The jasmonoyl‐isoleucine receptor CORONATINE INSENSITIVE1 suppresses defense gene expression in Arabidopsis roots independently of its ligand

Abstract

Summary The F‐box protein CORONANTINE INSENSITIVE1 (COI1) serves as the receptor for the plant hormone jasmonoyl‐isoleucine (JA‐Ile). COI1, its co‐receptors of the JASMONATE ZIM‐domain (JAZ) protein family, and JA‐Ile form a functional unit that regulates growth or defense mechanisms in response to various stress cues. Strikingly, COI1, but not JA‐Ile, is required for susceptibility of Arabidopsis thaliana towards the soil‐borne vascular pathogen Verticillium longisporum. In order to obtain marker genes for further analysis of this JA‐Ile‐independent COI1 function, transcriptome analysis of roots of coi1 and allene oxide synthase (aos) plants (impaired in JA biosynthesis) was performed. Intriguingly, nearly all of the genes that are differentially expressed in coi1 versus aos and wild type are constitutively more highly expressed in coi1. To support our notion that COI1 acts independently of its known downstream signaling components, coi1 plants were complemented with a COI1 variant (COI1AA) that is compromised in its interaction with JAZs. As expected, these plants showed only weak induction of the expression of the JA‐Ile marker gene VEGETATIVE STORAGE PROTEIN2 after wounding and remained sterile. On the other hand, genes affected by COI1 but not by JA‐Ile were still strongly repressed by COI1AA. We suggest that COI1 has a potential moonlighting function that serves to repress gene expression in a JA‐Ile‐ and JAZ‐independent manner.

Analysis of the JA-Ile-independent function of COI1 in Arabidopsis thaliana upon infection with Verticillium longisporum

“…The genes found to be de-repressed here are largely overlapping with the set of genes we have previously reported to be suppressed by COI1 in roots (Ulrich et al, 2021). This interesting group of 149 genes identified here raises the question whether activation of gene expression after infection with V. longisporum is achieved via the inactivation of the COI1mediated repression.…”

“…This difference is mainly due to the constitutive up-regulation of 316 genes in coi1 roots. This repressive effect of COI1, which is only observed in roots and not in shoots, has been detected before under axenic growth conditions (Ulrich et al, 2021).…”

“…Transcriptome analysis of Verticillium longisporum-infected Arabidopsis roots has been performed before with axenically grown seedlings Ulrich et al, 2021). In our hands, V. longisporum only entered the xylem when seedlings were cultured for one day without any nutrients.…”

“…Prompted by these findings, we have recently shown that in Arabidopsis roots, COI1 acts as repressor of defence gene expression (Ulrich et al, 2021). RNA-seq analysis revealed that in coi1 roots a number of SA defence-related genes are basally de-repressed.…”

“…Again, aos mutant roots behave like WT roots and show no such de-repression. This repressor function of COI1 is uncoupled from its role in the JA pathway as it does not require JA-Ile and most likely no interaction with JAZ proteins (Ulrich et al, 2021). It remains to be elucidated how this COI1mediated repression is mechanistically achieved.…”