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

Xiaoyu Guo; Xue Ding; Juan Dong

doi:https://doi.org/10.1038/s41467-022-30254-2

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

Xiaoyu Guo, Xue Ding, Juan Dong

Waksman Institute of Microbiology

Rutgers, The State University

Research output: Contribution to journal › Article › peer-review

Abstract

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.

Original language	English (US)
Article number	2438
Journal	Nature communications
Volume	13
Issue number	1
DOIs	https://doi.org/10.1038/s41467-022-30254-2
State	Published - Dec 2022

ASJC Scopus subject areas

Chemistry(all)
Biochemistry, Genetics and Molecular Biology(all)
General
Physics and Astronomy(all)

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https://doi.org/10.1038/s41467-022-30254-2

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title = "Dichotomy of the BSL phosphatase signaling spatially regulates MAPK components in stomatal fate determination",

abstract = "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.",

author = "Xiaoyu Guo and Xue Ding and Juan Dong",

note = "Funding Information: We thank Dr. Dongtao Ren (China Agricultural University) and Dr. Zhiyong Wang (Stanford University) for sharing plant reagents and DNA resources. We thank Dr. Tsuyoshi Nakagawa (Shimane University) for sharing the R4 Gateway Binary Vectors (R4pGWB). We thank the ABRC stock center for providing T-DNA insertional mutants. This research was supported by grants from the National Institute of Health GM109080 and GM131827 to J.D. J.D. is also supported by grants from the National Science Foundation 2049642, 1952823, and 1851907. Funding Information: We thank Dr. Dongtao Ren (China Agricultural University) and Dr. Zhiyong Wang (Stanford University) for sharing plant reagents and DNA resources. We thank Dr. Tsuyoshi Nakagawa (Shimane University) for sharing the R4 Gateway Binary Vectors (R4pGWB). We thank the ABRC stock center for providing T-DNA insertional mutants. This research was supported by grants from the National Institute of Health GM109080 and GM131827 to J.D. J.D. is also supported by grants from the National Science Foundation 2049642, 1952823, and 1851907. Publisher Copyright: {\textcopyright} 2022, The Author(s).",

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doi = "https://doi.org/10.1038/s41467-022-30254-2",

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AU - Ding, Xue

AU - Dong, Juan

N1 - Funding Information: We thank Dr. Dongtao Ren (China Agricultural University) and Dr. Zhiyong Wang (Stanford University) for sharing plant reagents and DNA resources. We thank Dr. Tsuyoshi Nakagawa (Shimane University) for sharing the R4 Gateway Binary Vectors (R4pGWB). We thank the ABRC stock center for providing T-DNA insertional mutants. This research was supported by grants from the National Institute of Health GM109080 and GM131827 to J.D. J.D. is also supported by grants from the National Science Foundation 2049642, 1952823, and 1851907. Funding Information: We thank Dr. Dongtao Ren (China Agricultural University) and Dr. Zhiyong Wang (Stanford University) for sharing plant reagents and DNA resources. We thank Dr. Tsuyoshi Nakagawa (Shimane University) for sharing the R4 Gateway Binary Vectors (R4pGWB). We thank the ABRC stock center for providing T-DNA insertional mutants. This research was supported by grants from the National Institute of Health GM109080 and GM131827 to J.D. J.D. is also supported by grants from the National Science Foundation 2049642, 1952823, and 1851907. Publisher Copyright: © 2022, The Author(s).

PY - 2022/12

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N2 - 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.

AB - 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.

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

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