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

Author

Listed:
  • Mamoru Matsumura

    (Nagoya University)

  • Mika Nomoto

    (Nagoya University
    Nagoya University)

  • Tomotaka Itaya

    (Nagoya University
    Nagoya University)

  • Yuri Aratani

    (Saitama University)

  • Mizuki Iwamoto

    (University of Tsukuba)

  • Takakazu Matsuura

    (Okayama University)

  • Yuki Hayashi

    (Nagoya University)

  • Tsuyoshi Mori

    (Nagoya University)

  • Michael J. Skelly

    (University of Edinburgh)

  • Yoshiharu Y. Yamamoto

    (Gifu University)

  • Toshinori Kinoshita

    (Nagoya University
    Nagoya University)

  • Izumi C. Mori

    (Okayama University)

  • Takamasa Suzuki

    (Chubu University)

  • Shigeyuki Betsuyaku

    (University of Tsukuba
    University of Tsukuba)

  • Steven H. Spoel

    (University of Edinburgh)

  • Masatsugu Toyota

    (Saitama University)

  • Yasuomi Tada

    (Nagoya University
    Nagoya University)

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.

Suggested Citation

  • Mamoru Matsumura & Mika Nomoto & Tomotaka Itaya & Yuri Aratani & Mizuki Iwamoto & Takakazu Matsuura & Yuki Hayashi & Tsuyoshi Mori & Michael J. Skelly & Yoshiharu Y. Yamamoto & Toshinori Kinoshita & I, 2022. "Mechanosensory trichome cells evoke a mechanical stimuli–induced immune response in Arabidopsis thaliana," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28813-8
    DOI: 10.1038/s41467-022-28813-8
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    References listed on IDEAS

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    1. Marie Boudsocq & Matthew R. Willmann & Matthew McCormack & Horim Lee & Libo Shan & Ping He & Jenifer Bush & Shu-Hua Cheng & Jen Sheen, 2010. "Differential innate immune signalling via Ca2+ sensor protein kinases," Nature, Nature, vol. 464(7287), pages 418-422, March.
    2. Jonathan D. G. Jones & Jeffery L. Dangl, 2006. "The plant immune system," Nature, Nature, vol. 444(7117), pages 323-329, November.
    3. Xiu-Fang Xin & Kinya Nomura & Kyaw Aung & André C. Velásquez & Jian Yao & Freddy Boutrot & Jeff H. Chang & Cyril Zipfel & Sheng Yang He, 2016. "Bacteria establish an aqueous living space in plants crucial for virulence," Nature, Nature, vol. 539(7630), pages 524-529, November.
    4. Liqun Du & Gul S. Ali & Kayla A. Simons & Jingguo Hou & Tianbao Yang & A. S. N. Reddy & B. W. Poovaiah, 2009. "Ca2+/calmodulin regulates salicylic-acid-mediated plant immunity," Nature, Nature, vol. 457(7233), pages 1154-1158, February.
    5. Musoki Mwimba & Sargis Karapetyan & Lijing Liu & Jorge Marqués & Erin M. McGinnis & Nicolas E. Buchler & Xinnian Dong, 2018. "Daily humidity oscillation regulates the circadian clock to influence plant physiology," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
    6. Mian Zhou & Wei Wang & Sargis Karapetyan & Musoki Mwimba & Jorge Marqués & Nicolas E. Buchler & Xinnian Dong, 2015. "Redox rhythm reinforces the circadian clock to gate immune response," Nature, Nature, vol. 523(7561), pages 472-476, July.
    7. Cyril Zipfel & Silke Robatzek & Lionel Navarro & Edward J. Oakeley & Jonathan D. G. Jones & Georg Felix & Thomas Boller, 2004. "Bacterial disease resistance in Arabidopsis through flagellin perception," Nature, Nature, vol. 428(6984), pages 764-767, April.
    8. Wei Wang & Jinyoung Yang Barnaby & Yasuomi Tada & Hairi Li & Mahmut Tör & Daniela Caldelari & Dae-un Lee & Xiang-Dong Fu & Xinnian Dong, 2011. "Timing of plant immune responses by a central circadian regulator," Nature, Nature, vol. 470(7332), pages 110-114, February.
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