Sam T. Mugford

SUMMARY: Aphids use stylet mouthparts to probe plant tissues and deliver oral secretions into host cells, modulating immunity to establish long-term phloem feeding sites in sieve elements. This feeding behaviour make aphids efficient vectors of plant pathogens. We previously showed that Myzus persicae cathepsin B (CathB) effectors promote aphid colonization, accumulate in dynamic cytoplasmic processing bodies (p-bodies), bind the key Arabidopsis thaliana immune regulator EDS1, and recruit EDS1 together with its signalling partners PAD4 and ADR1 to p-bodies. However, the extent to which CathB effectors suppress EDS1-regulated immunity remains unclear. Here, we show that CathB6-expressing Arabidopsis lines exhibit substantial transcriptomic overlap with the eds1-2 mutant, consistent with CathB6 suppression of EDS1-dependent immunity. However, CathB6 also induces broader transcriptional reprogramming beyond that explained by loss of EDS1 function. A yeast two-hybrid screen identified the transcription factors GLK1 and GLK2, as well as several MORF proteins, as CathB6 interactors. CathB6-expressing plants recapitulated GLK- and MORF-regulated transcriptional changes, suppressing GUN1-associated activity while maintaining GLK-mediated expression of photosynthesis-associated nuclear genes (PhANGs). We found that GLKs promotes CathB6 nuclear accumulation and reduces its p-body association. TurboID proximity labelling further linked CathB6 to PhANG-associated proteins, known MORF2- and GUN1-interacting factors, p-body components, and actin–tubulin/myosin machinery, the latter being consistent with the highly dynamic behaviour of CathB6-associated p-bodies. Together, these data indicate that, beyond suppressing EDS1-mediated defenses, CathB6 interferes with the MORF2–GUN1–GLK signalling pathway, modulating plant defense responses while sustaining GLK-mediated PhANG expression to maintain cellular homeostasis during aphid attack. SIGNIFICANCE STATEMENT: Aphids damage crops and spread plant diseases while feeding. We discovered how a protein in aphid saliva, CathB6, helps these pests establish themselves on plants. CathB6 weakens a major immune pathway and alters communication between chloroplasts and the cell nucleus. This allows the aphid to reduce plant defences while maintaining photosynthesis and normal cell function. These findings reveal a sophisticated survival strategy and may identify ways to develop crops that are more resistant to aphids.

Philaenus spumarius (L.), the meadow spittlebug, is the principal European vector of Xylella fastidiosa . This xylem-feeding insect has a broad host range, ecological plasticity, and mobility, making it an efficient vector across diverse landscapes. Yet, major gaps remain in understanding its genetic diversity, migration patterns, and local adaptation, limiting effective control of X. fastidiosa outbreaks. To address these gaps, we worked with a global network of researchers and citizen scientists to assemble a geographically and ecologically diverse collection of P. spumarius samples. We generated a chromosome-level genome assembly for P. spumarius and high-quality assemblies for four related spittlebug species, providing a robust genomic framework for evolutionary and epidemiological studies. Resequencing 430 P. spumarius individuals from across the globe uncovered boreal, temperate, and semi-arid lineages shaped by geography and climate. The lineages vary in reproductive isolation and in the degree of mito-nuclear divergence. Iberian populations grouped with an individual identified as P. tesselatus contributing to regional genetic complexity. Genomic scans identified loci under selection in Apulian populations, including signatures in sulfotransferase (SULT) genes potentially linked to behavioural plasticity, host plant specialisation, or insecticide resistance in olive-growing regions. Migration analyses indicated limited long-distance dispersal but strong local connectivity, consistent with the rapid regional spread of X. fastidiosa . Together, these findings reveal the lineage structure and adaptive potential of P. spumarius , the key vector of X. fastidiosa in Europe. They underscore the importance of targeted surveillance of locally adapted populations and provide genomic tools for monitoring vector dynamics and mitigating emerging disease risks.

Summary: Damage‐associated molecular pattern (DAMP)‐triggered immunity (DTI) serves as a crucial first line of defence against aphid attack, yet how aphids manage this response remains unclear. By investigating the colonisation of Arabidopsis thaliana by the highly polyphagous peach–potato aphid (Myzus persicae), we identified cell wall‐derived DAMPs, specifically oligogalacturonides (OGs), as key in inducing DTI against aphids. The OG‐responsive immune components BRASSINOSTEROID INSENSITIVE 1‐ASSOCIATED RECEPTOR KINASE 1/BAK1‐LIKE 1, CPK5/CPK6, GLYCINE‐RICH PROTEIN 3, and EDS1 collectively contribute to DTI limiting aphid colonisation. We found that aphid feeding limits OG production in response to wounding. Additionally, the salivary chemosensory protein (CSP) effector Mp10/CSP4, which is known to be delivered into the cytoplasm of plant cells early in aphid attack, inhibits OG‐induced DTI. While Mp10 suppresses OG‐induced DTI, it also interacts with EDS1‐mediated defences, enhancing aphid fecundity in the absence of EDS1 while restoring OG responsiveness, revealing its broader role in immune modulation and effector‐driven host adaptation.

Aphids are small insects that have developed specialized mouthparts and effector proteins to establish long-term relationships with plants. The peach-potato aphid Myzus persicae is a generalist, feeding on many plant species and capable of transmitting numerous pathogens. This study reveals how host-responsive cathepsin B (CathB) proteins in the oral secretions of M. persicae facilitate aphid survival by modulating plant immune responses. Host-responsive CathB proteins localize to plant processing bodies (p-bodies), cytoplasmic ribonucleoprotein granules involved in messenger RNA storage or decay. Upon localization, these CathB proteins recruit key immune regulators EDS1, PAD4, and ADR1 to these bodies, suppressing plant defenses. A plant protein, Acd28.9 (Hsp20 family), counteracts this CathB activity and contributes to plant resistance to aphids. These findings highlight an unexpected role for p-bodies in plant immunity and uncover a plant resistance mechanism to aphid infestation.

Obligate host-associated bacteria with reduced genomes, such as phytoplasmas, face strong evolutionary constraints, including metabolic dependence on hosts, limited horizontal gene transfer (HGT), and frequent population bottlenecks. Despite these limitations, phytoplasmas, which are parasitic, insect-transmitted plant pathogens maintain a diverse arsenal of secreted effectors that manipulate both plant and insect hosts to promote infection and transmission. These effectors can suppress immunity and reprogram plant development, including witch’s broom and leaf-like flowers, through ubiquitin-independent degradation of key transcription factors. However, how phytoplasmas diversify and maintain these effectors in the absence of frequent genetic exchange remains unclear. To address this, we analysed the effectoromes of 239 phytoplasma genomes and identified a diverse set of secreted proteins, which we designated as Phytoplasma-Associated Molecular Effectors (PhAMEs). We found that PhAMEs targeting evolutionarily conserved and structurally constrained surfaces of host proteins are widespread across phytoplasmas. These effectors adopt compact, efficient folds. They often function as molecular scaffolds with dual interaction surfaces capable of linking host proteins or integrating signalling pathways. Such scaffolding PhAMEs have evolved multiple times independently, providing clear evidence of convergent evolution. Despite severe genomic constrains imposed by genome reduction and limited HGT, gene duplications, interface variations, domain fusions, and repeat expansions have helped the shaping effector fold and diversity. While the overall effector repertoire of phytoplasmas appeared largely unique, some PhAME domains share similarities with proteins from other mollicutes and pathogens. Collectively, our findings shed light on how genome-reduced bacteria innovate molecular functions and offer insights into phytoplasma biology, effector evolution, and host-pathogen dynamics. They also lay the groundwork for protein engineering approaches aimed at discovering or designing novel biomolecules with biotechnological potential.

Psyllids are major vectors of plant diseases, including Candidatus Liberibacter solanacearum (CLso), the bacterial agent associated with “zebra chip” disease in potatoes and “carrot yellows” disease in carrot. Despite their agricultural significance, there is limited knowledge on the genome structure and genetic diversity of psyllids. In this study, we provide chromosome-level genome assemblies for three psyllid species known to transmit CLso: Dyspersa apicalis (carrot psyllid), Dyspersa pallida, and Trioza urticae (nettle psyllid). As D. apicalis is recognized as the primary vector of CLso by carrot growers in Northern Europe, we also resequenced populations of this species from Finland, Norway, and Austria. Genome assemblies were constructed using PacBio HiFi and Hi–C sequencing data, yielding genome sizes of 594.01 Mbp for D. apicalis; 587.80 Mbp for D. pallida; and 655.58 Mbp for T. urticae. Over 90% of sequences anchored into 13 pseudo-chromosomes per species. D. apicalis and D. pallida assemblies exhibited high completeness, capturing over 92% of conserved Hemiptera single-copy orthologs. Furthermore, we identified sequences of the primary psyllid symbiont, Candidatus Carsonella ruddii, in all three species. Gene annotations were produced for each assembly: 17,932 unique protein-coding genes were predicted for D. apicalis; 18,292 for D. pallida; and 16,007 for T. urticae. We observed significant expansions in gene families, particularly those linked to potential insecticide detoxification, within the Dyspersa lineage. Resequencing also revealed the existence of multiple subpopulations of D. apicalis across Europe. These high-quality genome resources will support future research on genome evolution, insect–plant–pest interactions, and disease management strategies.

SUMMARY: Damage-associated molecular pattern (DAMP)-triggered immunity (DTI) serves as a crucial first line of defence against aphid attack, yet the mechanisms by which aphids suppress this response remain unclear. By investigating the colonisation of Arabidopsis thaliana by the highly polyphagous peach-potato aphid ( Myzus persicae ), we identified cell wall-derived DAMPs, specifically oligogalacturonides (OGs), as key in inducing DTI against aphids. The OG-responsive immune components BAK1/BKK1, CPK5/CPK6, GRP3, and EDS1 collectively contribute to DTI limiting aphid colonisation. We found that aphids limit OG production during feeding. Additionally, the salivary chemosensory protein (CSP) effector Mp10/CSP4, which is known to be delivered into the cytoplasm of plant cells early in aphid attack, inhibits OG-induced DTI. While Mp10 suppresses OG-induced DTI, it also interacts with EDS1-mediated defences, enhancing aphid fecundity in the absence of EDS1 but restoring OG responsiveness under attack, revealing its broader role in immune modulation and effector-driven host adaptation.

Psyllids are major vectors of plant diseases, including Candidatus Liberibacter solanacearum (CLso), the bacterial agent associated with ‘zebra chip’ disease in potatoes and ‘carrot yellows’ disease in carrot. Despite their agricultural significance, there is limited knowledge on the genome structure and genetic diversity of psyllids. In this study, we provide chromosome-level genome assemblies for three psyllid species known to transmit CLso: Dyspersa apicalis (carrot psyllid), Dyspersa pallida, and Trioza urticae (nettle psyllid). As D. apicalis is recognised as the primary vector of CLso by carrot growers in Northern Europe, we also resequenced populations of this species from Finland, Norway, and Austria. Genome assemblies were constructed using PacBio HiFi and Hi-C sequencing data, yielding genome sizes of: 594.01 Mbp for D. apicalis; 587.80 Mbp for D. pallida; and 655.58 Mbp for T. urticae. Over 90% of sequences anchored into 13 pseudo-chromosomes per species. The assemblies for D. apicalis and D. pallida exhibited high completeness, capturing over 92% of conserved Hemiptera single-copy orthologues, as assessed by Benchmarking Universal Single-Copy Orthologues (BUSCO) analysis. Furthermore, we identified sequences of the primary psyllid symbiont, Candidatus Carsonella ruddii, in all three species. Comparative genomic analyses demonstrated synteny with other psyllid species. Notably, we observed significant expansions in gene families, particularly those linked to potential insecticide detoxification, within the Dyspersa lineage. Resequencing efforts also revealed the existence of multiple subpopulations of D. apicalis across Europe. These high-quality genome resources will support future research on genome evolution, insect-plant-pest interactions, and strategies for disease management. Significance Psyllid species are significant agricultural pests, known for transmitting plant diseases like Candidatus Liberibacter solanacearum (CLso), which causes ‘zebra chip’ in potatoes and ‘carrot yellows.’ However, genomic data on psyllids are limited. In this study, we present high-quality, chromosome-level genome assemblies for three psyllid species: Dyspersa apicalis, Dyspersa pallida, and Trioza urticae. We generated genome assemblies with over 90% of sequences anchored to 13 pseudo-chromosomes. Comparative analyses revealed gene expansions, particularly in detoxification pathways, suggesting adaptations within the Dyspersa lineage. Population resequencing of D. apicalis across Europe uncovered genetic subpopulations. These genomes will advance understanding of psyllid biology and inform disease management strategies.

Aphids are small insects that have developed specialized mouthparts and effector proteins to establish long-term relationships with plants. The peach-potato aphid, Myzus persicae , is a generalist, feeding on many plant species and capable of transmitting numerous pathogens. This study reveals how host-responsive cathepsins B (CathB) in the oral secretions of M. persicae facilitate aphid survival by modulating plant immune responses. Aphid CathB localize to processing bodies (p-bodies) and recruit key immune regulators EDS1, PAD4, and ADR1 to these bodies, suppressing plant defenses. A plant protein, Acd28.9 (Hsp20 family), counteracts this CathB activity and contributes to plant resistance to aphids. These findings highlight a novel role for p-bodies in plant immunity and uncover a plant resistance mechanism to aphid infestation.

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.