Phyllosphere microbial associations improve plant reproductive success

Authors: MEHLFERBER, ELIJAH - University Of California; DEBRAY, REENA - University Of California Berkeley; CONOVER, ASA - University Of California Berkeley; SHERMAN, JULIA - University Of California Berkeley; KAULBACH, GRIFFIN - Haverford College; REED, ROBERT - I-Cultiver; McCue, Kent; FERREL, JON - Azomite Mineral Products, Inc; KHANNA, RAJNISH - I-Cultiver; KOSKELLA, BRITT - University Of California

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/9/2023
Publication Date: 12/8/2023
Citation: Mehlferber, E., Debray, R., Conover, A., Sherman, J., Kaulbach, G., Reed, R., Mc Cue, K.F., Ferrel, J., Khanna, R., Koskella, B. 2023. Phyllosphere microbial associations improve plant reproductive success. Frontiers in Plant Science. 14,2023. https://doi.org/10.3389/fpls.2023.1273330.
DOI: https://doi.org/10.3389/fpls.2023.1273330

Interpretive Summary: Microbes are present on and in almost all living organisms. The importance of a healthy and diverse community of microbes (the microbiome) affects the health, wellbeing and productivity of the organism. In plants the microbiome of the soil has been the most studied, in and around the roots. We are now beginning to understand the importance of the microbiome above ground on the leaves and stems of plants. In the greenhouse there is limited natural mixing of microbes normally present in the natural agricultural setting. We expected that the presence of limited microbes to colonize the leaves in the greenhouse might affect plant productivity and health. To examine this we introduced an artificial community of microbes onto the surface of the plants. Greenhouse grown tomatoes were supplied microbes onto the surface of their leaves. We found that the addition of microbes to the leaves had an effect of the number and diversity of microbes on the plant that was associated with an increase in fruit production when the artificial community was added to the leaves. This suggested the greenhouse environment was lacking in the diversity of microbes that could have a beneficial effect on the plant growth and that the addition of an initial microbial community can benefit the plant productivity and health.

Technical Abstract: The above-ground plant microbiome (the phyllosphere) is increasingly recognized as an important component of plant health. We hypothesized that phyllosphere interactions may be disrupted in a greenhouse setting, where microbial dispersal is limited, and that the addition of a microbial amendment might yield important benefits to the host plant. Using a newly developed synthetic phyllosphere microbiome for Tomato, we tested this hypothesis across multiple trials by manipulating microbial colonization of leaves and measuring subsequent plant growth and reproductive success, comparing results from plants grown in both greenhouse and field settings. We confirmed that greenhouse grown plants have a depauperate phyllosphere microbiome, and that the addition of the synthetic microbial community was responsible for a clear and repeatable increase in fruit production in this setting. We further show that this effect is synergistic with the addition of micronutrient based soil amendments, with important implications for agriculture. These results suggest that greenhouse environments have poor phyllosphere microbiome establishment, with negative impacts on the plant. The results also implicate the phyllosphere microbiome as a key component of plant fitness, emphasizing that these communities have a clear role to play in the ecology and evolution of plant communities.