Interkingdom interactions: Transcriptional Reprogramming of Tomato by beneficial and harmful organisms

The impact of beneficial arbuscular mycorrhizal (AM) fungi on tomato growth has been extensively studied. As components of the plant microbiota, they significantly modulate genes not only in roots but also systemically. Some AM fungi host their own bacterial microbiota including bacteria living on the hyphal surface as well as obligate endobacteria residing inside the fungal cytoplasm. Two isogenic lines of Gigaspora margarita one hosting a Burkholderia-related endobacterium (Candidatus Glomeribacter gigasporarum, CaGg), and the other cured of its endobacterium (CaGg-) were used to investigate the role of CaGg in the response of tomato plants to Botrytis cinerea infection. Six treatment groups were established: control plants; plants mycorrhized by either G. margarita CaGg or G. margarita CaGg- and the same groups challenged with B. cinerea. At the phenotypic level, no significant differences were observed among the control and mycorrhized plants in the absence of the pathogen. In contrast, plants colonized by the AM fungus CaGg exhibited alleviated disease symptoms upon B. cinerea infection.Transcriptomic analyses were performed on leaves sampled from all the treatments. Ordination analysis confirmed that both the symbiotic fungi and the pathogen were the main modulators of the transcriptomic response. AM fungi primarily triggered pathways involved in plant-cell communication, transcription regulatory activity, hormone metabolism and photosynthesis, while the pathogen induced changes in genes related to plant-pathogen interaction, glutathione metabolism and starch/sucrose metabolism. Quantitative and qualitative changes were also dependent on the presence of endobacterium both in healthy and B. cinerea infected plants.