Rhizosphere Microbiome Co-Occurrence Network Analysis across a Tomato Domestication Gradient.

When plant-available phosphorus (P) is lost from a soil solution, it often accumulates in the soil as a pool of unavailable legacy P. To acquire legacy P, plants employ recovery strategies, such as forming associations with soil microbes. However, the degree to which plants rely on microbial associations for this purpose varies with crop domestication and subsequent breeding. Here, by generating microbial co-occurrence networks, we sought to explore rhizosphere bacterial interactions in low-P conditions and how they change with tomato domestication and breeding. We grew wild tomato, traditional tomato (developed circa 1900), and modern tomato (developed circa 2020) in high-P and low-P soil throughout their vegetative developmental stage. Co-occurrence network analysis revealed that as the tomatoes progressed along the stages of domestication, the rhizosphere microbiome increased in complexity in a P deficit. However, with the addition of P fertilizer, the wild tomato group became more complex, surpassing the complexity of traditional and modern tomato, suggesting a high degree of responsiveness in the rhizosphere microbiome to P fertilizer by wild tomato relatives. By illustrating these changing patterns of network complexity in the tomato rhizosphere microbiome, we can further understand how plant domestication and breeding have shaped plant-microbe interactions.

Tomato domestication rather than subsequent breeding events reduces microbial associations related to phosphorus recovery.

Legacy phosphorus (P) is a reservoir of sparingly available P, and its recovery could enhance sustainable use of nonrenewable mineral fertilizers. Domestication has affected P acquisition, but it is unknown if subsequent breeding efforts, like the Green Revolution (GR), had a similar effect. We examined how domestication and breeding events altered P acquisition by growing wild, traditional (pre-GR), and modern (post-GR) tomato in soil with legacy P but low bioavailable P. Wild tomatoes, particularly accession LA0716 (Solanum pennellii), heavily cultured rhizosphere P solubilizers, suggesting reliance on microbial associations to acquire P. Wild tomato also had a greater abundance of other putatively beneficial bacteria, including those that produce chelating agents and antibiotic compounds. Although wild tomatoes had a high abundance of these P solubilizers, they had lower relative biomass and greater P stress factor than traditional or modern tomato. Compared to wild tomato, domesticated tomato was more tolerant to P deficiency, and both cultivated groups had a similar rhizosphere bacterial community composition. Ultimately, this study suggests that while domestication changed tomato P recovery by reducing microbial associations, subsequent breeding processes have not further impacted microbial P acquisition mechanisms. Selecting microbial P-related traits that diminished with domestication may therefore increase legacy P solubilization.

Harnessing Phosphorous (P) Fertilizer-Insensitive Bacteria to Enhance Rhizosphere P Bioavailability in Legumes.

Phosphorous (P) is widely used in agriculture; yet, P fertilizers are a nonrenewable resource. Thus, mechanisms to improve soil P bioavailability need to be found. Legumes are efficient in P acquisition and, therefore, could be used to develop new technologies to improve soil P bioavailability. Here, we studied different species and varieties of legumes and their rhizosphere microbiome responses to low-P stress. Some varieties of common beans, cowpeas, and peas displayed a similar biomass with and without P fertilization. The rhizosphere microbiome of those varieties grown without P was composed of unique microbes displaying different levels of P solubilization and mineralization. When those varieties were amended with P, some of the microbes involved in P solubilization and mineralization decreased in abundance, but other microbes were insensitive to P fertilization. The microbes that decreased in abundance upon P fertilization belonged to groups that are commonly used as biofertilizers such as Pseudomonas and Azospirillum. The microbes that were not affected by P fertilization constitute unique species involved in P mineralization such as Arenimonas daejeonensis, Hyphomicrobium hollandicum, Paenibacillus oenotherae, and Microlunatus speluncae. These P-insensitive microbes could be used to optimize P utilization and drive future sustainable agricultural practices to reduce human dependency on a nonrenewable resource.