Phytochelatin and coumarin enrichment in root exudates of arsenic‐treated white lupin

Abstract

Soil contamination with toxic metalloids, such as arsenic, can represent a substantial human health and environmental risk. Some plants are thought to tolerate soil toxicity using root exudation, however, the nature of this response to arsenic remains largely unknown. Here, white lupin plants were exposed to arsenic in a semihydroponic system and their exudates were profiled using untargeted liquid chromatography-tandem mass spectrometry. Arsenic concentrations up to 1 ppm were tolerated and led to the accumulation of 12.9 μg As g À1 dry weight (DW) and 411 μg As g À1 DW in above-ground and belowground tissues, respectively. From 193 exuded metabolites, 34 were significantly differentially abundant due to 1 ppm arsenic, including depletion of glutathione disulphide and enrichment of phytochelatins and coumarins. Significant enrichment of phytochelatins in exudates of arsenic-treated plants was further confirmed using exudate sampling with strict root exclusion. The chemical tolerance toolkit in white lupin included nutrient acquisition metabolites as well as phytochelatins, the major intracellular metal-binding detoxification oligopeptides which have not been previously reported as having an extracellular role. These findings highlight the value of untargeted metabolite profiling approaches to reveal the unexpected and inform strategies to mitigate anthropogenic pollution in soils around the world.

Root phenotypes for the future

“…Arsenic is another toxic metalloid that represents a substantial threat to human health and environmental risk. In this issue, Frémont et al (2022) report that white lupin is able to tolerate high levels of As by secreting in root exudates phytochelatins, major intracellular metal‐binding detoxification oligopeptides, not previously reported to have an extracellular role. Metal‐polluted soils often contain more than one metal, yet few studies have investigated the impact mixtures of toxic metals have on plants.…”

Harnessing belowground processes for sustainable intensification of agricultural systems

“…Thanks to recent developments not only in analytical instrumentation, but also in computing power, available data processing software as well as metabolite databases, the number of non-targeted metabolomic exudation studies aiming to reveal the entire metabolite composition released by roots has significantly increased in the past five years. These analytical advances allowed for better insights into how root exudates change with plant development (Zhalnina et al 2018 ) as well as upon altered environmental conditions including nutrient availability (Smercina et al 2021 ; Tantriani et al 2020 ; Wang et al 2022 ; Ziegler et al 2016 ), soil pollution (Frémont et al 2022 ; Wang et al 2021a ), drought (Gargallo-Garriga et al 2018 ; Ghatak et al 2022 ), pathogen infection (Balendres et al 2016 ; Zhang et al 2020 ), inoculation with symbionts and beneficial rhizobacteria (Riviezzi et al 2021 ) and intercropping (Vora et al 2021 ), as well as on how exudation differs between different genotypes (Lopez-Guerrero et al 2022 ; Mönchgesang et al 2016 ). Furthermore, combining in-depth exudate analysis with improved microbiome profiling techniques also led to significant progress regarding our knowledge of effects of specific exudate compounds or compound classes on the soil microbiome and/or other rhizosphere processes in the past decade.…”

“…Furthermore, available data bases used for compound identification to date only allow to identify about 10–30% of analyzed features (e.g. Frémont et al 2022 ; Herz et al 2018 ; van Dam and Bouwmeester 2016 ). While it is admittedly difficult to discuss unidentified metabolites, our interpretations and conclusions particularly in the context of plant–microbe interactions might still be prone to biases if we keep our sole focus on exudate metabolites that we can identify.…”

Convergent and divergent responses of the rhizosphere chemistry and bacterial communities to a stress gradient in the Atacama Desert

“…Analysing rhizosphere chemistry is complex since it includes plant exudates, their breakdown products as well as microbial compounds (18). For instance, plants release organic acids to improve resource uptake or tolerance to soil toxicity (19,20). Plants exudate flavonoids, coumarins and lipids to condition rhizosphere microbiota and benzoxazinoids can be metabolised by microorganisms into antimicrobial compounds (7,8,14,(21)(22)(23).…”