Shoot-root interaction in control of camalexin exudation in Arabidopsis

Abstract

Plants exude secondary metabolites from the roots to shape the composition and function of their microbiome. Many of these compounds are known for their anti-microbial activity and are part of the plant immunity, such as the indole-derived phytoalexin camalexin. Here we studied the dynamics of camalexin synthesis and exudation upon induction of Arabidopsis thaliana with a plant growth promotion bacteria Pseudomonas sp. CH267 or a bacterial pathogen Burkholderia glumae PG1. We show that while the camalexin accumulation and exudation is more rapidly but transiently induced upon interaction with the growth promoting strain, the pathogen induces a higher and more stable camalexin levels. By combination of experiments with cut shoots and roots and grafting of wild type plant with mutants in camalexin synthesis we showed that while camalexin can be produced and released by both organs, in intact plant the exuded camalexin originates in the shoots. We also reveal that the root specific CYP71A27 affects specifically the outcome of interaction with plant growth promoting bacteria and that its transcript levels are controlled by a shoot derived signal. In conclusion, camalexin synthesis seems to be controlled on a whole plant level and coordinated between shoots and roots.

ER body‐resident myrosinases and tryptophan specialized metabolism modulate root microbiota assembly

“…The role of root‐produced camalexin in regulating root‐commensal interaction has also been reported (Koprivova et al ., 2019, 2023), which is in line with the role of specialized metabolites in interaction with microbes in a wide range of plant species (Singh et al ., 2022). Interestingly, camalexin exudation appears to play a positive role in accommodating a plant growth‐promoting bacterial commensal CH267 (Koprivova et al ., 2019, 2023), illustrating its function not only as an antimicrobial but also for recruiting beneficial microbes. Therefore, it is possible that camalexin and I3CA produced from IAN via IG metabolism directly influence root microbiota assembly.…”

“…Camalexin operates as an antimicrobial compound and affects microbial behavior directly (Bednarek et al, 2005), while I3CA has been shown to mediate b-aminobutyric acid-triggered priming of immune responses and to covalently bind to cell wall oligosaccharides upon infection in A. thaliana (Hagemeier et al, 2001;Tan et al, 2004;Gamir et al, 2012Gamir et al, , 2018. The role of root-produced camalexin in regulating root-commensal interaction has also been reported (Koprivova et al, 2019(Koprivova et al, , 2023, which is in line with the role of specialized metabolites in interaction with microbes in a wide range of plant species (Singh et al, 2022). Interestingly, camalexin exudation appears to play a positive role in accommodating a plant growth-promoting bacterial commensal CH267 (Koprivova et al, 2019(Koprivova et al, , 2023, illustrating its function not only as an antimicrobial but also for recruiting beneficial microbes.…”

“…It is also important to consider the fact that the exudates used in our experiments were collected from axenic, na€ ıve plants, that is, in the absence of microbes or any immune elicitors. It has been well described that plant immune status has an impact on root metabolomic profiles (Millet et al, 2010;Koprivova et al, 2019) as well as on root exudation profiles (Bednarek et al, 2005;Badri & Vivanco, 2009;Koprivova et al, 2020Koprivova et al, , 2023. Therefore, it is likely that the metabolomic profile of root exudates may be substantially different between axenic and soil conditions.…”

The mysterious non‐arbuscular mycorrhizal status of Brassicaceae species

“…Camalexin and glucosinolates are two important classes of sulfur‐containing secondary metabolites that are specifically synthesized by the Brassicaceae plants. Using Arabidopsis mutants deficient in camalexin, Koprivova et al (2023) reported that this phytoalexin affects the activity of rhizospheric microbes and shields the plant from the benefits of plant growth‐promoting (PGP) bacteria (Koprivova et al, 2019, 2023). Noteworthy, plant secondary metabolite, coumarin scopoletin has been shown as an important signal for the initial steps of AMF‐plant symbiotic associations (Cosme et al, 2021).…”

Editorial: Specialized metabolites manipulating organismal behaviors and rhizospheric communications

“…However, they are not the only ones shaping underground communications; many other intriguing root-released metabolites, such as 6-methoxy-2-benzoxazolin, blumenols, and camalexin, are also involved in the rhizospheric interactions ( Hu et al., 2018 ; Fiorilli et al. ; Koprivova et al., 2023 ).…”