Journal
DEVELOPMENTAL CELL
Volume 57, Issue 5, Pages 569-+Publisher
CELL PRESS
DOI: 10.1016/j.devcel.2022.01.014
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Funding
- MEXT KAKENHI [17H06476]
- WPI-ITbM
- UT Austin
- Spanish Ministry of Science and Innovation [RTI2018-094793-B-I00]
- European Research Council [2018-AdG_833617]
- Howard Hughes Medical Institute
- Johnson & Johnson Centennial Chair in Plant Cell Biology at the UT Austin
- Young Leader Cultivation Program from Nagoya University
- Walter Benjamin Program, Deutsche Forschungsgemeinschaft [447617898]
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This study reveals that precise cell-cycle control is crucial for the differentiation and formation of plant stomata. The identification of SMR4 as a molecular brake induced by MUTE provides insight into the regulation of cell cycle in stomatal-lineage cells. The interaction between SMR4 and specific cyclins highlights the importance of timely proliferative cell cycle for stomatal-lineage identity.
Differentiation of specialized cell types requires precise cell-cycle control. Plant stomata are generated through asymmetric divisions of a stem-cell-like precursor followed by a single symmetric division that creates paired guard cells surrounding a pore. The stomatal-lineage-specific transcription factor MUTE terminates the asymmetric divisions and commits to differentiation. However, the role of cell-cycle machineries in this transition remains unknown. We discover that the symmetric division is slower than the asymmetric division in Arabidopsis. We identify a plant-specific cyclin-dependent kinase inhibitor, SIAMESE-RELATED4 (SMR4), as a MUTE-induced molecular brake that decelerates the cell cycle. SMR4 physically and functionally associates with CYCD3;1 and extends the G1 phase of asymmetric divisions. By contrast, SMR4 fails to interact with CYCD5;1, a MUTE-induced G1 cyclin, and permits the symmetric division. Our work unravels a molecular framework of the proliferation-to-differentiation switch within the stomatal lineage and suggests that a timely proliferative cell cycle is critical for stomatal-lineage identity.
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