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Reprogramming plant development with microbial organic volatile compounds for sustainable food production

Periodic Reporting for period 1 - ReproDev (Reprogramming plant development with microbial organic volatile compounds for sustainable food production)

Reporting period: 2020-01-01 to 2021-12-31

Plant roots are associated with numerous beneficial microbes that can be used to improve plant growth and protect against diseases. One important, but understudied, aspect of plant-microbe and microbe-microbe interactions that affects these processes is communication via volatile organic compounds (VOCs). VOCs are low-molecular-weight lipophilic compounds that affect several aspects of plant growth and health, as well as microbial communication.
This project sought to advance research exploring VOCs mediated microbe-microbe and microbe-plant interactions via a range of novel approaches and ecological experiments.
Below, the four main experiments conducted within the research project are described:

Experiment 1: Microbial volatile organic compounds with dual-function play more important roles in plant-microbe interactions than single-function compounds
Using a collection of 200 bacterial strains we constructed 4 different bacterial communities each expected to have a different impact on plant growth promotion and pathogen inhibition. We found that that plant growth promotion was reduced in when plants were exposed to a 5-strain community of bacterial strains as compared to single-strain exposure, and that mixing the strains together provided a larger affected than when they were spotted out separately. On the other hand, pathogen suppression was found to be higher when bacteria were presented as homogenized communities as opposed to separately inoculated strains, and the effects communities of the same composition were correlated across these two forms of inoculation. These results suggest that antimicrobial activities are upon an increase in interspecies interactions, especially when different strains are mixed together.

Experiment 2: Spatially structured microorganisms cause transgressive overyielding in clonal plant populations
Plant biodiversity both within species and across species has consistently been found to be correlated to higher productivity. However, the diversity of plant phenotypes is also determined to a large degree by interactions with the associated microbiome. This plant holobiont perspective suggests that relationships between plant biodiversity and function need to include interactions with multiple players within the plant microbiome. We created plant phenotypic diversity by exposure to different VOC-producing microbes. We found that increasing this level of diversity, resulting in increased community yield. Most interestingly, we found that competition was reduced when plant communities consisted of plants that had been exposed to VOC-producing bacteria and the level of competition suppression was correlated with the diversity of different plant-microbe interactions previously experienced by the plants. We conclude that heterogenous association of plants with different soil microorganisms can generate overyielding effects similar to those observed in multispecies communities, calling for a reassessment of the biodiversity-ecosystem functioning relationship through a holobiont lens.

Experiment 3: Microbe-associated plants complement neighboring plants with no association with microbes
In this experiment, we sought to examine if the beneficial effects of plant-microbe interactions might be extended to neighboring plants that had not been exposed to bacterial VOCs. To this end, we extended Experiment 2 to include naïve target plants that had never been exposed to bacterial VOCs. We found that while the overall effect of plant density was negative on individual plant productivity, the presence of neighboring plants that had experienced bacterial VOCs significantly reduced the competitive effects on naïve target plants compared to only naïve plants grown together. The facilitative effects of neighboring VOC-exposed plants on naïve target plants also increased as a function of neighboring holobiont diversity. We conclude that plants associated with different soil microorganisms can not only alleviate competition amongst each other and improve plant productivity, but they can also facilitate neighboring plants that have not experienced such interactions.

Experiment 4: Underground globalization: volatile organic compounds can connect bulk and rhizosphere soils enabling an extended plant metamicrobiome
We sought to examine how long-distance interactions could potentially link bulk and rhizosphere soil microbiomes, allowing the exchange of information between topologically disconnected microbial metapopulations and the host plant. Bacterial strains known to produce plant growth-promoting VOCs were then inoculated one or two microcosms away from a target microcosm containing a lettuce plant. Interestingly, plant growth was increased by the presence of connected soil microcosms, even in the absence of strain inoculations. Plant growth was further stimulated by strain inoculations one or two microcosms removed from the center, indicating the effects of bacterial inoculation on plant growth were transferred across a considerable distance.

Together these, experiments have yielded a rich data that provide novel insights into how plant-microbe interactions can influence plant growth at the community level. The main dissemination pathways for this project are through oral and poster sessions at important international conferences such as that of the International Society of Microbial Ecology (ISME) and though publication in high quality international scientific journals (1 published, 3 in preparation). The results also offer new perspectives within the plant and agricultural sciences, thus increasing the likelihood of broad scientific and practical impacts. All presentations and manuscripts stemming from this work cite the valued support and funding of EU MC program.
This project has provided novel data and perspectives on issues related to plant growth promotion and the informed use of plant -microbe interactions in boosting plant performance. Given the need for more stainable agricultural practices, the work presented in not only of scientific interest, but also has broader societal relevance. Plant competition is a major limitation of crop yield, and the prospect of reducing plant competition through microbial VOC treatments opens up a whole new avenue for innovative cropping strategies that maximizes yield without requiring further intensification of farming systems. We propose that management strategies promoting the beta diversity in plant-associated microbes may generate different, complementary plant phenotypes out of clonal plant populations. Furthermore, the discoveries stemming from this project also opens up new perspectives with respect to ecosystem restoration, where plant-microbe interactions may help to increase phenotypic diversity and thereby improve resistance and resilience to environmental perturbations. Thus, the results of this project should prove to be important for both farmers and restoration managers raising the importance of heterogeneity at the microscale level. Sampling local microbiomes together with aboveground plants may also help predict and manage better (agro-)ecosystem responses to global change effects.