Group leader, Research Director (INRA DR2), Research Associate position at the Sainsbury lab in Cambridge, UK and Associate Professor at Kumamoto University in Japan
Plant Reproduction and Development lab, ENS Lyon, France
Microtubule behavior at the shoot apical meristem in Arabidopsis thaliana
Olivier Hamant and his group are exploring the role of mechanical stress in development. They focus their work on the shoot apical meristem (located at the stem tips) which contains the stem cells in the plant model Arabidopsis thaliana. Using microscopy, biophysics and computaional modeling, they identified a role of forces in the control of growth, cell polarity, cell division plane orientation and gene expression. They currently investigate how such mechanical signals are transduced in plant cells.
A number of studies have shown how the gene regulatory network impacts the mechanical properties of cells to control shape changes. Olivier Hamant’s group wants to address the converse question: how does mechanical stress in turn feed back on development? All developing organisms experience internal mechanical stress. There is
accumulating evidence that mechanical forces contribute to many aspects of cell biology in animal systems, including cell identity (e.g. Engler et al., 2006), cell division (e.g. Théry et al., 2006), and cell polarity (e.g. Houk et al., 2012). While most of these studies have focused on single cells in culture, the existence of cell-cell interactions in tissues also implies that the communication and propagation of mechanical forces between adjacent cells contribute to shape changes and developmental decisions.
Pioneering studies on Drosophila imaginal discs have shown that mechanical stress may synchronize cell division profiles (Hufnagel et al., 2007) and that tension lines may act as boundaries to separate functional domains (Landsberg et al., 2009). The expression pattern of the twist gene has also been shown to depend on mechanical strain in the Drosophila embryo (Farge, 2003). Nonetheless, very little is known regarding the role of mechanical feedbacks at the tissue scale, notably because of the complex developmental behaviours of cells in animal tissues, which include division, elongation, death and migration. Because plant cells are glued to each other by their contiguous walls and do not migrate, together with the absence of cell death in young tissues, plant tissues represent a much simpler experimental system to investigate the contribution of mechanical stress to tissue development.
Reexamining older work by Paul Green and others, Olivier Hamant’s group and his collaborators have shown that plant cells are able to respond to mechanical stress by reorienting their cortical microtubules in tissues, thus relating this mechanical
feedback to growth anisotropy and shape changes (Hamant et al., 2008). This in fact can be related to Wolff’s law in bones, as the reorientation of microtubules along maximal tension implies that cellulose will be deposited so as to resist maximal stress. The analysis of the molecular mechanism linking microtubules and mechanical anisotropy of cell walls also revealed that plant stems twist by default (Landrein et al., 2013).
A role of mechanical stress in promoting growth heterogeneity between adjacent cells was also identified. This result is counterintuitive as one may have thought that adjacent cells would instead attempt to reach a compromise when growth becomes heterogeneous. The active maintenance of growth heterogeneity may in fact facilitate the initiation of sharp differential growth gradients that are required for organogenesis (Uyttewaal et al., 2012).
Beyond microtubules, the group also identified a role of mechanical signals in cell polarity, notably focusing on the plant hormone auxin efflux carrier PIN1, which localizes to the most tensed membranes within a cell (Heisler et al., 2010). More recently, mechanical stress at the shoot apical meristem was involved in the regulation of gene expression pattern. In particular, the central meristem regulator and homeobox gene STM was shown to be induced by mechanical perturbations. In normal condition, the promoter of this gene is more highly expressed in folded regions of the shoot apical meristem, i.e. in domains where stress anisotropy is the strongest (Landrein et al., 2015).
This research has many perspectives : what is the nature of the mechanoperception pathways? What are the specificities of the
mechanotransduction pathways in a multicellular walled organism? What are the similarities with animal systems? How is an elastic mechanical deformation translated into a plastic developmental response? Does this memory involve specific mechanoreceptors associated with the cell wall and long term modifications of the cell wall composition? Is this memory also marked in chromatin? Which types of epigenetic marks are present on mechanosensitive genes? Are the mechanosensitive genes induced by a mechanical deformation of the nucleus?
At the tissue scale, how are mechanical forces used to coordinate growth between adjacent cells? Is gene expression affected by mechanical stress between adjacent cells? Is the timing and orientation of cell division controlled by mechanical deformations of neighboring cells? Conversely, do dividing cells induce mechanical stresses that impact the behavior of neighboring cells?
Beyond growth, do mechanical signals contribute to the determination of cell fate and patterning? Is the identity of the epidermis determined to resist to the mechanical stress generated by underlying cells? Is an expression boundary also a mechanical boundary? How does growth coordination by mechanical stress influence the robustness of gene expression patterns? Does mechanical stress contribute to the maintenance of stem cell fate?
• 2003: PhD, Institut Jean-Pierre Bourgin, INRA France and VIB, Gent, Belgium, Véronique Pautot and Gerrit Beemster’s labs
• 2003-2005: Postdoctoral fellow, UC Berkeley, USA, Zac Cande’s lab
• 2006-2007: Postdoctoral fellow, ENS Lyon, France, Jan Traas’ lab
• 2007 Appointed Research associate (INRA CR, permanent position), RDP, ENS Lyon, France, Jan Traas’ lab
• 2010 : Appointed Group leader with Pr Arezki Boudaoud at the Joliot Curie Lab, Lyon, France
• Grant from the European Research Council (ERC Consolidator Grant), 2014
• Laurier jeune chercheur, awarded to a young INRA researcher each year, INRA 2012
• Paul Doisteau - Emile Blutet Prize, awarded to a researcher working on plant biology every 4 years, French Science Academy, 2012
• Prize from the scientific journal « La recherche », French ministry of research, 2009
April 2012, Cell
Dec 2088, Science