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Termination of asymmetric cell division and differentiation of stomata

Abstract

Stomata consist of a pair of guard cells that mediate gas and water-vapour exchange between plants and the atmosphere. Stomatal precursor cells—meristemoids—possess a transient stem-cell-like property and undergo several rounds of asymmetric divisions before further differentiation. Here we report that the Arabidopsis thaliana basic helix–loop–helix (bHLH) protein MUTE is a key switch for meristemoid fate transition. In the absence of MUTE, meristemoids abort after excessive asymmetric divisions and fail to differentiate stomata. Constitutive overexpression of MUTE directs the entire epidermis to adopt guard cell identity. MUTE has two paralogues: FAMA, a regulator of guard cell morphogenesis, and SPEECHLESS (SPCH). We show that SPCH directs the first asymmetric division that initiates stomatal lineage. Together, SPCH, MUTE and FAMA bHLH proteins control stomatal development at three consecutive steps: initiation, meristemoid differentiation and guard cell morphogenesis. Our findings highlight the roles of closely related bHLHs in cell type differentiation in plants and animals.

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Figure 1: MUTE is required for meristemoid differentiation.
Figure 2: Genetic interactions between MUTE and known regulators of stomatal patterning and differentiation.
Figure 3: MUTE bHLH protein triggers stomatal differentiation.
Figure 4: SPCH a paralogue of MUTE , initiates stomatal cell lineages.

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Acknowledgements

We thank C. Doe, B. Wakimoto, J. McAbee, and T. Kakimoto for commenting on the manuscript; F. Sack and T. Altmann for a gift of flp, sdd1 and TMM::TMM–GFP; S. Poethig and D. Bergmann for E994; T. Nakagawa and ABRC for cloning vectors; SIGnAL and ABRC for T-DNA insertion lines; and P. Chan for confocal microscopy expertise. Our thanks to D. Bergmann for sharing unpublished results and discussion about stomatal development. This work was supported in part by the grants from DOE and NSF to K.U.T. L.J.P. was supported by the NRI USDA/CSREES fellowship, and K.U.T. is a CREST JST investigator.

Author Contributions K.U.T. supervised the entire project. K.U.T. and L.J.P. conceived and designed the experiments, and wrote the manuscript with comments from co-authors. L.J.P. isolated the mute mutant and performed characterization of mutants and transgenic plants with N.L.B. D.B.S. identified the MUTE gene by map-based cloning.

The NCBI/GenBank accession numbers for the genes described in this manuscript are: DQ863645 (MUTE mRNA), DQ864972 (MUTE genomic) and DQ868373 (SPCH mRNA).

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Correspondence to Keiko U. Torii.

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Supplementary information

Supplementary Information

This file contains Supplementary Methods, Supplementary Figures 1-6 and additional references. (PDF 4761 kb)

Supplementary Table 1

This file contains Supplementary Table 1 which shows PCR markers and their primer DNA sequence for genotypic analysis of stomatal development mutants. (XLS 18 kb)

Supplementary Table 2

This file contains Supplementary Table 2 which shows CAPS and dCAPS PCR markers and their primer DNA sequence used for map-based cloning of MUTE. (XLS 200 kb)

Supplementary Table 3a

This file contains Supplementary Table 3 which shows PCR primers and DNA sequence used for plasmid construction. (XLS 9 kb)

Supplementary Table 3b

This file contains Supplementary Table 3 which shows PCR primers and DNA sequence used for RT-PCR.. (XLS 16 kb)

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Pillitteri, L., Sloan, D., Bogenschutz, N. et al. Termination of asymmetric cell division and differentiation of stomata. Nature 445, 501–505 (2007). https://doi.org/10.1038/nature05467

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