Manipulation of juvenile hormone signaling by the fire blight pathogen Erwinia amylovora mediates fecundity enhancement of pear psylla.

Abstract

In nature, plant pathogens often rely on insect vectors for transmission. Through long-term evolution, plant pathogens and insect vectors have established a mutually beneficial symbiotic relationship. Fire blight, caused by the Gram-negative bacterium Erwinia amylovora (Eam), poses a significant global threat to apple and pear production due to its rapid dissemination among host plants of the Rosaceae family. Despite evidence of E. amylovora transmission by various insects, the association between this pathogen and the pear psylla Cacopsylla chinensis, a common vector insect in pear orchards, remains unclear. Sampling investigations and qRT-PCR results revealed that C. chinensis, from 11 pear orchards severely affected by fire blight disease in Xinjiang of China, harbored varying levels of this pathogen. Eam-positive females exhibited significantly higher fecundity compared to Eam-negative individuals, displaying accelerated ovarian development and a notable increase in egg production. Further RNAi results revealed that juvenile hormone (JH) receptor methoprene-tolerant (CcMet) and a crucial downstream gene Krüppel-homologue 1 (CcKr-h1) mediated the fecundity improvement of C. chinensis induced by Eam. Additionally, miR-2b, which targets CcKr-h1, was identified as being involved in Eam-induced fecundity enhancement in C. chinensis. This study unveils, for the first time, that Eam colonize and amplify the fecundity of C. chinensis females. Host miR-2b targets CcKr-h1 of the JH signaling pathway to regulate the heightened fecundity of C. chinensis induced by Eam. These findings not only broaden our understanding of the interaction between plant pathogens and insect vectors, but also provide novel strategies for managing fire blight and pear psylla. © 2024 Society of Chemical Industry.