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Richard Smith
Max Planck, Köln
John Innes Centre, Norwich

Richard's lab uses mathematical and computer simulation techniques to investigate questions in plant development. Working in close collaboration with experimental biologists, they develop cellular-level simulation models of hormone signaling and patterning in plant tissue. These models involve a biochemical aspect, genes, proteins, hormones, combined with growing, changing geometry as cells divide and tissues grow. They are interested in the interaction between these two processes. How genes control physical properties of cells resulting in growth, and how the resulting change in geometry and physical forces feeds back on signaling and gene regulation. With this in mind, they are researching methods to quantify mechanical properties in plant tissues, to facilitate the construction of biophysically-based simulation models of plant growth.

 

Lab members

Richard Smith (principal investigator)

Milad Adibi (Postdoc)

Brendan Lane (Postdoc)

Gabriella Mosca (Postdoc)

Sören Strauss (Postdoc)

Aleksandra Sapala (PhD student)

 

Research

Much of our research involves the precise tracking of cell shape change, either from growth or elastic deformation. Since plants display symplastic growth, considerable information about morphogenesis can be obtained by looking at shape change in the surface layer of cells. However, in many systems, the surface layer of cells is not flat, and cell shape information is lost when doing max projections of confocal image data onto a plane. To address this problem, we have developed specialized software (www.MorphoGraphX.org) for the quantification of curved surface layers of cells. Working somewhere between 2 and 3D, MorphoGraphX is able to turn 3D confocal image stacks into curved surface images, which are then processed with standard algorithms we have adapted for this purpose. We are now extending our software for full 3D cell segmentation, fluorescence quantification, shape analysis, and other image processing problems as our research demands.

Cellular force microscopy (CFM) is a new micro-indentation technique (Routier-Kierzkowska et al. 2012) that we have developed in collaboration with the Nelson lab and Femtotools. Sample stiffness is measured by indenting a thin probe connected to a force sensor. The recorded force and displacement are then used to determine the stiffness. Similar to atomic force microscopy (AFM), CFM uses computer controlled actuators to move the probe and can be used to create high-resolution stiffness maps as well as height maps. Some advantages of CFM are the wide range of forces that can be measured, filling the gap between AFM and load cells. CFM also has greater geometrical freedom; it is able to make large movements (up to cm's) and its long slender probe can access areas that a cantilever cannot. The CFM system is also highly flexible and can be used in combination with various optical microscopes, including both upright and inverted confocal systems.

Early embryo development provides an excellent system to study morphogenesis. In this system cell expansion, cell division, and genetic activity can be followed cell by cell in great detail. In collaboration with the Weijers lab, we use state of the art 3D imaging and molecular techniques to link gene and signaling networks to morphogenesis in plants. We test our hypothesis by using 3D spatial simulation models, developed in collaboration with the Prusinkiewicz lab, that are based on cell shape information extracted from sample tissue using MorphoGraphX. By developing a close integration between our simulation and imaging environments we will be able to use gene expression marker levels as direct input to our models, as well as to test model outputs. Our goal is to move one step closer to a true virtual plant tissue.

Another great system for exploring the link between genetics and cell expansion is the mature Arabidopsis embryo. During germination a decision is made based largely on environmental cues to break dormancy and commence growth. Driven by the gibberellic acid (GA) signaling pathway, this binary growth switch represents an ideal system for examining the relationship between the induction of growth promoting gene expression and organ morphogenesis. In collaborating with the Bassel lab, Birmingham, we are developing methods to quantify cell shape change and gene expression in 3D. These data are being used to feed a physically-based finite-element (FEM) simulation model of the embryo that we are using to explore the regulation of cell expansion in a geometrically and mechanically realistic environment.

 

Publications

2018

Sapala, A., Runions, A., Routier-Kierzkowska, A.-L., Das Gupta, M., Hong, L., Hofhuis, H., Verger, S., Mosca, G., Li, C.-B., Hay, A., Hamant, O., Roeder, A., Tsiantis, M., Prusinkiewicz, R., & Smith, R. S. (2018). Why plants make puzzle cells, and how their shape emerges. eLife, 7: e32794. doi:10.7554/eLife.32794.

2017

Hervieux, N., Tsugawa, S., Fruleux, A., Dumond, M., Routier-Kierzkowska, A.-L., Komatsuzaki, T., Boudaoud, A., Larkin, J. C., Smith, R. S., Li, C.-B., & Hamant, O. (2017). Mechanical Shielding of Rapidly Growing Cells Buffers Growth Heterogeneity and Contributes to Organ Shape Reproducibility. Current Biology,27(22), 3468-3479.e4. doi:10.1016/j.cub.2017.10.033.

Jones, A.R., Forero-Vargas, M., Withers, S.P., Smith, R.S., Traas, J., Dewitte, W., Murray, J.A.H. Cell-size dependent progression of the cell cycle creates homeostasis and flexibility of plant cell size. Nature Communications 8 (2017).

McKim, S. M., Routier-Kierzkowska, A.-L., Monniaux, M., Kierzkowski, D., Pieper, B., Smith, R. S., Tsiantis, M., & Hay, A. (2017). Seasonal Regulation of Petal Number. Plant Physiology, 175(2), 886-903. doi:10.1104/pp.17.00563.

Mosca, M., Sapala, A., Strauss, A., Routier-Kierzkowskai, A-L., Smith, R.S. On the micro-indentation of plant cells in a tissue context. Physical Biology 14 (2017).

Stamm, P., Strauß, S., Montenegro-Johnson, T. D., Smith, R. S., & Bassel, G. W. (2017). In Silico Methods for Cell Annotation, Quantification of Gene Expression, and Cell Geometry at Single-Cell Resolution Using 3DCellAtlas. PLANT HORMONES: METHODS AND PROTOCOLS, 3RD EDITION, 99-123. doi:10.1007/978-1-4939-6469-7_11.

Tsugawa, S., Hervieux, N., Kierzkowski, D., Routier-Kierzkowska, A.-L., Sapala, A., Hamant, O., Smith, R. S., Roeder, A. H. K., Boudaoud, A., & Li, C.-B. (2017). Clones of cells switch from reduction to enhancement of size variability in Arabidopsis sepals. Development, 144(23), 4398-4405. doi:10.1242/dev.153999.

2016 

Hong, L., Dumond, M., Tsugawa, S., Sapala, A., Routier-Kierzkowska, A-L., Zhou, Y., Chen, C., Kiss, A., Zhu, M., Hamant, O., Smith, R.S., Komatsuzaki, T., Li, C-B., Boudaoud, A., Roeder, A.H.K. Variable Cell Growth Yields Reproducible Organ Development through Spatiotemporal Averaging. Developmental Cell 38(1), 15-32 (2016). 

Žádníková, P., Wabnik, K., Abuzeineh, A., Gallemi, M., Van Der Straeten, M., Smith, R.S., Inzé, D., Friml, J., Prusinkiewicz, P., Benková, E. A Model of Differential Growth-Guided Apical Hook Formation in Plants. The Plant Cell28(10), 2464-2477 (2016)

Hofhuis, H., Moulton, D., Lessinnes, T., Routier-Kierzkowska, A.L., Bomphrey, R.J., Mosca, G., Reinhardt, H., Sarchet, P., Gan, X., Tsiantis, M. and Ventikos, Y. Morphomechanical Innovation Drives Explosive Seed Dispersal. Cell, 166: 222-233

Tsugawa, S., Hervieux, N., Hamant, O., Boudaoud, A., Smith, R. S., Li, C. B., and Komatsuzaki, T. Extracting Subcellular Fibrillar Alignment with Error Estimation: Application to Microtubules. Biophysical journal, 110: 1836-1844.

Hervieux, N., Dumond, M., Sapala, A., Routier-Kierzkowska, A.L., Kierzkowski, D., Roeder, A.H., Smith, R.S., Boudaoud, A. and Hamant, O. A mechanical feedback restricts sepal growth and shape in Arabidopsis. Current Biology, 26: 1019-1028.

Bassel, George W., and Richard S. Smith. Quantifying morphogenesis in plants in 4D. Current opinion in plant biology, 29: 87-94.

Kirchhelle, C., Chow, C.M., Foucart, C., Neto, H., Stierhof, Y.D., Kalde, M., Walton, C., Fricker, M., Smith, R.S., Jérusalem, A. and Irani, N. The Specification of Geometric Edges by a Plant Rab GTPase Is an Essential Cell-Patterning Principle During Organogenesis in Arabidopsis. Developmental cell, 36: 386-400.

von Wangenheim, D., Fangerau, J., Schmitz, A., Smith, R. S., Leitte, H., Stelzer, E. H., & Maizel, A. Rules and self-organizing properties of post-embryonic plant organ cell division patterns. Current Biology, 26: 439-449

Scheuring, D., Löfke, C., Krüger, F., Kittelmann, M., Eisa, A., Hughes, L., Smith, R.S., Hawes, C., Schumacher, K. and Kleine-Vehn, J. Actin-dependent vacuolar occupancy of the cell determines auxin-induced growth repression. Proceedings of the National Academy of Sciences, 113: 452-457.

Martinez, C. C., Chitwood, D. H., Smith, R. S., and Sinha, N. R. Left-right leaf asymmetry in decussate and distichous phyllotactic systems. BioRxiv, 043869.

 

2015 

Tauriello, G., Meyer, H. M., Smith, R. S., Koumoutsakos, P., and Roeder, A. H. Variability and constancy in cellular growth of Arabidopsis sepals. Plant physiology, 169: 2342-2358.

Weber, A., Braybrook, S., Huflejt, M., Mosca, G., Routier-Kierzkowska, A. L., and Smith, R. S. Measuring the mechanical properties of plant cells by combining micro-indentation with osmotic treatments. Journal of experimental botany, 66: 3229-3241.

Barbier de Reuille, P.B., Routier-Kierzkowska, A.L., Kierzkowski, D., Bassel, G.W., Schüpbach, T., Tauriello, G., Bajpai, N., Strauss, S., Weber, A., Kiss, A. and Burian, A., 2015. MorphoGraphX: a platform for quantifying morphogenesis in 4D. Elife, 4, e05864.

Montenegro-Johnson, T.D., Stamm, P., Strauss, S., Topham, A.T., Tsagris, M., Wood, A.T., Smith, R.S. and Bassel, G.W. Digital single-cell analysis of plant organ development using 3DCellAtlas.