Microbiome-mediated phosphorus acquisition in wild and domesticated tomatoes

Abstract

Phosphorus (P) is a plant-essential mineral, and because of soil retention reactions, is often sparingly available. To address this limited availability, P fertilizers that are derived from finite phosphate rock are necessarily applied. As a result, modern cultivars are adapted to grow with high fertility. Conversely, wild crops grow in terrestrial soils with poor nutrition. However, it remains unclear how domestication altered the soil microbiome related to P recovery in certain crops and how soil microbiomes of wild crops respond to exogenous P. Here, we use tomato as a model crop because of its global importance, rapid growth, and morphological variation. To begin to address these unknowns, we investigated how P deficiency affected microbial associations at different stages of domestication and breeding: wild, traditional (developed circa 1900), and modern (developed circa 2020). We determined that although modern and traditional tomato were minimally affected by the P deficit, as showcased through their higher shoot P concentrations and relative biomass, wild tomatoes promoted associations with P solubilizing bacteria. There was variation within wild tomatoes, with Solanum pennellii associating with P solubilizing bacteria greater than other accessions. Conversely, traditional and modern tomatoes responded similarly to P deficiency in their growth and microbial associations. We subsequently investigated the responsiveness to P by these bacteriomes. Using the data culled from the first experiment, we explored the degree to which the microbiome of wild, traditional, and modern tomato responded to exogenous P application. By examining the microbial co-occurrence networks of P depleted soils, we determined that rhizosphere microbiome complexity increased progressively along a domestication gradient. However, upon P resupply, these differences diminished, and the wild tomato rhizosphere was as complex as the domesticated tomatoes. These results suggest that microbiome of wild tomato is highly responsive to fertilization. Finally, we explored how a wild and modern tomato representative responded to applied P. Because all tested modern and traditional tomatoes showed similar responses in the prior experiments, a single modern representative (S. lycopersicum 'Quali T 27') was selected for this investigation. Solanum pennellii was selected as the wild representative because of its strong ability to associate with its soil microbial community. We determined that wild tomato maintained higher soil P values compared to modern while also promoting microbial fluctuations, microbial biomass, and P solubilizer relative abundance. This microbially-informed strategy by wild tomato is likely a result of its root exudate profile. Wild tomato exuded trehalose and glycerol compounds, which were shown to promote bacterial P solubilizing activity. In a separate trial, we grew modern tomato in soils conditioned with a modern tomato or a wild tomato. Biomass was greater for those tomatoes planted in soils with an initial wild plant. However, this difference may be a result of residual P by wild tomato because the modern tomato was unable to maintain the microbiome cultivated by the wild tomato. Taken together, these findings underscore how domestication has attenuated root-microbe interactions and responsiveness related to P. By elucidating this divergence in wild and modern tomatoes, we can begin to design methods to reincorporate traits lost to domestication, thereby promoting soil P cycling while reducing exogenous inputs of nonrenewable P fertilizers.