019). Feeling Stressed or Strained? A Biophysical Model for Cell Wall Mechanosensing in Plants. FRONTIERS IN PLANT SCIENCE 10:757. https://doi.org/10.3389/fpls.2019.00757
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
Galletti, R.*, Verger, S.*, Hamant, O., Ingram, G. (2016). Developing a ‘thick skin’: a paradoxical role for mechanical tension in maintaining epidermal integrity? Development. 143, 3249-3258.
http://dev.biologists.org/content/143/18/3249.long
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

Publications

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2022 (1)

Characterising the mechanics of cell–cell adhesion in plants. Atakhani, A., Bogdziewiez, L., & Verger, S. Quantitative Plant Biology, 3. February 2022.

Characterising the mechanics of cell–cell adhesion in plants [link]

Paper doi link bibtex abstract

@article{atakhani_characterising_2022,
	title = {Characterising the mechanics of cell–cell adhesion in plants},
	volume = {3},
	issn = {2632-8828},
	url = {https://www.cambridge.org/core/journals/quantitative-plant-biology/article/characterising-the-mechanics-of-cellcell-adhesion-in-plants/9D165A5D6EA6F2B1927B9F0F38F88AAC},
	doi = {10/gpjfdn},
	abstract = {, 

Cell–cell adhesion is a fundamental feature of multicellular organisms. To ensure multicellular integrity, adhesion needs to be tightly controlled and maintained. In plants, cell–cell adhesion remains poorly understood. Here, we argue that to be able to understand how cell–cell adhesion works in plants, we need to understand and quantitatively measure the mechanics behind it. We first introduce cell–cell adhesion in the context of multicellularity, briefly explain the notions of adhesion strength, work and energy and present the current knowledge concerning the mechanisms of cell–cell adhesion in plants. Because still relatively little is known in plants, we then turn to animals, but also algae, bacteria, yeast and fungi, and examine how adhesion works and how it can be quantitatively measured in these systems. From this, we explore how the mechanics of cell adhesion could be quantitatively characterised in plants, opening future perspectives for understanding plant multicellularity.},
	language = {en},
	urldate = {2022-02-16},
	journal = {Quantitative Plant Biology},
	author = {Atakhani, Asal and Bogdziewiez, Léa and Verger, Stéphane},
	month = feb,
	year = {2022},
	keywords = {adhesion strength, cell–cell adhesion, multicellularity, plant, single cell, tissue},
}

2021 (3)

Effects of Arabidopsis wall associated kinase mutations on ESMERALDA1 and elicitor induced ROS. Kohorn, B. D., Greed, B. E., Mouille, G., Verger, S., & Kohorn, S. L. PLOS ONE, 16(5): e0251922. May 2021.

Effects of Arabidopsis wall associated kinase mutations on ESMERALDA1 and elicitor induced ROS [link]

Paper doi link bibtex abstract

@article{kohorn_effects_2021,
	title = {Effects of {Arabidopsis} wall associated kinase mutations on {ESMERALDA1} and elicitor induced {ROS}},
	volume = {16},
	issn = {1932-6203},
	url = {https://dx.plos.org/10.1371/journal.pone.0251922},
	doi = {10/gkct4r},
	abstract = {Angiosperm cell adhesion is dependent on interactions between pectin polysaccharides which make up a significant portion of the plant cell wall. Cell adhesion in Arabidopsis may also be regulated through a pectin-related signaling cascade mediated by a putative O-fucosyltransferase ESMERALDA1 (ESMD1), and the Epidermal Growth Factor (EGF) domains of the pectin binding Wall associated Kinases (WAKs) are a primary candidate substrate for ESMD1 activity. Genetic interactions between WAKs and ESMD1 were examined using a dominant hyperactive allele of WAK2,
              WAK2cTAP
              , and a mutant of the putative O-fucosyltransferase ESMD1. WAK2cTAP expression results in a dwarf phenotype and activation of the stress response and reactive oxygen species (ROS) production, while
              esmd1
              is a suppressor of a pectin deficiency induced loss of adhesion. Here we find that
              esmd1
              suppresses the WAK2cTAP dwarf and stress response phenotype, including ROS accumulation and gene expression. Additional analysis suggests that mutations of the potential WAK EGF O-fucosylation site also abate the WAK2cTAP phenotype, yet only evidence for an N-linked but not O-linked sugar addition can be found. Moreover, a
              WAK
              locus deletion allele has no effect on the ability of
              esmd1
              to suppress an adhesion deficiency, indicating WAKs and their modification are not a required component of the potential ESMD1 signaling mechanism involved in the control of cell adhesion. The WAK locus deletion does however affect the induction of ROS but not the transcriptional response induced by the elicitors Flagellin, Chitin and oligogalacturonides (OGs).},
	language = {en},
	number = {5},
	urldate = {2021-06-03},
	journal = {PLOS ONE},
	author = {Kohorn, Bruce D. and Greed, Bridgid E. and Mouille, Gregory and Verger, Stéphane and Kohorn, Susan L.},
	editor = {Zabotina, Olga A.},
	month = may,
	year = {2021},
	pages = {e0251922},
}

External Mechanical Cues Reveal a Katanin-Independent Mechanism behind Auxin-Mediated Tissue Bending in Plants. Baral, A., Aryal, B., Jonsson, K., Morris, E., Demes, E., Takatani, S., Verger, S., Xu, T., Bennett, M., Hamant, O., & Bhalerao, R. P. Developmental Cell, 56(1): 67–80.e3. January 2021.

External Mechanical Cues Reveal a Katanin-Independent Mechanism behind Auxin-Mediated Tissue Bending in Plants [link]

Paper doi link bibtex

@article{baral_external_2021,
	title = {External {Mechanical} {Cues} {Reveal} a {Katanin}-{Independent} {Mechanism} behind {Auxin}-{Mediated} {Tissue} {Bending} in {Plants}},
	volume = {56},
	issn = {15345807},
	url = {https://linkinghub.elsevier.com/retrieve/pii/S1534580720309837},
	doi = {10/ghtbf9},
	language = {en},
	number = {1},
	urldate = {2021-06-03},
	journal = {Developmental Cell},
	author = {Baral, Anirban and Aryal, Bibek and Jonsson, Kristoffer and Morris, Emily and Demes, Elsa and Takatani, Shogo and Verger, Stéphane and Xu, Tongda and Bennett, Malcolm and Hamant, Olivier and Bhalerao, Rishikesh P.},
	month = jan,
	year = {2021},
	pages = {67--80.e3},
}

FERONIA and microtubules independently contribute to mechanical integrity in the Arabidopsis shoot. Malivert, A., Erguvan, Ö., Chevallier, A., Dehem, A., Friaud, R., Liu, M., Martin, M., Peyraud, T., Hamant, O., & Verger, S. PLOS Biology, 19(11): e3001454. November 2021.

FERONIA and microtubules independently contribute to mechanical integrity in the Arabidopsis shoot [link]

Paper doi link bibtex abstract

@article{malivert_feronia_2021,
	title = {{FERONIA} and microtubules independently contribute to mechanical integrity in the {Arabidopsis} shoot},
	volume = {19},
	issn = {1545-7885},
	url = {https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.3001454},
	doi = {10/gpkx26},
	abstract = {To survive, cells must constantly resist mechanical stress. In plants, this involves the reinforcement of cell walls, notably through microtubule-dependent cellulose deposition. How wall sensing might contribute to this response is unknown. Here, we tested whether the microtubule response to stress acts downstream of known wall sensors. Using a multistep screen with 11 mutant lines, we identify FERONIA (FER) as the primary candidate for the cell’s response to stress in the shoot. However, this does not imply that FER acts upstream of the microtubule response to stress. In fact, when performing mechanical perturbations, we instead show that the expected microtubule response to stress does not require FER. We reveal that the feronia phenotype can be partially rescued by reducing tensile stress levels. Conversely, in the absence of both microtubules and FER, cells appear to swell and burst. Altogether, this shows that the microtubule response to stress acts as an independent pathway to resist stress, in parallel to FER. We propose that both pathways are required to maintain the mechanical integrity of plant cells.},
	language = {en},
	number = {11},
	urldate = {2022-02-25},
	journal = {PLOS Biology},
	author = {Malivert, Alice and Erguvan, Özer and Chevallier, Antoine and Dehem, Antoine and Friaud, Rodrigue and Liu, Mengying and Martin, Marjolaine and Peyraud, Théophile and Hamant, Olivier and Verger, Stéphane},
	month = nov,
	year = {2021},
	keywords = {Anisotropy, Cellulose, Hypocotyl, Mechanical stress, Microtubules, Pavement cells, Plant cotyledon, Seedlings},
	pages = {e3001454},
}

2020 (2)

Microtubule Response to Tensile Stress Is Curbed by NEK6 to Buffer Growth Variation in the Arabidopsis Hypocotyl. Takatani, S., Verger, S., Okamoto, T., Takahashi, T., Hamant, O., & Motose, H. Current Biology, 30(8): 1491–1503.e2. April 2020.

Microtubule Response to Tensile Stress Is Curbed by NEK6 to Buffer Growth Variation in the Arabidopsis Hypocotyl [link]

Paper doi link bibtex

@article{takatani_microtubule_2020,
	title = {Microtubule {Response} to {Tensile} {Stress} {Is} {Curbed} by {NEK6} to {Buffer} {Growth} {Variation} in the {Arabidopsis} {Hypocotyl}},
	volume = {30},
	issn = {09609822},
	url = {https://linkinghub.elsevier.com/retrieve/pii/S0960982220301974},
	doi = {10.1016/j.cub.2020.02.024},
	language = {en},
	number = {8},
	urldate = {2021-06-07},
	journal = {Current Biology},
	author = {Takatani, Shogo and Verger, Stéphane and Okamoto, Takashi and Takahashi, Taku and Hamant, Olivier and Motose, Hiroyasu},
	month = apr,
	year = {2020},
	pages = {1491--1503.e2},
}

Polar expedition: mechanisms for protein polar localization. Raggi, S., Demes, E., Liu, S., Verger, S., & Robert, S. Current Opinion in Plant Biology, 53: 134–140. February 2020.

Polar expedition: mechanisms for protein polar localization [link]

Paper doi link bibtex

@article{raggi_polar_2020,
	title = {Polar expedition: mechanisms for protein polar localization},
	volume = {53},
	issn = {13695266},
	shorttitle = {Polar expedition},
	url = {https://linkinghub.elsevier.com/retrieve/pii/S1369526619301165},
	doi = {10.1016/j.pbi.2019.12.001},
	language = {en},
	urldate = {2021-06-07},
	journal = {Current Opinion in Plant Biology},
	author = {Raggi, Sara and Demes, Elsa and Liu, Sijia and Verger, Stéphane and Robert, Stéphanie},
	month = feb,
	year = {2020},
	pages = {134--140},
}

2019 (3)

Feeling Stressed or Strained? A Biophysical Model for Cell Wall Mechanosensing in Plants. Fruleux, A., Verger, S., & Boudaoud, A. Frontiers in Plant Science, 10: 757. June 2019.

Feeling Stressed or Strained? A Biophysical Model for Cell Wall Mechanosensing in Plants [link]

Paper doi link bibtex

@article{fruleux_feeling_2019,
	title = {Feeling {Stressed} or {Strained}? {A} {Biophysical} {Model} for {Cell} {Wall} {Mechanosensing} in {Plants}},
	volume = {10},
	issn = {1664-462X},
	shorttitle = {Feeling {Stressed} or {Strained}?},
	url = {https://www.frontiersin.org/article/10.3389/fpls.2019.00757/full},
	doi = {10/gg484c},
	urldate = {2021-06-07},
	journal = {Frontiers in Plant Science},
	author = {Fruleux, Antoine and Verger, Stéphane and Boudaoud, Arezki},
	month = jun,
	year = {2019},
	pages = {757},
}

ImageJ SurfCut: a user-friendly pipeline for high-throughput extraction of cell contours from 3D image stacks. Erguvan, Ö., Louveaux, M., Hamant, O., & Verger, S. BMC Biology, 17(1): 38. December 2019.

ImageJ SurfCut: a user-friendly pipeline for high-throughput extraction of cell contours from 3D image stacks [link]

Paper doi link bibtex

@article{erguvan_imagej_2019,
	title = {{ImageJ} {SurfCut}: a user-friendly pipeline for high-throughput extraction of cell contours from {3D} image stacks},
	volume = {17},
	issn = {1741-7007},
	shorttitle = {{ImageJ} {SurfCut}},
	url = {https://bmcbiol.biomedcentral.com/articles/10.1186/s12915-019-0657-1},
	doi = {10/gf2hww},
	language = {en},
	number = {1},
	urldate = {2021-06-07},
	journal = {BMC Biology},
	author = {Erguvan, Özer and Louveaux, Marion and Hamant, Olivier and Verger, Stéphane},
	month = dec,
	year = {2019},
	pages = {38},
}

Mechanical Conflicts in Twisting Growth Revealed by Cell-Cell Adhesion Defects. Verger, S., Liu, M., & Hamant, O. Frontiers in Plant Science, 10: 173. February 2019.

Mechanical Conflicts in Twisting Growth Revealed by Cell-Cell Adhesion Defects [link]

Paper doi link bibtex

@article{verger_mechanical_2019,
	title = {Mechanical {Conflicts} in {Twisting} {Growth} {Revealed} by {Cell}-{Cell} {Adhesion} {Defects}},
	volume = {10},
	issn = {1664-462X},
	url = {https://www.frontiersin.org/article/10.3389/fpls.2019.00173/full},
	doi = {10/gkf56m},
	urldate = {2021-06-07},
	journal = {Frontiers in Plant Science},
	author = {Verger, Stéphane and Liu, Mengying and Hamant, Olivier},
	month = feb,
	year = {2019},
	pages = {173},
}

2018 (4)

A tension-adhesion feedback loop in plant epidermis. Verger, S., Long, Y., Boudaoud, A., & Hamant, O. eLife, 7: e34460. April 2018. Publisher: eLife Sciences Publications, Ltd

A tension-adhesion feedback loop in plant epidermis [link]

Paper doi link bibtex abstract

@article{verger_tension-adhesion_2018,
	title = {A tension-adhesion feedback loop in plant epidermis},
	volume = {7},
	issn = {2050-084X},
	url = {https://doi.org/10.7554/eLife.34460},
	doi = {10/gdd8s2},
	abstract = {Mechanical forces have emerged as coordinating signals for most cell functions. Yet, because forces are invisible, mapping tensile stress patterns in tissues remains a major challenge in all kingdoms. Here we take advantage of the adhesion defects in the Arabidopsis mutant quasimodo1 (qua1) to deduce stress patterns in tissues. By reducing the water potential and epidermal tension in planta, we rescued the adhesion defects in qua1, formally associating gaping and tensile stress patterns in the mutant. Using suboptimal water potential conditions, we revealed the relative contributions of shape- and growth-derived stress in prescribing maximal tension directions in aerial tissues. Consistently, the tension patterns deduced from the gaping patterns in qua1 matched the pattern of cortical microtubules, which are thought to align with maximal tension, in wild-type organs. Conversely, loss of epidermis continuity in the qua1 mutant hampered supracellular microtubule alignments, revealing that coordination through tensile stress requires cell-cell adhesion.},
	urldate = {2021-06-07},
	journal = {eLife},
	author = {Verger, Stéphane and Long, Yuchen and Boudaoud, Arezki and Hamant, Olivier},
	editor = {Hardtke, Christian S and Bergmann, Dominique C},
	month = apr,
	year = {2018},
	note = {Publisher: eLife Sciences Publications, Ltd},
	keywords = {cell adhesion, mechanical stress, microtubules, plant organs},
	pages = {e34460},
}

An Image Analysis Pipeline to Quantify Emerging Cracks in Materials or Adhesion Defects in Living Tissues. Verger, S., Cerutti, G., & Hamant, O. BIO-PROTOCOL, 8(19). 2018.

An Image Analysis Pipeline to Quantify Emerging Cracks in Materials or Adhesion Defects in Living Tissues [link]

Paper doi link bibtex

@article{verger_image_2018,
	title = {An {Image} {Analysis} {Pipeline} to {Quantify} {Emerging} {Cracks} in {Materials} or {Adhesion} {Defects} in {Living} {Tissues}},
	volume = {8},
	issn = {2331-8325},
	url = {https://bio-protocol.org/e3036},
	doi = {10/gkf56f},
	language = {en},
	number = {19},
	urldate = {2021-06-07},
	journal = {BIO-PROTOCOL},
	author = {Verger, Stéphane and Cerutti, Guillaume and Hamant, Olivier},
	year = {2018},
}

Plant Physiology: FERONIA Defends the Cell Walls against Corrosion. Verger, S., & Hamant, O. Current Biology, 28(5): R215–R217. March 2018.

Plant Physiology: FERONIA Defends the Cell Walls against Corrosion [link]

Paper doi link bibtex abstract

@article{verger_plant_2018,
	title = {Plant {Physiology}: {FERONIA} {Defends} the {Cell} {Walls} against {Corrosion}},
	volume = {28},
	issn = {0960-9822},
	shorttitle = {Plant {Physiology}},
	url = {https://www.sciencedirect.com/science/article/pii/S0960982218300769},
	doi = {10/gc3gx6},
	abstract = {A new study uncovers the role of wall sensing and remodeling in the plant response to salt stress, identifying the FERONIA receptor kinase as a key player in that process, likely through direct sensing of cell wall pectins.},
	language = {en},
	number = {5},
	urldate = {2021-06-07},
	journal = {Current Biology},
	author = {Verger, Stéphane and Hamant, Olivier},
	month = mar,
	year = {2018},
	pages = {R215--R217},
}

Why plants make puzzle cells, and how their shape emerges. Sapala, A., Runions, A., Routier-Kierzkowska, A., Das Gupta, M., Hong, L., Hofhuis, H., Verger, S., Mosca, G., Li, C., Hay, A., Hamant, O., Roeder, A. H., Tsiantis, M., Prusinkiewicz, P., & Smith, R. S eLife, 7: e32794. February 2018. Publisher: eLife Sciences Publications, Ltd

Why plants make puzzle cells, and how their shape emerges [link]

Paper doi link bibtex abstract

@article{sapala_why_2018,
	title = {Why plants make puzzle cells, and how their shape emerges},
	volume = {7},
	issn = {2050-084X},
	url = {https://doi.org/10.7554/eLife.32794},
	doi = {10/gc3w3z},
	abstract = {The shape and function of plant cells are often highly interdependent. The puzzle-shaped cells that appear in the epidermis of many plants are a striking example of a complex cell shape, however their functional benefit has remained elusive. We propose that these intricate forms provide an effective strategy to reduce mechanical stress in the cell wall of the epidermis. When tissue-level growth is isotropic, we hypothesize that lobes emerge at the cellular level to prevent formation of large isodiametric cells that would bulge under the stress produced by turgor pressure. Data from various plant organs and species support the relationship between lobes and growth isotropy, which we test with mutants where growth direction is perturbed. Using simulation models we show that a mechanism actively regulating cellular stress plausibly reproduces the development of epidermal cell shape. Together, our results suggest that mechanical stress is a key driver of cell-shape morphogenesis.},
	urldate = {2021-06-07},
	journal = {eLife},
	author = {Sapala, Aleksandra and Runions, Adam and Routier-Kierzkowska, Anne-Lise and Das Gupta, Mainak and Hong, Lilan and Hofhuis, Hugo and Verger, Stéphane and Mosca, Gabriella and Li, Chun-Biu and Hay, Angela and Hamant, Olivier and Roeder, Adrienne HK and Tsiantis, Miltos and Prusinkiewicz, Przemyslaw and Smith, Richard S},
	editor = {McCormick, Sheila},
	month = feb,
	year = {2018},
	note = {Publisher: eLife Sciences Publications, Ltd},
	keywords = {growth, modelling, morphogenesis, organ shape, pavement cells, plant development},
	pages = {e32794},
}

2016 (2)

Cell adhesion in plants is under the control of putative O-fucosyltransferases. Verger, S., Chabout, S., Gineau, E., & Mouille, G. Development, 143(14): 2536–2540. July 2016.

Cell adhesion in plants is under the control of putative O-fucosyltransferases [link]

Paper doi link bibtex abstract

@article{verger_cell_2016,
	title = {Cell adhesion in plants is under the control of putative {O}-fucosyltransferases},
	volume = {143},
	issn = {0950-1991},
	url = {https://doi.org/10.1242/dev.132308},
	doi = {10/f9n5bb},
	abstract = {Cell-to-cell adhesion in plants is mediated by the cell wall and the presence of a pectin-rich middle lamella. However, we know very little about how the plant actually controls and maintains cell adhesion during growth and development and how it deals with the dynamic cell wall remodeling that takes place. Here we investigate the molecular mechanisms that control cell adhesion in plants. We carried out a genetic suppressor screen and a genetic analysis of cell adhesion-defective Arabidopsis thaliana mutants. We identified a genetic suppressor of a cell adhesion defect affecting a putative O-fucosyltransferase. Furthermore, we show that the state of cell adhesion is not directly linked with pectin content in the cell wall but instead is associated with altered pectin-related signaling. Our results suggest that cell adhesion is under the control of a feedback signal from the state of the pectin in the cell wall. Such a mechanism could be necessary for the control and maintenance of cell adhesion during growth and development.},
	number = {14},
	urldate = {2021-06-07},
	journal = {Development},
	author = {Verger, Stéphane and Chabout, Salem and Gineau, Emilie and Mouille, Grégory},
	month = jul,
	year = {2016},
	pages = {2536--2540},
}

Developing a ‘thick skin’: a paradoxical role for mechanical tension in maintaining epidermal integrity?. Galletti, R., Verger, S., Hamant, O., & Ingram, G. C. Development, 143(18): 3249–3258. September 2016.

Developing a ‘thick skin’: a paradoxical role for mechanical tension in maintaining epidermal integrity? [link]

Paper doi link bibtex abstract

@article{galletti_developing_2016,
	title = {Developing a ‘thick skin’: a paradoxical role for mechanical tension in maintaining epidermal integrity?},
	volume = {143},
	issn = {0950-1991},
	shorttitle = {Developing a ‘thick skin’},
	url = {https://doi.org/10.1242/dev.132837},
	doi = {10.1242/dev.132837},
	abstract = {Plant aerial epidermal tissues, like animal epithelia, act as load-bearing layers and hence play pivotal roles in development. The presence of tension in the epidermis has morphogenetic implications for organ shapes but it also constantly threatens the integrity of this tissue. Here, we explore the multi-scale relationship between tension and cell adhesion in the plant epidermis, and we examine how tensile stress perception may act as a regulatory input to preserve epidermal tissue integrity and thus normal morphogenesis. From this, we identify parallels between plant epidermal and animal epithelial tissues and highlight a list of unexplored questions for future research.},
	number = {18},
	urldate = {2021-10-14},
	journal = {Development},
	author = {Galletti, Roberta and Verger, Stéphane and Hamant, Olivier and Ingram, Gwyneth C.},
	month = sep,
	year = {2016},
	pages = {3249--3258},
}

2013 (1)

A galactosyltransferase acting on arabinogalactan protein glycans is essential for embryo development in Arabidopsis. Geshi, N., Johansen, J. N., Dilokpimol, A., Rolland, A., Belcram, K., Verger, S., Kotake, T., Tsumuraya, Y., Kaneko, S., Tryfona, T., Dupree, P., Scheller, H. V., Höfte, H., & Mouille, G. The Plant Journal,n/a–n/a. August 2013.

A galactosyltransferase acting on arabinogalactan protein glycans is essential for embryo development in Arabidopsis [link]

Paper doi link bibtex

@article{geshi_galactosyltransferase_2013,
	title = {A galactosyltransferase acting on arabinogalactan protein glycans is essential for embryo development in {Arabidopsis}},
	issn = {09607412},
	url = {http://doi.wiley.com/10.1111/tpj.12281},
	doi = {10/gkgdks},
	language = {en},
	urldate = {2021-06-08},
	journal = {The Plant Journal},
	author = {Geshi, Naomi and Johansen, Jorunn N. and Dilokpimol, Adiphol and Rolland, Aurélia and Belcram, Katia and Verger, Stéphane and Kotake, Toshihisa and Tsumuraya, Yoichi and Kaneko, Satoshi and Tryfona, Theodora and Dupree, Paul and Scheller, Henrik V. and Höfte, Herman and Mouille, Gregory},
	month = aug,
	year = {2013},
	pages = {n/a--n/a},
}