Quantitative approaches to multicellular dynamics in plant development

Throughout plant development, cells grow, divide and become different from one another to form tissues and organs that perform specific functions. This process results from the interplay of cell signalling, mediated by gene regulatory networks and hormonal transport, and mechanical cues, together with the integration of environmental signals such as temperature and light. We still have a limited quantitative understanding of the complex multicellular dynamics that occur in developing plant tissues, and how such dynamics result in reproducible developmental outcomes.

At the MPIPZ, we are studying the multicellular dynamics of different plant developmental processes using a combination of mathematical modelling, time-lapse microscopy and quantitative image analysis.

 

Dynamics of cellular patterning

In developing tissues, initially equivalent cells become different from each other, forming tissues containing different cell types. The arrangement of different cell types is called a cellular pattern. In our group, we are studying how complex cellular patterns are formed in different developmental contexts as a result of the interplay of cell signalling and growth.

In one collaboration with the Locke and Jönsson labs (University of Cambridge) and the Roeder Lab (University of Cornell), we found that temporal fluctuations in the cellular concentration of a transcription factor contribute in patterning the epidermis of the Arabidopsis sepal. Our work suggests that noise in gene expression is one factor in creating cellular patterns.

After arriving recently at the MPIPZ, we are continuing to investigate how patterning is generated in the epidermis. In the leaf epidermis, a combination of cellular patterns arises. Across the blade, trichomes (protective hair cells), stomata (gas exchange cells), and giant cells (large cells which have been related to organ curvature control) appear scattered, interspersed between undulated pavement cells. In each of these different patterns, we are evaluating how important noise in gene expression is for patterning initiation, and how cell-to-cell interactions, cell growth and division affect the patterning process itself. Our final goal is to understand how specific combinations of the different patterns arise.

Figure 1: Microscopy image showing the arrangement of different cell types in the Arabidopsis leaf epidermis. Cell outlines are shown in yellow (MYR-YFP marker), and cell nuclei are shown in magenta (H2B-RFP marker).

In this image, stomata cells appear scattered throughout the epidermis (small yellow ellipsoid-shaped cell pairs), and a large trichome coming out of the epidermis is visible. The undulated-shaped cells are pavement cells. In our group we are studying what are the dynamical principles driving the formation of these cellular patterns.

Dynamics of developmental transitions

Plants undergo striking developmental transitions throughout development such as seed germination or floral induction. These processes can be understood as rich multicellular dynamic systems that are continuously modulated by environmental cues. Little is known about the dynamics of the key regulators of these complex developmental processes at the single cell and multicellular levels.

In a recent collaboration with the Leyser and Locke groups (University of Cambridge) we modelled the dynamics of the gene regulatory network underlying seed germination to understand why seeds exposed to the same environmental conditions germinated at different times. Our results indicate that variability in seed germination times can be understood as an emergent property of noise in gene expression, and that the variability range can be modulated by the properties of the underlying genetic network for seed germination.

In collaboration with the Coupland group at the MPIPZ, we will explore how spatio-temporal patterns of gene expression at both single cell and tissue levels drive the initiation of flowering. Our group will generate multicellular models that incorporate the interplay of the environmental cues with the molecular pathways that drive the flowering process.

 

Selected publications

Abley*, K., Formosa-Jordan*, P., Tavares, H., Chan, E., Leyser, O. and Locke, J. C.W. (2020) An ABA-GA bistable switch can account for natural variation in the variability of Arabidopsis seed germination time. BioRxiv. Link

Landrein, B., Formosa-Jordan, P., Malivert, A., Schuster, C., Melnyk, C. W., Yang, W., Turnbull, C., Meyerowitz, E. M., Locke, J. C.W. and Jönsson, H. (2018) Nitrate modulates stem cell dynamics in Arabidopsis shoot meristems through cytokinins. Proc. Nat. Acad. Sci. USA. 115:1382-1387. Link

Formosa-Jordan*, P., Teles*, J. and Jönsson, H. (2018) Single-cell approaches for understanding morphogenesis using Computational Morphodynamics. In: Morris R. (eds) Mathematical Modelling in Plant Biology. Springer, Cham Link

Fàbregas*, N., Formosa-Jordan*, P., Ibañes, M. and Caño-Delgado, A. I.  (2017) Experimental and Theoretical Methods to Approach the Study of Vascular Patterning in the Plant Shoot.  In "Xylem - Methods and Protocols", Methods in Molecular Biology, ed. M. de Lucas and J. Peter Etchells. Springer Science+Business Media, New York. (*: equal contributors) Link

Meyer*, H. M., Teles*, J., Formosa-Jordan*, P., Refahi, Y., San-Bento, R., Ingram, G., Jönsson, H., Locke, J. C.W. and Roeder, A. H.K. (2017) Fluctuations of the transcription factor ATML1 generate the pattern of giant cells in the Arabidopsis sepal. eLife, 10.7554/eLife.19131. (*: equal contributors)  Link

Fàbregas*, N.,  Formosa-Jordan*, P., Confraria*, A., Siligato, R., Alonso, J. M., Swarup, R., Bennett, M. J., Pekka Mähönen, A., Caño-Delgado, A. I. and Ibañes, M. (2015) Influx carriers control vascular patterning and xylem differentiation in Arabidopsis thaliana. PLoS Genetics11(4): e1005183. doi:10.1371/journal.pgen.1005183. (*: equal contributors)  Link

 

To see the full list of publications, see the following Link

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