Mechanosensory trichome cells evoke a mechanical stimuli–induced immune response in Arabidopsis thaliana

Mamoru Matsumura; Mika Nomoto; Tomotaka Itaya; Yuri Aratani; Mizuki Iwamoto; Takakazu Matsuura; Yuki Hayashi; Tsuyoshi Mori; Michael Skelly; Yoshiharu Y Yamamoto; Toshinori Kinoshita; Izumi C. Mori; Takamasa Suzuki; Shigeyuki Betsuyaku; Steven H Spoel; Masatsugu Toyota; Yasuomi Tada

doi:10.1038/s41467-022-28813-8

Mechanosensory trichome cells evoke a mechanical stimuli–induced immune response in Arabidopsis thaliana

Mamoru Matsumura, Mika Nomoto, Tomotaka Itaya, Yuri Aratani, Mizuki Iwamoto, Takakazu Matsuura, Yuki Hayashi, Tsuyoshi Mori, Michael Skelly, Yoshiharu Y Yamamoto, Toshinori Kinoshita, Izumi C. Mori, Takamasa Suzuki, Shigeyuki Betsuyaku, Steven H Spoel, Masatsugu Toyota, Yasuomi Tada

School of Biological Sciences

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

Abstract

Perception of pathogen-derived ligands by corresponding host receptors is a pivotal strategy in eukaryotic innate immunity. In plants, this is complemented by circadian anticipation of infection timing, promoting basal resistance even in the absence of pathogen threat. Here, we report that trichomes, hair-like structures on the epidermis, directly sense external mechanical forces, including raindrops, to anticipate pathogen infections in Arabidopsis thaliana. Exposure of leaf surfaces to mechanical stimuli initiates the concentric propagation of intercellular calcium waves away from trichomes to induce defence-related genes. Propagating calcium waves enable effective immunity against pathogenic microbes through the CALMODULIN-BINDING TRANSCRIPTION ACTIVATOR 3 (CAMTA3) and mitogen-activated protein kinases. We propose an early layer of plant immunity in which trichomes function as mechanosensory cells that detect potential risks.

Original language	English
Article number	1216
Number of pages	15
Journal	Nature Communications
Volume	13
Issue number	1
DOIs	https://doi.org/10.1038/s41467-022-28813-8
Publication status	Published - 8 Mar 2022

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TadaEtalNC2022MechanosensoryTrichomeCellsEvokeAMechanicalFinal published version, 7.66 MBLicence: Creative Commons: Attribution (CC-BY)

2 Finished

Understanding the influence of environmental signals on establishment of plant disease resistance
Spoel, S.
UK-based charities
16/03/18 → 15/03/20
Project: Research
IMMUNE-EXPRESS: Proteasome-Mediated Gene Expression in Plant Immunity
Spoel, S.
EU government bodies
1/03/16 → 31/08/21
Project: Research

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Matsumura, M., Nomoto, M., Itaya, T., Aratani, Y., Iwamoto, M., Matsuura, T., Hayashi, Y., Mori, T., Skelly, M., Yamamoto, Y. Y., Kinoshita, T., Mori, I. C., Suzuki, T., Betsuyaku, S., Spoel, S. H., Toyota, M., & Tada, Y. (2022). Mechanosensory trichome cells evoke a mechanical stimuli–induced immune response in Arabidopsis thaliana. Nature Communications, 13(1), [1216]. https://doi.org/10.1038/s41467-022-28813-8

@article{fae49b0ad68e4f8f916a9a18db3ece84,

title = "Mechanosensory trichome cells evoke a mechanical stimuli–induced immune response in Arabidopsis thaliana",

abstract = "Perception of pathogen-derived ligands by corresponding host receptors is a pivotal strategy in eukaryotic innate immunity. In plants, this is complemented by circadian anticipation of infection timing, promoting basal resistance even in the absence of pathogen threat. Here, we report that trichomes, hair-like structures on the epidermis, directly sense external mechanical forces, including raindrops, to anticipate pathogen infections in Arabidopsis thaliana. Exposure of leaf surfaces to mechanical stimuli initiates the concentric propagation of intercellular calcium waves away from trichomes to induce defence-related genes. Propagating calcium waves enable effective immunity against pathogenic microbes through the CALMODULIN-BINDING TRANSCRIPTION ACTIVATOR 3 (CAMTA3) and mitogen-activated protein kinases. We propose an early layer of plant immunity in which trichomes function as mechanosensory cells that detect potential risks.",

author = "Mamoru Matsumura and Mika Nomoto and Tomotaka Itaya and Yuri Aratani and Mizuki Iwamoto and Takakazu Matsuura and Yuki Hayashi and Tsuyoshi Mori and Michael Skelly and Yamamoto, {Yoshiharu Y} and Toshinori Kinoshita and Mori, {Izumi C.} and Takamasa Suzuki and Shigeyuki Betsuyaku and Spoel, {Steven H} and Masatsugu Toyota and Yasuomi Tada",

note = "Funding Information: We thank M.F. Thomashow for the seeds of CAMTA3 variants, S. Ishiguro for the seeds of cer1-1 and cer3-1, Y. Takano for Alternaria brassicicola Ryo-1, N. Nakayama, T. Kawasaki, T. Matsushita, and G. Goshima for discussion of the work. This work was supported by JSPS KAKENHI Grant Numbers JP23120520, JP25120718, and JP18K19334 (to Y.T.), JP15H05955 (to Y.T. and T.K.), and JP19H05363, JP21H00366 (to M.N.) and by Cooperative Research Grant #1707 of the Plant Transgenic Design Initiative (PTraD) by Gene Research Center, Tsukuba-Plant Innovation Research Center, the University of Tsukuba (to Y.T.). Publisher Copyright: {\textcopyright} 2022, The Author(s).",

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month = mar,

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doi = "10.1038/s41467-022-28813-8",

language = "English",

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Matsumura, M, Nomoto, M, Itaya, T, Aratani, Y, Iwamoto, M, Matsuura, T, Hayashi, Y, Mori, T, Skelly, M, Yamamoto, YY, Kinoshita, T, Mori, IC, Suzuki, T, Betsuyaku, S, Spoel, SH, Toyota, M & Tada, Y 2022, 'Mechanosensory trichome cells evoke a mechanical stimuli–induced immune response in Arabidopsis thaliana', Nature Communications, vol. 13, no. 1, 1216. https://doi.org/10.1038/s41467-022-28813-8

TY - JOUR

T1 - Mechanosensory trichome cells evoke a mechanical stimuli–induced immune response in Arabidopsis thaliana

AU - Matsumura, Mamoru

AU - Nomoto, Mika

AU - Itaya, Tomotaka

AU - Aratani, Yuri

AU - Iwamoto, Mizuki

AU - Matsuura, Takakazu

AU - Hayashi, Yuki

AU - Mori, Tsuyoshi

AU - Skelly, Michael

AU - Yamamoto, Yoshiharu Y

AU - Kinoshita, Toshinori

AU - Mori, Izumi C.

AU - Suzuki, Takamasa

AU - Betsuyaku, Shigeyuki

AU - Spoel, Steven H

AU - Toyota, Masatsugu

AU - Tada, Yasuomi

N1 - Funding Information: We thank M.F. Thomashow for the seeds of CAMTA3 variants, S. Ishiguro for the seeds of cer1-1 and cer3-1, Y. Takano for Alternaria brassicicola Ryo-1, N. Nakayama, T. Kawasaki, T. Matsushita, and G. Goshima for discussion of the work. This work was supported by JSPS KAKENHI Grant Numbers JP23120520, JP25120718, and JP18K19334 (to Y.T.), JP15H05955 (to Y.T. and T.K.), and JP19H05363, JP21H00366 (to M.N.) and by Cooperative Research Grant #1707 of the Plant Transgenic Design Initiative (PTraD) by Gene Research Center, Tsukuba-Plant Innovation Research Center, the University of Tsukuba (to Y.T.). Publisher Copyright: © 2022, The Author(s).

PY - 2022/3/8

Y1 - 2022/3/8

N2 - Perception of pathogen-derived ligands by corresponding host receptors is a pivotal strategy in eukaryotic innate immunity. In plants, this is complemented by circadian anticipation of infection timing, promoting basal resistance even in the absence of pathogen threat. Here, we report that trichomes, hair-like structures on the epidermis, directly sense external mechanical forces, including raindrops, to anticipate pathogen infections in Arabidopsis thaliana. Exposure of leaf surfaces to mechanical stimuli initiates the concentric propagation of intercellular calcium waves away from trichomes to induce defence-related genes. Propagating calcium waves enable effective immunity against pathogenic microbes through the CALMODULIN-BINDING TRANSCRIPTION ACTIVATOR 3 (CAMTA3) and mitogen-activated protein kinases. We propose an early layer of plant immunity in which trichomes function as mechanosensory cells that detect potential risks.

AB - Perception of pathogen-derived ligands by corresponding host receptors is a pivotal strategy in eukaryotic innate immunity. In plants, this is complemented by circadian anticipation of infection timing, promoting basal resistance even in the absence of pathogen threat. Here, we report that trichomes, hair-like structures on the epidermis, directly sense external mechanical forces, including raindrops, to anticipate pathogen infections in Arabidopsis thaliana. Exposure of leaf surfaces to mechanical stimuli initiates the concentric propagation of intercellular calcium waves away from trichomes to induce defence-related genes. Propagating calcium waves enable effective immunity against pathogenic microbes through the CALMODULIN-BINDING TRANSCRIPTION ACTIVATOR 3 (CAMTA3) and mitogen-activated protein kinases. We propose an early layer of plant immunity in which trichomes function as mechanosensory cells that detect potential risks.

U2 - 10.1038/s41467-022-28813-8

DO - 10.1038/s41467-022-28813-8

M3 - Article

C2 - 35260555

VL - 13

JO - Nature Communications

JF - Nature Communications

SN - 2041-1723

IS - 1

M1 - 1216

ER -

Mechanosensory trichome cells evoke a mechanical stimuli–induced immune response in Arabidopsis thaliana

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Understanding the influence of environmental signals on establishment of plant disease resistance

IMMUNE-EXPRESS: Proteasome-Mediated Gene Expression in Plant Immunity

Cite this