The phytoplasma bacterial plant parasite depends on leafhopper insects to spread and propagate itself. This study reveals how phytoplasma subverts plant development to turn flowers into leaves and thus make its host more attractive to leafhoppers.
Pathogens that rely upon multiple hosts to complete their life cycles often modify behavior and development of these hosts to coerce them into improving pathogen fitness. However, few studies describe mechanisms underlying host coercion. In this study, we elucidate the mechanism by which an insect-transmitted pathogen of plants alters floral development to convert flowers into vegetative tissues. We find that phytoplasma produce a novel effector protein (SAP54) that interacts with members of the MADS-domain transcription factor (MTF) family, including key regulators SEPALLATA3 and APETALA1, that occupy central positions in the regulation of floral development. SAP54 mediates degradation of MTFs by interacting with proteins of the RADIATION SENSITIVE23 (RAD23) family, eukaryotic proteins that shuttle substrates to the proteasome. Arabidopsis rad23 mutants do not show conversion of flowers into leaf-like tissues in the presence of SAP54 and during phytoplasma infection, emphasizing the importance of RAD23 to the activity of SAP54. Remarkably, plants with SAP54-induced leaf-like flowers are more attractive for colonization by phytoplasma leafhopper vectors and this colonization preference is dependent on RAD23. An effector that targets and suppresses flowering while simultaneously promoting insect herbivore colonization is unprecedented. Moreover, RAD23 proteins have, to our knowledge, no known roles in flower development, nor plant defence mechanisms against insects. Thus SAP54 generates a short circuit between two key pathways of the host to alter development, resulting in sterile plants, and promotes attractiveness of these plants to leafhopper vectors helping the obligate phytoplasmas reproduce and propagate (zombie plants).
Parasites that colonize multiple hosts often coerce these hosts into improving their own survival and reproduction rates. However, how parasites do this is largely unknown. Phytoplasmas are bacterial plant parasites that require sap-feeding insect vectors—leafhoppers—for their propagation and dispersal. It has been known for a long time that phytoplasmas stimulate dramatic developmental changes in a broad range of plant species, such as the conversion of flowers into leaves known as phyllody and the proliferation of stems known as “witches' broom.” Here we report how and why phytoplasmas cause these dramatic developmental changes. We identified a phytoplasma virulence protein, SAP54, which transforms flowers into leaves and converts plants into more attractive hosts for the egg-laying and reproduction of their leafhopper vectors. We show that SAP54 exerts its effect by promoting the degradation of proteins that regulate important developmental processes in flowering plants. These proteins are highly conserved transcription factors of the MADS-box family, and reducing their activity through SAP54–mediated degradation curtails flower development, generating sterile plants. This degradation process requires RAD23, a protein that recruits the transcription factors to the protein degradation machinery. The resulting sterile plants, which form leaves in place of flowers, are more attractive to leafhoppers, arguably making phytoplasmas master manipulators of the parasite world.