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A mechanistic framework for noncell autonomous stem cell induction in Arabidopsis

Significance Cell–cell communication is a prerequisite of multicellular development and noncell autonomous stem cell induction has been conserved during evolution. Cytoplasmic bridges, called plasmodesmata, which facilitate the exchange of molecules between neighboring cells, are a striking innovation for cell–cell signaling in plants. Here, we show that plasmodesmata function is required for the activity of shoot apical stem cells in Arabidopsis and provide evidence that the stem cell inducing transcription factor WUSCHEL moves from the niche into the stem cells via this route. WUSCHEL movement is functionally relevant and mediated by multiple protein domains. Because parts of the protein that restrict movement are required for homodimerization, the formation of WUSCHEL dimers might contribute to the regulation of stem cell activity in Arabidopsis. Cell–cell communication is essential for multicellular development and, consequently, evolution has brought about an array of distinct mechanisms serving this purpose. Consistently, induction and maintenance of stem cell fate by noncell autonomous signals is a feature shared by many organisms and may depend on secreted factors, direct cell–cell contact, matrix interactions, or a combination of these mechanisms. Although many basic cellular processes are well conserved between animals and plants, cell-to-cell signaling is one function where substantial diversity has arisen between the two kingdoms of life. One of the most striking differences is the presence of cytoplasmic bridges, called plasmodesmata, which facilitate the exchange of molecules between neighboring plant cells and provide a unique route for cell–cell communication in the plant lineage. Here, we provide evidence that the stem cell inducing transcription factor WUSCHEL (WUS), expressed in the niche, moves to the stem cells via plasmodesmata in a highly regulated fashion and that this movement is required for WUS function and, thus, stem cell activity in Arabidopsis thaliana. We show that cell context-independent mobility is encoded in the WUS protein sequence and mediated by multiple domains. Finally, we demonstrate that parts of the protein that restrict movement are required for WUS homodimerization, suggesting that formation of WUS dimers might contribute to the regulation of apical stem cell activity.