Dichotomy of the BSL phosphatase signaling spatially regulates MAPK components in stomatal fate determination

• Published in: Nature communications Vol. 13; no. 1; p. 2438
• Main Authors: Guo, Xiaoyu, Ding, Xue, Dong, Juan
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 04.05.2022; Nature Publishing Group; Nature Portfolio
• Subjects: 14; 14/19; 631/449/2124; 631/449/2653/2658; 631/449/2675; 82/1; 82/83; 96; Arabidopsis; Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Biological activity; Biological Phenomena; Deactivation; Gene Expression Regulation, Plant; Humanities and Social Sciences; Kinases; MAP kinase; MAPKK kinase; Mitogen-Activated Protein Kinase Kinases - genetics; Mitogen-Activated Protein Kinase Kinases - metabolism; multidisciplinary; Nuclei (cytology); Phosphatase; Phosphoric Monoester Hydrolases - metabolism; Proteins; Science; Science (multidisciplinary); Signaling; Stomata; Transcription factors
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-022-30254-2

MAPK signaling modules play crucial roles in regulating numerous biological processes in all eukaryotic cells. How MAPK signaling specificity and strength are tightly controlled remains a major challenging question. In Arabidopsis stomatal development, the MAPKK Kinase YODA (YDA) functions at the cell periphery to inhibit stomatal production by activating MAPK 3 and 6 (MPK3/6) that directly phosphorylate stomatal fate-determining transcription factors for degradation in the nucleus. Recently, we demonstrated that BSL1, one of the four BSL protein phosphatases, localizes to the cell cortex to activate YDA, elevating MPK3/6 activity to suppress stomatal formation. Here, we showed that at the plasma membrane, all four members of BSL proteins contribute to the YDA activation. However, in the nucleus, specific BSL members (BSL2, BSL3, and BSU1) directly deactivate MPK6 to counteract the linear MAPK pathway, thereby promoting stomatal formation. Thus, the pivotal MAPK signaling in stomatal fate determination is spatially modulated by a signaling dichotomy of the BSL protein phosphatases in Arabidopsis , providing a prominent example of how MAPK activities are integrated and specified by signaling compartmentalization at the subcellular level. In Arabidopsis, BSL1 localizes to the cell cortex and activates the MAPKK Kinase YDA to inhibit stomatal production. Here the authors show that three other BSL proteins BSL2, BSL3, and BSU1 act in the nucleus to deactivate MPK6 and promote stomatal formation.