Molecular Matchmakers: Phytoplasma Effector SAP54 Targets MADS-Box Factor SVP to Enhance Attraction of Fecund Female Vectors by Modulating Leaf Responses to Male Presence

Abstract

Obligate parasites often trigger significant changes in their hosts to facilitate transmission to new hosts. The molecular mechanisms behind these hyper-extended phenotypes - where genetic information of the parasite modulates the biology of one host to facilitate transmission through another host - remain largely unclear. This study explores the role of the virulence protein SAP54, produced by parasitic phytoplasmas, in attracting leafhopper vectors. SAP54 is responsible for the induction of leaf-like flowers in phytoplasma-infected plants. However, we previously demonstrated that leaves are responsible for this attraction instead of leaf-like flowers. Here we made the surprising discovery that SAP54 enhances the colonization of plants by leafhopper females predominantly in the presence of leafhopper males, suggesting a sex-specific mechanism. In contrast, the presence of SAP54 alongside leafhopper females discourages further female colonization. We demonstrate that SAP54 effectively suppresses biotic stress response pathways in leaves exposed to the males. Critically, the host plant MADS-box transcription factor SHORT VEGETATIVE PHASE (SVP) emerges as a key element in the female leafhopper preference for plants exposed to males, with SAP54 promoting the degradation of SVP. This preference extends to female colonization of male-exposed svp null mutant plants over those not exposed to males. Our research underscores the dual role of the phytoplasma effector SAP54 in host development alteration and vector attraction - integral to the phytoplasma life cycle. Importantly, we clarify how SAP54, by targeting SVP, heightens leaf vulnerability to leafhopper males, thus facilitating female attraction and subsequent plant colonization by the insects. This study not only provides insights into the long reach of single parasite genes in extended phenotypes, but also opens avenues for understanding how transcription factors that regulate plant developmental processes intersect with and influence plant-insect interactions.