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Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway

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Abstract

Plants must coordinate the regulation of biochemistry and anatomy to optimize photosynthesis and water-use efficiency. The formation of stomata, epidermal pores that facilitate gas exchange, is highly coordinated with other aspects of photosynthetic development. The signalling pathways controlling stomata development are not fully understood1,2, although mitogen-activated protein kinase (MAPK) signalling is known to have key roles. Here we demonstrate in Arabidopsis that brassinosteroid regulates stomatal development by activating the MAPK kinase kinase (MAPKKK) YDA (also known as YODA). Genetic analyses indicate that receptor kinase-mediated brassinosteroid signalling inhibits stomatal development through the glycogen synthase kinase 3 (GSK3)-like kinase BIN2, and BIN2 acts upstream of YDA but downstream of the ERECTA family of receptor kinases. Complementary in vitro and in vivo assays show that BIN2 phosphorylates YDA to inhibit YDA phosphorylation of its substrate MKK4, and that activities of downstream MAPKs are reduced in brassinosteroid-deficient mutants but increased by treatment with either brassinosteroid or GSK3-kinase inhibitor. Our results indicate that brassinosteroid inhibits stomatal development by alleviating GSK3-mediated inhibition of this MAPK module, providing two key links; that of a plant MAPKKK to its upstream regulators and of brassinosteroid to a specific developmental output.

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Figure 1: Brassinosteroid negatively regulates stomatal development.
Figure 2: Arabidopsis GSK3 acts downstream of ERECTA family and TMM but upstream of YDA in the stomatal development signalling pathway.
Figure 3: BIN2 inhibits YDA kinase activity through phosphorylation.

Change history

  • 08 February 2012

    The original supplementary information file posted online was incorrect and has been replaced.

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Acknowledgements

We thank K. Torii for providing seeds of the er erl1 erl2 triple mutant and scrm-D mutant, J.-M. Zhou for providing the HOPAI1 transgenic line and J. Li for providing the bin2-3 bil1 bil2 triple mutant. Research was primarily supported by a grant from the National Institutes of Health (R01GM066258), and partially supported by the US Department of Energy (DE-FG02-08ER15973) and the Herman Frasch Foundation. D.C.B. is an investigator of the Howard Hughes Medical Institute.

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T.-W.K. performed all experiments. T.-W.K. and Z.-Y.W. designed the experiments, analysed data and wrote the manuscript. M.M. cloned complementary DNAs of BSL2 and BSL3, and BSL2pro-BSL2. D.C.B. contributed materials and wrote the manuscript.

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Correspondence to Zhi-Yong Wang.

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The authors declare no competing financial interests.

Supplementary information

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This file contains Supplementary Figures 1-13 with legends. The original file posted online was incorrect and was replaced on 8 February 2012. (PDF 4371 kb)

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Kim, TW., Michniewicz, M., Bergmann, D. et al. Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway. Nature 482, 419–422 (2012). https://doi.org/10.1038/nature10794

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