An aphid facultative symbiont suppresses plant defence by manipulating aphid gene expression in salivary glands

Abstract

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 harbouring S. symbiotica had longer feeding duration on Medicago truncatula than Serratia-free aphids. Contrastingly, Serratia-free aphids triggered higher accumulation of reactive oxygen species (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, impairs plant defence response by suppressing Ca²⁺ elevation and ROS accumulation, allowing colonization of aphids. This study has provided an insight into how facultative symbionts facilitate aphid colonization and adaptation to host plants.

Keywords: Acyrthosiphon pisum; Serratia symbiotica; calcium; histidine-rich calcium-binding protein-like.