An Aphid Facultative Symbiont Suppresses Plant Defense 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 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.