Interfering with plant developmental timing promotes susceptibility to insect vectors of a bacterial parasite

Abstract

Multi-trophic parasites often modulate host behaviors and development to attract other hosts. However, whether these modulations are controlled by specific parasite genes and are adaptive remains debated. Insect-transmitted phytoplasma parasites take control of their plant host by turning them into Zombie plants, which feature spectacular vegetative organ proliferations and juvenilization. The phytoplasma effector SAP05 induces these symptoms by mediating the degradation of multiple plant SPL and GATA developmental transcription factors via recruiting the ubiquitin receptor RPN10. Here, we investigated if these SAP05-induced modulations impact the leafhopper vectors on which phytoplasmas depend for spread. SAP05 promotes leafhopper reproduction on Arabidopsis thaliana in a RPN10-dependent manner. Moreover, SAP05 homologs that degrade SPLs and both SPLs and GATAs promote leafhopper reproduction, whereas those that degrade only GATAs do not. Leafhoppers also produced more progeny on plants with misregulated MiR156, which suppresses SPL expression. SPLs control several developmental processes. Surprisingly, leaf color and shape changes and increased leaf numbers did not correlate to leafhopper progeny increases, whereas disturbing the plant phase transition processes did. Therefore, only specific phenotypes induced by a single parasite gene extend beyond one host to control another and promote host-host attractions of a multi-trophic parasite.