Nature, Vol.587, No.7832, 92-+, 2020
Quinone perception in plants via leucine-rich-repeat receptor-like kinases
Quinones are produced and sensed in all kingdoms of life(1-4). Plants are primary producers of quinone(1,2), 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 useArabidopsis thalianaand DMBQ as a model plant and quinone to show that DMBQ signalling occurs inArabidopsisvia elevation of cytosolic Ca(2)(+)concentration. We performed a forward genetic screen inArabidopsisthat isolated DMBQ-unresponsive mutants, which we namedcannot respond to DMBQ 1(card1). TheCANNOT RESPOND TO DMBQ 1(CARD1;At5g49760, also known asHPCA1) gene encodes a leucine-rich-repeat receptor-like kinase that is highly conserved in land plants. InArabidopsis, DMBQ triggers defence-related gene expression, andcard1mutants show impaired immunity against bacterial pathogens. InPhtheirospermum japonicum(a plant that parasitizes roots), DMBQ initiates Ca(2+)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 Ca(2+)concentration in thecard1mutant. 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. Dimethoxy-1,4-benzoquinone signalling occurs inArabidopsisand in the root parasitePhtheirospermum japonicumvia increases in cytosolic Ca(2+)concentration mediated by the leucine-rich-repeat receptor-like kinase CARD1 inArabidopsis, or by its homologues inP. japonicum.