Heather M, Meyer, José, Teles, Pau, Formosa-Jordan, Yassin, Refahi, Rita, San-Bento, Gwyneth, Ingram, Henrik, Jönsson, James C W, Locke, and Adrienne H K, Roeder
Multicellular development produces patterns of specialized cell types. Yet, it is often unclear how individual cells within a field of identical cells initiate the patterning process. Using live imaging, quantitative image analyses and modeling, we show that during Arabidopsis thaliana sepal development, fluctuations in the concentration of the transcription factor ATML1 pattern a field of identical epidermal cells to differentiate into giant cells interspersed between smaller cells. We find that ATML1 is expressed in all epidermal cells. However, its level fluctuates in each of these cells. If ATML1 levels surpass a threshold during the G2 phase of the cell cycle, the cell will likely enter a state of endoreduplication and become giant. Otherwise, the cell divides. Our results demonstrate a fluctuation-driven patterning mechanism for how cell fate decisions can be initiated through a random yet tightly regulated process. DOI: http://dx.doi.org/10.7554/eLife.19131.001, eLife digest Plant and animal organs contain several types of cells that perform different roles. As a plant or animal develops, these different cell types can form intricate patterns. To start the pattern, a few cells within a group of identical cells must somehow become different from their neighbors. Some patterns of cells are very well organized and easily reproduced. However, sometimes cells spontaneously become different from their neighbors, producing a less ordered pattern. In a plant called Arabidopsis (commonly known as Thale cress), a scattered pattern of giant cells and small cells spontaneously forms within a part of the developing flower called the sepal. A protein called ATML1 is a key regulator in the formation of giant cells, but because it is found in both giant cells and small cells, it is not clear how this regulation works. Mathematical models of this process suggest that identical cells could initially acquire subtle differences, potentially from random fluctuations in the activity of key regulatory molecules, to start the patterning process. Meyer, Teles, Formosa-Jordan et al. used a combination of microscopy, image analysis and mathematical modeling to investigate how the level of ATML1 fluctuates in cells to give rise to the pattern within the sepal. The experiments show that early in the development of the sepal, the levels of ATML1 fluctuate up and down in every sepal cell. If ATML1 reaches a high level specifically when a cell is preparing to divide, that cell will decide to become a giant cell, whereas if the level of ATML1 is low at this point, then the cell will divide and remain small. Overall, the findings of Meyer, Teles, Formosa-Jordan et al. demonstrate that fluctuations of key regulators while cells are preparing to divide are important for creating patterns during development. A future challenge is to examine whether other tissues in plants, or tissues in other organisms, use a similar mechanism to generate patterns of cells. DOI: http://dx.doi.org/10.7554/eLife.19131.002