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.

Bimodular architecture of bacterial effector SAP05 drives ubiquitin-independent targeted protein degradation

“…SAP05 binds both the von Willibrand factor type A (vWA) domain of Rpn10 and the zinc-finger (ZnF) domain of multiple members of two distinct plant transcription factor families, known as SQUAMOSA-PROMOTER BINDING PROTEIN-LIKE (SPL) and GATA BINDING FACTORS (GATAs) (Huang et al, 2021). By hijacking Rpn10, SAP05 mediates the degradation of these TFs, leading to dramatic changes in plant development that includes leaf and stem proliferations, neoteny and increased longevity (Huang et al, 2021), as well as increased plant colonization of phytoplasma insect vectors (Huang and Hogenhout, 2022). Other phytoplasma effectors, known as SAP54/phyllogens, were found to hijack the 26S proteasome shuttle factor RAD23 to mediate the degradation of plant MCM1, AGAMOUS, DEFICIENS, and SRF, serum response factor (MADS) domain transcription factors leading to the induction of leaf-like flowers and other changes in flower development (MacLean et al, 2014), and this also occurs in a ubiquitinindependent manner (Kitazawa et al, 2022).…”

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

“…As obligate bacterial parasites, phytoplasmas frequently trigger the emergence of unusual plant structures such as leaf-like floral parts (phyllody) and the excessive growth and clustering of leaves and branches (witch's broom) (Lee et al, 2000;Al-Subhi et al, 2018;Kumari et al, 2019). These alterations not only compromise plant health but also promote attraction and colonization of insect vectors that are primarily responsible for phytoplasma spread and transmission (Sugio et al, 2011a;Frost et al, 2013;MacLean et al, 2014;Orlovskis & Hogenhout, 2016;Clements et al, 2021;Al-Subhi et al, 2021;Huang & Hogenhout, 2022). The responsible phytoplasma genes encode for effector molecules that, once inside the plant cell cytoplasm, target and typically disrupt or degrade essential plant transcription factors involved in growth, development, and defence (review by Wang et al, 2024 and references therein as well as Liu et al, 2023;Suzuki et al, 2024;Correa Marrero et al, 2024;Yan et al, 2024;Zhang et al, 2024).…”

Protein interaction mapping reveals widespread targeting of development‐related host transcription factors by phytoplasma effectors

“…Phytoplasma‐infected plants often display altered morphology (Bertaccini, 2007) that suggest interference with fundamental developmental processes. For example, the Aster Yellows phytoplasma strain Witches' Broom ( C. Phytoplasma asteris ; AY‐WB phytoplasma) induces phyllody (conversion of flowers into leaf‐like structures), virescence (green coloration of non‐green floral tissue) and witches' brooms (increased proliferation of stems, branches and leaves), and promotes the attraction of AY‐WB leafhopper vectors to infected plants (Huang et al., 2020, 2021; Huang & Hogenhout, 2022; MacLean et al., 2014; Orlovskis & Hogenhout, 2016; Pecher et al., 2019; Sugio, Kingdom, et al., 2011; Sugio, MacLean, et al., 2011). Additionally, infected plants are often sterile, and thus serve the sole purpose of feeding and propagating the bacteria.…”

“…SAP11 binds and destabilizes certain TCP transcription factors involved in axillary meristem outgrowth, leaf shape determination, and jasmonate signalling, leading to an altered morphology and decreased plant defense (Chang et al., 2018; Pecher et al., 2019; Sugio et al., 2014; Sugio, Kingdom, et al., 2011; Wang et al., 2018). These three SAP effectors promote the attraction and reproduction of leafhopper vectors on plants (Huang & Hogenhout, 2022; Orlovskis & Hogenhout, 2016; Sugio, Kingdom, et al., 2011; Sugio, MacLean, et al., 2011). Finally, TENGU causes dwarfism, witches' broom, and arrested flower development.…”