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

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 emerging from the epidermis is visible. The undulating cells are pavement cells. In our group, we are studying the nature of the dynamic principles that drive the formation of these cellular patterns. — **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 emerging from the epidermis is visible. The undulating cells are pavement cells. In our group, we are studying the nature of the dynamic principles that drive the formation of these cellular patterns.

**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 emerging from the epidermis is visible. The undulating cells are pavement cells. In our group, we are studying the nature of the dynamic principles that drive the formation of these cellular patterns.

In developing tissues, initially equivalent cells become different from each other, and form tissues that contain 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 to patterning the epidermis of the Arabidopsis thaliana sepal. Our work suggests that noise in gene expression is one factor involved in creating cellular patterns.

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 that have been related to organ curvature control) appear scattered, interspersed between undulating pavement cells. In each of these different patterns, we are evaluating how important the noise in gene expression is for initiating patterning, and how cell-to-cell interactions, cell growth and division affect the patterning process. Our ultimate goal is to understand how specific combinations of the different patterns arise.

Dynamics of developmental transitions

Figure 2. Microscopy image of the Arabidopsis shoot apical meristem and its surrounding lateral organ primordia during the floral transition. During the floral transition, the shoot apical meristem undergoes a striking morphological change from a flat to a domed structure. In our group, we are studying how this morphogenetic process occurs. Image by M. Cerise and P. Casanova-Ferrer. — **Figure 2.** **Microscopy image of the Arabidopsis shoot apical meristem and its surrounding lateral organ primordia during the floral transition**. During the floral transition, the shoot apical meristem undergoes a striking morphological change from a flat to a domed structure. In our group, we are studying how this morphogenetic process occurs. Image by M. Cerise and P. Casanova-Ferrer.

**Figure 2.** **Microscopy image of the Arabidopsis shoot apical meristem and its surrounding lateral organ primordia during the floral transition**. During the floral transition, the shoot apical meristem undergoes a striking morphological change from a flat to a domed structure. In our group, we are studying how this morphogenetic process occurs. Image by M. Cerise and P. Casanova-Ferrer.

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.

Currently, at the MPIPZ, we are exploring how spatio-temporal patterns of gene expression drive the initiation of flowering in the Arabidopsis shoot apical meristem, which is the tissue that produces the plant aerial organs. We are proposing new models that incorporate the interplay of the environmental cues with the molecular pathways that drive the flowering process. In parallel, we are generating quantitative image analysis pipelines to better understand the patterning process throughout the floral transition. This work is in collaboration with the Coupland group at the MPIPZ.

Selected publications

Abley*, K., Formosa-Jordan*, P., Tavares, H., Chan, E. Y. T., Afsharinafar, M., Leyser^, O. and Locke^, J. C.W. (2021) An ABA-GA bistable switch can account for natural variation in the variability of Arabidopsis seed germination time. eLife; 10:e59485. Link

Bertran Garcia de Olalla*, E., Cerise*, M., Rodríguez-Maroto, G., Casanova-Ferrer, P., Vayssières, A., Severing, E., López Sampere, Y., Wang, K., Schäfer, S., Formosa-Jordan, P. and Coupland, G. (2024). Coordination of shoot apical meristem shape and identity by APETALA2 during floral transition in Arabidopsis. Nature Communications, 15(1), 6930. Link

Clark*, F. K., Weissbart*, G., Wang*, X., Harline, K., Li, C., Formosa-Jordan^, P., & Roeder^ and A. H. K. (2024). A common pathway controls cell size in the sepal and leaf epidermis leading to a non-random pattern of giant cells. bioRxiv. 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

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

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. Link

Vijaya Batthula*, L.V., Russell*, N.J., Bagde, S.R., Saint-Antoine, M., Brownfield, B., Mughal, S., Apprill, L. E., Khosla, A., Clark, F. K., Schwarz, E. M., Alseekh, S., Fernie, A.R., Singh, A., Schrick, K., Fromme, J. C., Skirycz, A., Formosa-Jordan^, P. and Roeder^, A. H.R. (2024) The transcription factor ATML1 maintains giant cell identity by inducing synthesis of its own long-chain fatty acid-containing ligands. bioRxiv. Link

(*: equal contributors; ^: co-corresponding authors)

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