Tissue-wide Mechanical Forces Influence the Polarity of Stomatal Stem Cells in Arabidopsis

Mechanical information is an important contributor to cell polarity in uni- and multicellular systems [1-3]. In planar tissues like the Drosophila wing, cell polarity reorients during growth as cells divide and reorganize [4]. In another planar tissue, the Arabidopsis leaf epidermis [5], polarized, asymmetric divisions of stomatal stem cells (meristemoid mother cells [MMCs]) are fundamental for the generation and patterning of multiple cell types, including stomata. The activity of key transcription factors, polarizing factors [6], and peptide signals [7] explains some local stomatal patterns emerging from the behavior of a few lineally related cells [6, 8-11]. Here we demonstrate that, in addition to locally acting signals, tissue-wide mechanical forces can act as organizing cues, and that they do so by influencing the polarity of individual MMCs. If the mechanical stress environment in the tissue is altered through stretching or cell ablations, cellular polarity changes in response. In turn, polarity predicts the orientation of cellular and tissue outgrowth, leading to increased mechanical conflicts between neighboring cells. This interplay among growth, oriented divisions, and cell specification could contribute to the characteristic patterning of stomatal guard cells in the context of a growing leaf.