Obligate parasites often trigger significant changes in their hosts to facilitate transmission to new hosts. The molecular mechanisms behind these extended phenotypes - where genetic information of one organism is manifested as traits in another - 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 the insects were attracted to leaves and the leaf-like flowers were not required. Here, we made the surprising discovery that leaf exposure to leafhopper males is required for the attraction phenotype, suggesting a leaf response that distinguishes leafhopper sex in the presence of SAP54. In contrast, this phytoplasma effector 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. SAP54 essentially acts as a molecular 'matchmaker', helping male leafhoppers more easily locate mates by degrading SVP-containing complexes in leaves. 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.
Keywords: A. thaliana; SAP54/PHYL1; effector protein; extended phenotype; insect vector; phytoplasma; plant biology; short vegetative phase.
The parasitic bacterium phytoplasma is a master manipulator. It turns its hosts into sterile ‘zombie’ plants that remain alive only to support the parasite. Phytoplasma secretes a protein called SAP54, which transforms the flowers of the plants into leaf-like structures. Until recently, scientists believed this transformation was how the parasite attracted tiny sap-feeding insects called leafhoppers, which act as vectors that transport phytoplasma to its next host. However, more recent research has shown that the transformation of flowers into leaf-like structures is not needed to lure leafhoppers to the plant. So, what is it about SAP54 that manipulates the preferences of leafhoppers? To find out, Orlovskis et al. genetically modified plants to produce SAP54. They then carefully observed the number of male and female leafhoppers attracted to the mutant plants compared to plants that had not been genetically manipulated. They also used genetic analysis to investigate the proteins controlling the plant’s defence mechanisms. Orlovskis et al. found that SAP54 attracted female leafhoppers to the leaves of the plant, but only when males were also present. SAP54 also suppressed the plant’s defences when males were on the leaves, making the plant more inviting to females. Increasing the number of females naturally facilitates breeding, resulting in more insects that can transport the parasite to new host plants. A plant protein, called SHORT VEGETATIVE PHASE (or SVP for short), turned out to be critical in this process. Orlovskis et al. discovered that SAP54 promotes the breakdown of SVP, and plants lacking this protein also attracted more females when exposed to male leafhoppers. This suggests that SAP54 acts as a ‘molecular matchmaker’, helping male leafhoppers find mates by breaking down SVP in leaves. The involvement of SVP in attracting leafhoppers is surprising, as the family of proteins which SVP belongs to is primarily known for regulating developmental processes, such as flowering, rather than influencing how plants interact with their environment. These findings deepen our understanding of the complex relationships between parasites, plants and insects, demonstrating how parasites manipulate both plant biology and insect behaviour. This knowledge could inform new strategies for controlling plant diseases spread by insects, potentially reducing crop losses caused by phytoplasma.
© 2024, Orlovskis et al.