Root exudates drive the soil-borne legacy of aboveground pathogen infection

Abstract

BackgroundPlants are capable of building up beneficial rhizosphere communities as is evidenced by disease-suppressive soils. However, it is not known how and why soil bacterial communities are impacted by plant exposure to foliar pathogens and if such responses might improve plant performance in the presence of the pathogen. Here, we conditioned soil by growing multiple generations (five) of Arabidopsis thaliana inoculated aboveground with Pseudomonas syringae pv tomato (Pst) in the same soil. We then examined rhizosphere communities and plant performance in a subsequent generation (sixth) grown in pathogen-conditioned versus control-conditioned soil. Moreover, we assessed the role of altered root exudation profiles in shaping the root microbiome of infected plants.ResultsPlants grown in conditioned soil showed increased levels of jasmonic acid and improved disease resistance. Illumina Miseq 16S rRNA gene tag sequencing revealed that both rhizosphere and bulk soil bacterial communities were altered by Pst infection. Infected plants exhibited significantly higher exudation of amino acids, nucleotides, and long-chain organic acids (LCOAs) (C > 6) and lower exudation levels for sugars, alcohols, and short-chain organic acids (SCOAs) (C ≤ 6). Interestingly, addition of exogenous amino acids and LCOA also elicited a disease-suppressive response.ConclusionCollectively, our data suggest that plants can recruit beneficial rhizosphere communities via modification of plant exudation patterns in response to exposure to aboveground pathogens to the benefit of subsequent plant generations.Electronic supplementary materialThe online version of this article (10.1186/s40168-018-0537-x) contains supplementary material, which is available to authorized users.

High abundance of Ralstonia solanacearum changed tomato rhizosphere microbiome and metabolome

“…The rhizosphere microbiome which showed a direct effect on plant health and resistance to pathogens [27,33] was mastered by rhizosphere soil metabolites [26,47]. Root exudates depend on many abiotic and biotic factors, with the former including pathogen invasion, especially colonization.…”

“…For example, Fusarium oxysporum colonization could stimulate the secretion of phenolic acids [46]. Foliar pathogen infection increased the concentration of some amino acids and fatty acids in root exudates [47]. While a little knowledge of rhizosphere soil metabolites impacted by pathogen especially RS was revealed till now.…”

Conditioning the soil microbiome through plant–soil feedbacks suppresses an aboveground insect pest

“…One approach to steer soil microbiomes is to apply the ecological concept of plant-soil feedbacks (van der Putten et al, 2013;Bennett & Klironomos, 2018). Plants release primary and secondary metabolites through their roots that shape the soil and rhizosphere microbiome in a species-specific way (Hu et al, 2018;Yuan et al, 2018). Thus, when a new plant grows in soil in which another plant had previously grown, its performance can be enhanced or reduced, depending on changes in the soil triggered by the first plant.…”

The peanut pods-associated microbiota and their effects on aflatoxin contamination

“…These symbionts together with the microenvironment around form a unique micro-ecological flora, constituting a comprehensive ecological unit for plants [3] The effects of these symbiotic microbiota interactions on plants' adapting to environments have been widely noted for more than a century [6]. Many researchers have studied the possibility and molecular mechanisms of utilizing the symbiotic relationships between plants and microbiota for disease control [7][8][9][10]. However, technical limitations and insufficient depth of sequencing constrained the analysis of microbiota related to plant growth, disease resistance, and environmental adaptability [8,9].…”

“…Many researchers have studied the possibility and molecular mechanisms of utilizing the symbiotic relationships between plants and microbiota for disease control [7][8][9][10]. However, technical limitations and insufficient depth of sequencing constrained the analysis of microbiota related to plant growth, disease resistance, and environmental adaptability [8,9]. Nowadays, the novel high-throughput sequencing technology has facilitated the investigation of plant-associated microbiome and provided a glimpse of microbial diversity [9].…”