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.

Highlights

  • Plants are capable of building up beneficial rhizosphere communities as is evidenced by diseasesuppressive soils

  • When a sixth generation of plants was planted on these conditioned soils and confronted with Pst, plants grown in pathogen-conditioned soils developed significantly (p < 0.05) reduced disease symptoms as compared to plants grown in control-conditioned soil (Fig. 1a)

  • In this study, we found that infections by the foliar pathogen Pst triggered a soil-borne legacy that induced resistance in a following generation of plants

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Summary

Introduction

Plants are capable of building up beneficial rhizosphere communities as is evidenced by diseasesuppressive soils. Downy mildew infection in a first population of plants increased the resistance of a second population of plants growing in the same soil Together, these results indicate that plants can recruit beneficial microbes upon attack to generate a soil memory or “soil-borne legacy” that better prepares the generation of plants to avoid harmful effects of the pathogen [12,13,14,15]. These results indicate that plants can recruit beneficial microbes upon attack to generate a soil memory or “soil-borne legacy” that better prepares the generation of plants to avoid harmful effects of the pathogen [12,13,14,15] In this process, root exudates and other root-derived molecules are believed to play a role [12, 13, 16,17,18], direct evidence supporting this hypothesis is generally lacking. By combining these complementary lines of investigation (Additional file 1: Figure S1), we were able to examine how changing exudation patterns can act as a mechanism by which plants can build their soil-borne legacy to the benefit of future plant generations

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