An Aphid Facultative Symbiont Suppresses Plant Defense by Manipulating Aphid Gene Expression in Salivary Glands

Aphids often carry facultative symbionts to achieve diverse advantages. Serratia symbiotica, one of facultative endosymbionts, increases aphid tolerance to heat. However, whether it benefits aphid colonization on host plants is yet to be determined. In the current study, we found that Acyrthosiphon pisum harboring S. symbiotica had longer feeding duration on Medicago truncatula than Serratia-free aphids. Contrastingly, Serratia-free aphids triggered higher accumulation of ROS, jasmonic acid and salicylic acid responsive genes and cytosolic Ca2+ elevations than Serratia-infected aphids. Transcriptomic analysis of salivary glands indicated that a histidine-rich Ca2+-binding protein-like gene (ApHRC) was expressed more highly in the salivary gland of Serratia-infected aphids than that of Serratia-free aphids. Once ApHRC was silenced, Serratia-infected aphids also displayed shorter phloem-feeding duration and caused Ca2+ elevation and ROS accumulation in plants. Our results suggest that ApHRC, a potential effector up-regulated by S. symbiotica in the salivary glands, evaded plant defense response by suppressing Ca2+ elevation and ROS accumulation, allowing colonization of aphids. This study has provided a revolutionary insight into how facultative symbionts facilitate aphid colonization and adaption to host plants.