Microbiome-Mediated Resistance of Wild Tomato to the Invasive Insect Prodiplosis longifila

Plant roots are colonised by diverse communities of microorganisms that can affect plant growth and enhance plant resistance to (a) biotic stresses. We investigated the role of the indigenous soil microbiome in the resistance of tomato to the invasive sap-sucking insect Prodiplosis longifila (Diptera: Cecidomyiidae). Native and agricultural soils were sampled from the Andes 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 sterilised native and agricultural soils, wild tomato was more severely affected by the insect than the domesticated tomato. Microbiome analyses revealed that soil sterilisation impacted overall rhizobacterial diversity and abundance in wild tomato. Particularly, Actinoplanes abundance was reduced upon sterilisation, which significantly correlated with loss of insect resistance. Metagenome analyses and genome assembly of Micromonosporaceae (Actinoplanes family) suggested a putative association between motility, chemotaxis, membrane transport, chorismate, and lanthipeptide biosynthesis and insect resistance. This indicates that wild S. pimpinellifolium, in contrast to domesticated S. lycopersicum, relies on specific members of the root-associated microbiome for P. longifila protection.