Experimental evidence pointing to rain as a reservoir of tomato phyllosphere microbiota

Authors: MECHAN-LLONTOP, MARCO - Virginia Tech; TIAN, LONG - Virginia Tech; SHARMA, PARUL - Virginia Tech; HEFLIN, LOGAN - Virginia Tech; BERNAL-GALEANO, VIVIAN - Virginia Tech; HAAK, DAVID - Virginia Tech; Clarke, Christopher; VINATZER, BORIS - Virginia Tech

Submitted to: Phytobiomes Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/28/2021
Publication Date: 6/1/2021
Citation: Mechan-Llontop, M.E., Tian, L., Sharma, P., Heflin, L., Bernal-Galeano, V., Haak, D.C., Clarke, C.R., Vinatzer, B.A. 2021. Experimental evidence pointing to rain as a reservoir of tomato phyllosphere microbiota. Phytobiomes Journal. e-ISSN:2471-2906. https://doi.org/10.1094/PBIOMES-04-21-0025-R.
DOI: https://doi.org/10.1094/PBIOMES-04-21-0025-R

Interpretive Summary: Plant-associated microbial populations affect plant health and crop productivity. Controlling the community of plant-associated microbes for optimal crop performance is challenging due to the myriad potential reservoirs of microbial diversity that can be exposed to plants. The primary known reservoirs of microbial diversity that can alter plant-associated microbial populations are the atmosphere, the soil, and the plant seeds. We tested whether rain is also an important reservoir for microbial diversity that can alter the community of plant-associated microbes. Following both controlled laboratory sprays with collected rainwater and exposure to natural rain events, plants exposed to rain were significantly altered in the abundance and composition of microbial communities on plant leaves compared to control plants. This finding suggests that rain events can significantly impact plant-associated microbial communities and that rainwater is another impactful reservoir of plant-associated microbes. Our research contributes to a more complete understanding of environmental events and conditions that can affect plant-associated microbial populations and is critical for developing tools to maintain microbial communities that are optimal for crop productivity.

Technical Abstract: Plant microbiota play essential roles in plant health and crop productivity. Comparisons of community composition have suggested seeds, soil, and the atmosphere as reservoirs of phyllosphere microbiota. After finding that leaves of tomato (Solanum lycopersicum) plants exposed to rain carried a higher microbial population size than leaves of tomato plants not exposed to rain, here we experimentally tested the hypothesis that rain is a so far neglected reservoir of phyllosphere microbiota. Rain microbiota were thus compared with phyllosphere microbiota of tomato plants either treated with concentrated rain microbiota, filter-sterilized rain, or sterile water. Based on 16S rRNA amplicon sequencing, one-hundred four operational taxonomic units (OTUs) significantly increased in relative abundance after inoculation with concentrated rain microbiota but no OTU significantly increased after treatment with either sterile water or filter-sterilized rain. Some of the genera to which these 104 OTUs belonged were also found at higher relative abundance on tomatoes exposed to rain outdoors than on tomatoes grown protected from rain in a commercial greenhouse. Taken together, these results point to precipitation as a reservoir of phyllosphere microbiota and show the potential of controlled experiments to investigate the role of different reservoirs in the assembly of phyllosphere microbiota.