Rickettsia transmission from whitefly to plants benefits herbivore insects but is detrimental to fungal and viral pathogens

ABSTRACT Bacterial endosymbionts play important roles in the life histories of herbivorous insects by impacting their development, survival, reproduction, and stress tolerance. How endosymbionts may affect the interactions between plants and insect herbivores is still largely unclear. Here, we show that endosymbiotic Rickettsia belli can provide mutual benefits also outside of their hosts when the sap-sucking whitefly Bemisia tabaci transmits them to plants. This transmission facilitates the spread of Rickettsia but is shown to also enhance the performance of the whitefly and co-infesting caterpillars. In contrast, Rickettsia infection enhanced plant resistance to several pathogens. Inside the plants, Rickettsia triggers the expression of salicylic acid-related genes and the two pathogen-resistance genes TGA 2.1 and VRP, whereas they repressed genes of the jasmonic acid pathway. Performance experiments using wild type and mutant tomato plants confirmed that Rickettsia enhances the plants’ suitability for insect herbivores but makes them more resistant to fungal and viral pathogens. Our results imply that endosymbiotic Rickettsia of phloem-feeding insects affects plant defenses in a manner that facilitates their spread and transmission. This novel insight into how insects can exploit endosymbionts to manipulate plant defenses also opens possibilities to interfere with their ability to do so as a crop protection strategy.IMPORTANCEMost insects are associated with symbiotic bacteria in nature. These symbionts play important roles in the life histories of herbivorous insects by impacting their development, survival, reproduction as well as stress tolerance. Rickettsia is one important symbiont to the agricultural pest whitefly Bemisia tabaci. Here, for the first time, we revealed that the persistence of Rickettsia symbionts in tomato leaves significantly changed the defense pattern of tomato plants. These changes benefit both sap-feeding and leaf-chewing herbivore insects, such as increasing the fecundity of whitefly adults, enhancing the growth and development of the noctuid Spodoptera litura, but reducing the pathogenicity of Verticillium fungi and TYLCV virus to tomato plants distinctively. Our study unraveled a new horizon for the multiple interaction theories among plant-insect-bacterial symbionts.