Deep-sequencing transcriptome of Tomato growing in two soils containing their natural microbiota

Root-associated microbiota play a major role in shaping plant physiology under diverse environmental conditions. Such an impact may have systemic outcomes, also influencing traits of agronomic relevance. In particular, arbuscular mycorrhizae (AM) improve mineral nutrition and fortify plants against biotic and abiotic stresses. We took advantage of next-generation sequencing to study interactions between Solanum lycopersicum (tomato) and its root-associated microbiota. Two agricultural soils (RO and AL) containing diverse microbiota and with different biotic and abiotic features were considered. The RO and AL soils were conducive and suppressive, respectively, to the pathogen Fusarium oxysporum f. sp. lycopersici (FOL). A steamed, peat-moss soil was used as a control. Two tomato genotypes (FOL-resistant and susceptible) were grown in microcosms containing the three soils without pathogen inoculation. After three months, roots were sampled, AM colonization was assessed, and the transcriptome was analyzed by RNAseq. Morphological observations indicated that AM structures were present in the roots from RO soil, while their presence was severely reduced in AL soil. RNAseq analysis indicates that the two soils, with their microbiota, shape the root transcriptome differently than the steamed soil. Moreover, the soil type was shown to cause a more relevant impact on gene expression than plant genotype, that is, AL soil activated metabolic pathways dealing with plant-defense irrespective of genetic background. However, comparing the profiles of the two genotypes, distinct sets of transcripts involved in plant-pathogen signaling emerged among the differentially expressed genes, suggesting that genotype is the second parameter that impacts the transcript profile interacting with the soil. Finally, a meta-transcriptome reconstruction confirmed the presence and activity of fungal communities strictly associated with the roots in both soils. Overall, our data sheds light on tomato responses to complex natural microbiota and suggest a strong interplay occurring between soil biotic and abiotic features, microbiota diversity, and genotype in tuning plant gene expression.