Reports

Stomatal Patterning and Differentiation by Synergistic Interactions of Receptor Kinases

Elena D. Shpak,^1,2* Jessica Messmer McAbee,^1,2* Lynn Jo Pillitteri,¹ Keiko U. Torii^1,2

Coordinated spacing and patterning of stomata allow efficient gas exchange between plants and the atmosphere. Here we report that three ERECTA (ER)–family leucine-rich repeat–receptor-like kinases (LRR-RLKs) together control stomatal patterning, with specific family members regulating the specification of stomatal stem cell fate and the differentiation of guard cells. Loss-of-function mutations in all three ER-family genes cause stomatal clustering. Genetic interactions with a known stomatal patterning mutant too many mouths (tmm) revealed stoichiometric epistasis and combination-specific neomorphism. Our findings suggest that the negative regulation of ER-family RLKs by TMM, which is an LRR receptor–like protein, is critical for proper stomatal differentiation.

¹ Department of Biology, University of Washington, Seattle, WA 98195, USA.
² Core Research for Evolutional Science and Technology, Japan Science and Technology Agency, Saitama, 332-0012, Japan.

^* These authors contributed equally to this work.

To whom correspondence should be addressed. E-mail: ktorii{at}u.washington.edu

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Regulation of Arabidopsis Early Anther Development by the Mitogen-Activated Protein Kinases, MPK3 and MPK6, and the ERECTA and Related Receptor-Like Kinases.

C. L.H. Hord, Y.-J. Sun, L. J. Pillitteri, K. U. Torii, H. Wang, S. Zhang, and H. Ma (2008)
Mol Plant 1, 645-658
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SCREAM/ICE1 and SCREAM2 Specify Three Cell-State Transitional Steps Leading to Arabidopsis Stomatal Differentiation.

M. M. Kanaoka, L. J. Pillitteri, H. Fujii, Y. Yoshida, N. L. Bogenschutz, J. Takabayashi, J.-K. Zhu, and K. U. Torii (2008)
PLANT CELL 20, 1775-1785
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The bHLH Protein, MUTE, Controls Differentiation of Stomata and the Hydathode Pore in Arabidopsis.

L. J. Pillitteri, N. L. Bogenschutz, and K. U. Torii (2008)
Plant Cell Physiol. 49, 934-943
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A Genome-Wide Functional Investigation into the Roles of Receptor-Like Proteins in Arabidopsis.

G. Wang, U. Ellendorff, B. Kemp, J. W. Mansfield, A. Forsyth, K. Mitchell, K. Bastas, C.-M. Liu, A. Woods-Tor, C. Zipfel, et al. (2008)
Plant Physiology 147, 503-517
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Signaling of cell fate determination by the TPD1 small protein and EMS1 receptor kinase.

G. Jia, X. Liu, H. A. Owen, and D. Zhao (2008)
PNAS 105, 2220-2225
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The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule.

K. Hara, R. Kajita, K. U. Torii, D. C. Bergmann, and T. Kakimoto (2007)
Genes & Dev. 21, 1720-1725
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The Arabidopsis D-Type Cyclin CYCD4 Controls Cell Division in the Stomatal Lineage of the Hypocotyl Epidermis.

A. Kono, C. Umeda-Hara, S. Adachi, N. Nagata, M. Konomi, T. Nakagawa, H. Uchimiya, and M. Umeda (2007)
PLANT CELL 19, 1265-1277
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Making Holes in Leaves: Promoting Cell State Transitions in Stomatal Development.

M. K. Barton (2007)
PLANT CELL 19, 1140-1143
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Stomatal Development and Patterning Are Regulated by Environmentally Responsive Mitogen-Activated Protein Kinases in Arabidopsis.

H. Wang, N. Ngwenyama, Y. Liu, J. C. Walker, and S. Zhang (2007)
PLANT CELL 19, 63-73
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Arabidopsis FAMA Controls the Final Proliferation/Differentiation Switch during Stomatal Development.

K. Ohashi-Ito and D. C. Bergmann (2006)
PLANT CELL 18, 2493-2505
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Mutations in ABO1/ELO2, a Subunit of Holo-Elongator, Increase Abscisic Acid Sensitivity and Drought Tolerance in Arabidopsis thaliana..

Z. Chen, H. Zhang, D. Jablonowski, X. Zhou, X. Ren, X. Hong, R. Schaffrath, J.-K. Zhu, and Z. Gong (2006)
Mol. Cell. Biol. 26, 6902-6912
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The BAM1/BAM2 Receptor-Like Kinases Are Important Regulators of Arabidopsis Early Anther Development.

C. L.H. Hord, C. Chen, B. J. DeYoung, S. E. Clark, and H. Ma (2006)
PLANT CELL 18, 1667-1680
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Microtubule arrays and Arabidopsis stomatal development.

J. R. Lucas, J. A. Nadeau, and F. D. Sack (2006)
J. Exp. Bot. 57, 71-79
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Systemic signalling of environmental cues in Arabidopsis leaves.

S. A. Coupe, B. G. Palmer, J. A. Lake, S. A. Overy, K. Oxborough, F. I. Woodward, J. E. Gray, and W. P. Quick (2006)
J. Exp. Bot. 57, 329-341
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Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASES1 and 2 Are Essential for Tapetum Development and Microspore Maturation.

J. Colcombet, A. Boisson-Dernier, R. Ros-Palau, C. E. Vera, and J. I. Schroeder (2005)
PLANT CELL 17, 3350-3361
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Evolutionary Expansion, Gene Structure, and Expression of the Rice Wall-Associated Kinase Gene Family.

S. Zhang, C. Chen, L. Li, L. Meng, J. Singh, N. Jiang, X.-W. Deng, Z.-H. He, and P. G. Lemaux (2005)
Plant Physiology 139, 1107-1124
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The Arabidopsis R2R3 MYB Proteins FOUR LIPS and MYB88 Restrict Divisions Late in the Stomatal Cell Lineage.

L. B. Lai, J. A. Nadeau, J. Lucas, E.-K. Lee, T. Nakagawa, L. Zhao, M. Geisler, and F. D. Sack (2005)
PLANT CELL 17, 2754-2767
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