Abstract

Plants, as sessile organisms, rapidly sense, transduce and respond to different substances. While quinone-derived compounds are produced ubiquitiously in the environment across all kingdoms, with plants as the primary producers, they are often neglected in plant signalling research. Quinone-sensing components are well-studied in bacteria (e.g. YodB) and animals (e.g Nrf2/Keap1), but no molecular components have yet been presented in plants. One well-studied response in plants is the formation of the haustorium, a feeding structure in Orobanchaceae parasitic plants, upon sensing 2,6 dimethoxy-1,4-benzoquinone (DMBQ), which was isolated from sorghum root extract. However, elucidating the molecular mechanism of DMBQ perception in parasitic plants is challenging since key research tools are limited. Furthermore, the role of quinones as signals in non-parasitic plants is enigmatic since they do not form haustoria. Here we used DMBQ and Arabidopsis, as a model quinone and plant respectively, and showed that DMBQ induces various hallmarks of a signalling event in Arabidopsis at low-micromolar concentrations. In search for its cognate receptor, a forward genetic screen, using calcium reporters, was employed and 13 mutants were obtained and designated as CAnnot Respond to DMBQ 1 (card1) mutants. Genetic analysis and next-generation sequencing revealed that all 13 card1 mutants contain mutations in a single locus. CARD1 encodes an uncharacterised receptor-like kinase, whose homologues are present throughout land plant lineages. DMBQ induces a unique set of transcripts which is absent in card1 mutants. Furthermore, different types of quinones are capable of inducing [Ca2+]cyt increases in Arabidopsis at nanomolar concentrations and are CARD1 dependent, suggesting that quinones are bona fide signalling agents which are perceived by CARD1 . The role of quinones and CARD1 in non-parasitic plants, with respect to parasitic plants, and possible sensing mechanisms, will be shown and discussed. Altogether, this work paves the way to further unravel the importance of quinones as signalling agents and CARD1 functions in plants.