Microbiome-mediated tolerance of wild tomato to the invasive insect Prodiplosis longifila

Plant roots are colonized by diverse communities of microorganisms that can affect plant growth and enhance plant tolerance to (a)biotic stresses. Here, we investigated the role of the indigenous soil microbiome in tolerance of tomato to the invasive sap-sucking insect Prodiplosis longifila (Diptera: Cecidomyiidae).Native and agricultural soils were sampled from the Andean region in Southern Ecuador and tested, in greenhouse bioassays, for leaf tissue damage caused by P. longifila on domesticated Solanum lycopersicum cv. Moneymaker and wild tomato S. pimpinellifolium. We observed no significant differences in insect damage between domesticated and wild tomatoes grown in live native or agricultural soils. However, when grown in sterilized native and agricultural soils, wild tomato was more severely affected by the insect than the domesticated tomato. Subsequent microbiome analyses revealed that soil sterilization impacted overall rhizobacterial diversity and abundance in the wild tomato rhizosphere. Particularly, the abundance of Actinoplanes was reduced upon sterilization which significantly correlated with loss of insect tolerance. Metagenome analyses and subsequent genome assembly of Micromonosporaceae (Actinoplanes family) suggested a putative association between motility, chemotaxis, membrane transport, chorismate and lanthipeptide biosynthesis and insect tolerance. Collectively, these results suggest that wild tomato S. pimpinellifolium, in contrast to domesticated S. lycopersicum, relies on specific members of the root-associated microbiome for protection against the invasive insect P. longifila aboveground.