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

Anuphon Laohavisit, Takanori Wakatake, Nobuaki Ishihama, Hugh Mulvey, Kaori Takizawa, Takamasa Suzuki and Ken Shirasu ()
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Anuphon Laohavisit: RIKEN Center for Sustainable Resource Science
Takanori Wakatake: RIKEN Center for Sustainable Resource Science
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

Nature, 2020, vol. 587, issue 7832, 92-97

Abstract: 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.

Date: 2020
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DOI: 10.1038/s41586-020-2655-4

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