Immune activation by a phloem-colonizing plant pathogen drives citrus Huanglongbing disease development.

Abstract

Citrus Huanglongbing (HLB), caused by Candidatus Liberibacter asiaticus (CLas), was reported to be a pathogen-triggered immune disease. However, genetic evidence and mechanistic understanding for such a disease model are lacking. Here, we showed that mitigation of reactive oxygen species (ROS) accumulation by targeted overexpression of FLAVODOXIN in chloroplasts, but not mutation of respiratory burst oxidase protein D (RBOHD), reduces HLB symptoms. We explored the involvement of phloem callose deposition in HLB via treatment with a callose synthesis inhibitor, gene expression, mutation, and overexpression of CALS7 genes. Using tomato-Ca. L. psyllaurous as a surrogate, we demonstrated that Liberibacter causes immune diseases through the effector-triggered immunity (ETI) pathway mediated by two EDS1 modules (EDS1-NRG1 and EDS1-PAD4-ADR1) but not by NDR1. The eds1a/eds1b or eds1a mutant of citrus showed increased HLB resistance or reduced immune responses compared with the wild type after CLas inoculation. This study provides genetic evidence and mechanistic insights into Ca. Liberibacter-triggered immune-mediated diseases, highlighting parallels between immune dysregulation in humans and plants.