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Quinone perception in plants via leucine-rich-repeat receptor-like kinases

Author

Listed:
  • Anuphon Laohavisit

    (RIKEN Center for Sustainable Resource Science)

  • Takanori Wakatake

    (RIKEN Center for Sustainable Resource Science
    The University of Tokyo)

  • Nobuaki Ishihama

    (RIKEN Center for Sustainable Resource Science)

  • Hugh Mulvey

    (RIKEN Center for Sustainable Resource Science)

  • Kaori Takizawa

    (RIKEN Center for Sustainable Resource Science)

  • Takamasa Suzuki

    (Chubu University)

  • Ken Shirasu

    (RIKEN Center for Sustainable Resource Science
    The University of Tokyo)

Abstract

Quinones are produced and sensed in all kingdoms of life1–4. Plants are primary producers of quinone1,2, but the role of quinone as a signalling agent in plants remains largely unknown. One well-documented role of quinone is in the induction of haustoria (specialized feeding structures) in plants that parasitize roots, which occurs in the presence of the host-derived quinone compound 2,6-dimethoxy-1,4-benzoquinone (DMBQ)5. However, how parasitic plants sense DMBQ remains unclear, as is whether nonparasitic plants are capable of sensing quinones. Here we use Arabidopsis thaliana and DMBQ as a model plant and quinone to show that DMBQ signalling occurs in Arabidopsis via elevation of cytosolic Ca2+ concentration. We performed a forward genetic screen in Arabidopsis that isolated DMBQ-unresponsive mutants, which we named cannot respond to DMBQ 1 (card1). The CANNOT RESPOND TO DMBQ 1 (CARD1; At5g49760, also known as HPCA1) gene encodes a leucine-rich-repeat receptor-like kinase that is highly conserved in land plants. In Arabidopsis, DMBQ triggers defence-related gene expression, and card1 mutants show impaired immunity against bacterial pathogens. In Phtheirospermum japonicum (a plant that parasitizes roots), DMBQ initiates Ca2+ signalling in the root and is important for the development of the haustorium. Furthermore, CARD1 homologues from this parasitic plant complement DMBQ-induced elevation of cytosolic Ca2+ concentration in the card1 mutant. Our results demonstrate that plants—unlike animals and bacteria—use leucine-rich-repeat receptor-like kinases for quinone signalling. This work provides insights into the role of quinone signalling and CARD1 functions in plants that help us to better understand the signalling pathways used during the formation of the haustorium in parasitic plants and in plant immunity in nonparasitic plants.

Suggested Citation

  • Anuphon Laohavisit & Takanori Wakatake & Nobuaki Ishihama & Hugh Mulvey & Kaori Takizawa & Takamasa Suzuki & Ken Shirasu, 2020. "Quinone perception in plants via leucine-rich-repeat receptor-like kinases," Nature, Nature, vol. 587(7832), pages 92-97, November.
  • Handle: RePEc:nat:nature:v:587:y:2020:i:7832:d:10.1038_s41586-020-2655-4
    DOI: 10.1038/s41586-020-2655-4
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    Citations

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    Cited by:

    1. Anna Kokla & Martina Leso & Xiang Zhang & Jan Simura & Phanu T. Serivichyaswat & Songkui Cui & Karin Ljung & Satoko Yoshida & Charles W. Melnyk, 2022. "Nitrogen represses haustoria formation through abscisic acid in the parasitic plant Phtheirospermum japonicum," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    2. Du-Hwa Lee & Ho-Seok Lee & Min-Soo Choi & Katarzyna Parys & Kaori Honda & Yasumitsu Kondoh & Jung-Min Lee & Natalie Edelbacher & Geon Heo & Balaji Enugutti & Hiroyuki Osada & Ken Shirasu & Youssef Bel, 2024. "Reprogramming of flagellin receptor responses with surrogate ligands," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    3. Satoshi Ogawa & Songkui Cui & Alexandra R. F. White & David C. Nelson & Satoko Yoshida & Ken Shirasu, 2022. "Strigolactones are chemoattractants for host tropism in Orobanchaceae parasitic plants," Nature Communications, Nature, vol. 13(1), pages 1-11, December.

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