Exogenous glucosinolate produced by Arabidopsis thaliana has an impact on microbes in the rhizosphere and plant roots

Abstract

A specificity of Brassicaceous plants is the production of sulphur secondary metabolites called glucosinolates that can be hydrolysed into glucose and biocidal products. Among them, isothiocyanates are toxic to a wide range of microorganisms and particularly soil-borne pathogens. The aim of this study was to investigate the role of glucosinolates and their breakdown products as a factor of selection on rhizosphere microbial community associated with living Brassicaceae. We used a DNA-stable isotope probing approach to focus on the active microbial populations involved in root exudates degradation in rhizosphere. A transgenic Arabidopsis thaliana line producing an exogenous glucosinolate and the associated wild-type plant associated were grown under an enriched 13 CO 2 atmosphere in natural soil. DNA from the rhizospheric soil was separated by density gradient centrifugation. Bacterial (Alphaproteobacteria, Betaproteobacteria, Gammaproteobacteria and Acidobacteria), Archaea and fungal community structures were analysed by DGGE fingerprints of amplified 16S and 18S rRNA gene sequences. Specific populations were characterized by sequencing DGGE fragments. Roots of the transgenic plant line presented an altered profile of glucosinolates and other minor additional modifications. These modifications significantly influenced microbial community on roots and active populations in the rhizosphere. Alphaproteobacteria, particularly Rhizobiaceae, and fungal communities were mainly impacted by these Brassicaceous metabolites, in both structure and composition. Our results showed that even a minor modification in plant root could have important repercussions for soil microbial communities.

Effects of intraspecific variation in white cabbage (Brassica oleracea var. capitata) on soil organisms

“…living and dead plant material and root exudates) we still found no differences in the microorganism community between the cultivars or a response of the microorganisms to the glucosinolate profiles. This contrasts with previous studies recording that B. napus and A. thaliana chemotypes with different glucosinolate profiles influenced the microorganism community (Bressan et al 2009;Rumberger and Marschner 2003). Using identical bacterial primers as used in our study, Rumberger and Marschner (2003) found that 2-phenylethyl-isothiocyanate, the breakdown product of gluconasturtiin, influenced the bacterial community in roots and rhizosphere of B. napus.…”

“…Upon tissue damage, glucosinolates are degraded by the enzyme myrosinase, thereby forming toxic breakdown products such as (iso)thiocyanates (Wang et al 2009). Belowground, glucosinolates and their breakdown products are known to reduce the abundance of phytophagous organisms such as rootfeeding nematodes (Lazzeri et al 2004;Potter et al 1998;Potter et al 2000), fungi (Bressan et al 2009;Rumberger and Marschner 2003;Snapp et al 2007), and bacteria (Aires et al 2009;Bressan et al 2009;Rumberger and Marschner 2003). Aromatic glucosinolates, particularly gluconasturtiin and its breakdown product 2-phenylethyl isothiocyanate, are generally considered as the most toxic glucosinolates in plant roots (Potter et al 1998;Potter et al 2000;Rumberger and Marschner 2003;van Dam et al 2009;Vierheilig et al 2000).…”

Stability and succession of the rhizosphere microbiota depends upon plant type and soil composition

“…Some microbial root colonists are saprophytes, which also colonise splinters of wood inserted into soil (Bulgarelli et al, 2012), but others are selected by exudation of nutrient sources and phytoalexins, such as glucosinolates and avenacins (Sonderby et al, 2007;Bressan et al, 2009;Turner et al, 2013b). Furthermore, by altering the rhizosphere microbiota, plants induce formation of suppressive soil where growth of plant pathogens is inhibited (Lebreton et al, 2007;Kinkel et al, 2011;Mendes et al, 2011).…”

The evolution of quantitative traits in complex environments

“…In the absence of herbivory, do the selective advantages of various plant defenses persist or disappear? How do antiherbivore defenses such as glucosinolates respond to selective pressures imposed by other agents, such as pathogens (Sanchez-Vallet et al, 2010) and microbial mutualists (Bressan et al, 2009)? More generally, what role do different abiotic and biotic agents of selection play in the evolution of complex traits?…”