Volatile-mediated interspecific plant interaction promotes root colonization by beneficial bacteria via induced shifts in root exudation.

Volatile organic compounds (VOCs) released by plants can act as signaling molecules mediating ecological interactions. Therefore, the study of VOCs mediated intra- and interspecific interactions with downstream plant physiological responses is critical to advance our understanding of mechanisms underlying information exchange in plants. Here, we investigated how plant-emitted VOCs affect the performance of an interspecific neighboring plant via induced shifts in root exudate chemistry with implications for root-associated microbiota recruitment. First, we showed that VOCs emitted by potato-onion plants stimulate the growth of adjacent tomato plants. Then, we demonstrated that this positive effect on tomato biomass was attributed to shifts in the tomato rhizosphere microbiota. Specifically, we found potato-onion VOCs to indirectly affect the recruitment of specific bacteria (e.g., Pseudomonas and Bacillus spp.) in the tomato rhizosphere. Second, we identified and validated the compound dipropyl disulfide as the active molecule within the blend of potato-onion VOCs mediating this interspecific plant communication. Third, we showed that the effect on the tomato rhizosphere microbiota occurs via induced changes in root exudates of tomato plants caused by exposure to dipropyl disulfide. Last, Pseudomonas and Bacillus spp. bacteria enriched in the tomato rhizosphere were shown to have plant growth-promoting activities. Potato-onion VOCs-specifically dipropyl disulfide-can induce shifts in the root exudate of adjacent tomato plants, which results in the recruitment of plant-beneficial bacteria in the rhizosphere. Taken together, this study elucidated a new mechanism of interspecific plant interaction mediated by VOCs resulting in alterations in the rhizosphere microbiota with beneficial outcomes for plant performance. Video Abstract.

Zhou X ，Zhang J ，Shi J ，Khashi U Rahman M ，Liu H ，Wei Z ，Wu F ，Dini-Andreote F ... -  《Microbiome》

Interspecific plant interaction via root exudates structures the disease suppressiveness of rhizosphere microbiomes.

Terrestrial plants can affect the growth and health of adjacent plants via interspecific interaction. Here, we studied the mechanism by which plant root exudates affect the recruitment of the rhizosphere microbiome in adjacent plants-with implications for plant protection-using a tomato (Solanum lycopersicum)-potatoonion (Allium cepa var. agrogatum) intercropping system. First, we showed that the intercropping system results in a disease-suppressive rhizosphere microbiome that protects tomato plants against Verticillium wilt disease caused by the soilborne pathogen Verticillium dahliae. Second, 16S rRNA gene sequencing revealed that intercropping with potatoonion altered the composition of the tomato rhizosphere microbiome by promoting the colonization of specific Bacillus sp. This taxon was isolated and shown to inhibit V. dahliae growth and induce systemic resistance in tomato plants. Third, a belowground segregation experiment found that root exudates mediated the interspecific interaction between potatoonion and tomato. Moreover, experiments using split-root tomato plants found that root exudates from potatoonion, especially taxifolin-a flavonoid compound-stimulate tomato plants to recruit plant-beneficial bacteria, such as Bacillus sp. Lastly, ultra-high-pressure liquid chromatography-mass spectrometry analysis found that taxifolin alters tomato root exudate chemistry; thus, this compound acts indirectly in modulating root colonization by Bacillus sp. Our results revealed that this intercropping system can improve tomato plant fitness by changing rhizosphere microbiome recruitment via the use of signaling chemicals released by root exudates of potatoonion. This study revealed a novel mechanism by which interspecific plant interaction modulates the establishment of a disease-suppressive microbiome, thus opening up new avenues of research for precision plant microbiome manipulations.

Zhou X ，Zhang J ，Khashi U Rahman M ，Gao D ，Wei Z ，Wu F ，Dini-Andreote F ... -  《-》

Fusaric acid mediates the assembly of disease-suppressive rhizosphere microbiota via induced shifts in plant root exudates.

The plant health status is determined by the interplay of plant-pathogen-microbiota in the rhizosphere. Here, we investigate this tripartite system focusing on the pathogen Fusarium oxysporum f. sp. lycopersici (FOL) and tomato plants as a model system. First, we explore differences in tomato genotype resistance to FOL potentially associated with the differential recruitment of plant-protective rhizosphere taxa. Second, we show the production of fusaric acid by FOL to trigger systemic changes in the rhizosphere microbiota. Specifically, we show this molecule to have opposite effects on the recruitment of rhizosphere disease-suppressive taxa in the resistant and susceptible genotypes. Last, we elucidate that FOL and fusaric acid induce changes in the tomato root exudation with direct effects on the recruitment of specific disease-suppressive taxa. Our study unravels a mechanism mediating plant rhizosphere assembly and disease suppression by integrating plant physiological responses to microbial-mediated mechanisms in the rhizosphere.

Jin X ，Jia H ，Ran L ，Wu F ，Liu J ，Schlaeppi K ，Dini-Andreote F ，Wei Z ，Zhou X ... -  《Nature Communications》

Rhizosphere microbiome mediates systemic root metabolite exudation by root-to-root signaling.

Korenblum E ，Dong Y ，Szymanski J ，Panda S ，Jozwiak A ，Massalha H ，Meir S ，Rogachev I ，Aharoni A ... -  《-》

A non-invasive soil-based setup to study tomato root volatiles released by healthy and infected roots.

Gulati S ，Ballhausen MB ，Kulkarni P ，Grosch R ，Garbeva P ... -  《Scientific Reports》