Kliot, A. | Search bioRxiv

bioRxiv2024

The conserved aphid saliva chemosensory protein effector Mp10 targets plant AMSH deubiquitinases at cellular membranes to suppress pattern-triggered immunity

Chemosensory proteins (CSPs) are a conserved family present in insects and other arthropods, recognized for their critical roles in both intra- and interspecies communication. However, the functional mechanisms of these proteins remain largely unexplored. In our previous research, we identified a CSP in aphid saliva, Mp10, from the peach-potato aphid Myzus persicae, which functions as an effector protein modulating host plant immunity. Mp10 suppresses pattern recognition receptor (PRR)-triggered immunity (PTI), the first layer of plant defence, while also inducing effector-triggered immunity (ETI). In this study, we elucidate the molecular mechanisms by which Mp10 suppresses PTI. Our findings reveal that Mp10 interacts with AMSH deubiquitinase enzymes in plants, as shown by yeast two-hybrid, co-immunoprecipitation (co-IP), and FRET-FLIM assays, with these interactions predominantly localized to intracellular membranes. Mp10 was found to modulate the dynamics of membrane-bound PRR receptor kinases in plant cells. Co-IP and mass spectrometry analyses demonstrated that Mp10 and AMSH2 associate with a range of PRR kinases, PRR-associated kinases, and proteins involved in the intracellular trafficking of membrane proteins. Mp10 reduces the accumulation of these kinases at the cell surface by promoting their internalization to internal membranes, thereby dampening PTI. Supporting this, a dominant-negative catalytically inactive variant of AMSH2 also inhibits PTI. Interestingly, Mp10 orthologues from other sap-feeding hemipteran insects exhibit similar immune-suppressive activities, and our findings show that their interaction with plant AMSH proteins is conserved, indicating this immune-suppression mechanism is evolutionarily ancient.

plant biology↗

bioRxiv2024

Phytoplasma Targeting of MADS-Box Factor SVP Suppresses Leaf Responses to Insect Vector Males, Promoting Female Attraction and Colonization

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.

plant biology↗