Biology subjects

Hogenhout, S. A.

Publications and source records attributed to Hogenhout, S. A..

At least 19 recordsLinked to original sources

bioRxiv2026

The aphid effector CathB6 suppresses EDS1-dependentimmunity and rewires MORF2-GUN1-GLK signalling tosustain host cellular homeostasis in Arabidopsis

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 STATEMENTAphids 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.

plant biology↗

bioRxiv2026

Rapidly evolving aphid gall effector proteins exhibit saposin-like folds

Many insects manipulate plants by injecting effector proteins. In one extreme example of this molecular "hijacking", Hormaphis cornu aphids inject bicycle proteins into Hamamelis virginiana, contributing to the development of novel organs called galls. Bicycle proteins share no amino acid sequence similarity with proteins of known function. Here, we report the crystal structures of two divergent bicycle proteins. Both proteins contain saposin-like folds: one with multiple disulfide bonds exhibits a swapped domain topology; the other has no disulfide bonds and possesses two distinct, tandem domains. To explore the structural evolution of bicycle proteins, we attempted to predict bicycle protein structures with Alphafold2 (AF2) and other deep learning programs. While AF2 did not recover the two experimental structures using existing databases, it succeeded when provided with multiple sequence alignments (MSAs) of protein sequences from newly sequenced closely related species. Using this approach, we generated 2400 high-confidence bicycle protein predictions from seven aphid species. While all aphid bicycle proteins contain predicted saposin-like folds, they display a vast diversity of structural and physicochemical properties. While this diversity thwarts prediction of conserved functions encoded in structure, it suggests that bicycle proteins have evolved to target diverse plant processes and/or to evade plant immune surveillance. Our extension of AF2 with custom MSAs of proteins from closely related species provides a generalizable, powerful approach for predicting structures of rapidly evolving protein families. Significance statementParasites introduce specialized "effector" proteins into hosts to suppress host immunity and to release nutrients. The molecular functions and structures of most effector proteins are unknown. Effector proteins often evolve rapidly and share no similarity with proteins of known function. Here, we demonstrate that machine learning algorithms can predict the structures of aphid "bicycle" effector proteins when supplemented with data from closely related species. We exploit this finding to generate predictions of 2400 bicycle protein structures. Aphid bicycle proteins exploit a common folding motif, yet exhibit topologically distinct structures that form separate structural clusters. Despite the clustering of these proteins in structure space, they occupy a nearly uniformly physicochemical space, suggesting that they encode a large diversity of molecular functions.

molecular biology↗

bioRxiv2025

Whole-Genome Population Genomics Reveals Lineage Structure and Adaptive Potential of Philaenus spumarius, the Principal Vector of Xylella fastidiosa in Europe

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.

evolutionary biology↗

bioRxiv2025

RNA editing fine-tunes transcriptional plasticity and enhances the adaptability of Myzus persicae to diverse host plants

Parthenogenetic organisms can adapt to diverse and rapidly changing environments despite limited standing genetic variation, but the molecular mechanisms enabling such adaptability remain unclear. Here, we investigate this question in the green peach aphid (Myzus persicae, GPA), an asexual generalist herbivore capable of colonizing a wide range of host plants without underlying genetic change. By integrating RNA-seq and DNA-seq from genetically identical clones reared on different hosts, we identified 1,368 high-confidence RNA editing sites (RES), many of which exhibited strong host-dependent differences in editing levels. These RES encompassed all 12 possible nucleotide substitutions, with A-to-I, C-to-U, and U-to-C conversions being particularly prevalent. Editing at several sites shifted dynamically within 48 hours of host transfer and often coincided with changes in transcript abundance. Functional knockdown of the editing genes ADAR1 and ADAR2 reduced editing at specific sites, diminished fecundity, and abolished aphid survival on new hosts. Comparative analyses across aphid species reveal that although the biochemical signatures of A-to-I editing are deeply conserved, the genomic locations and functional roles of edited transcripts are species specific, reflecting lineage-specific adaptive strategies. Together, our findings demonstrate that RNA editing provides a rapid, reversible mechanism for environmental acclimation in GPA, enabling adaptive phenotypic plasticity even in the absence of genetic variation. This work establishes RNA editing as a key molecular basis for the remarkable ecological generalism of clonal organisms. Significance statementA major question in evolutionary biology is how clonal organisms with little genetic variation rapidly adapt to diverse, changing environments. Here we show that RNA editing provides a mechanism enabling the parthenogenetic green peach aphid (Myzus persicae) to colonize a wide range of host plants. RNA editing generates transcriptomic diversity, responds quickly to host shifts, and is essential for adaptation, as silencing ADAR genes disrupts A-to-I editing, reduces fitness, and prevents survival on new hosts. Comparative analyses across aphid species reveal that although the biochemical features of A-to-I editing are conserved, its genomic deployment and functional outcomes differ among species, reflecting lineage-specific strategies. These findings demonstrate that RNA editing creates a dynamic regulatory layer that offsets constraints of asexual reproduction.

molecular biology↗

bioRxiv2025

Effector Innovation in Genome-Reduced Phytoplasmas and Other Host-Dependent Mollicutes

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 witchs 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.

microbiology↗

bioRxiv2025

Aphid effector Mp10 balances immune suppression and defence activation through EDS1-dependent modulation of plant DAMP responses

O_LIDamage-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. C_LIO_LIBy 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. C_LIO_LIWe 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. C_LIO_LIWhile 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. C_LI

plant biology↗

bioRxiv2024

Plant-induced transcriptional plasticity diverges between generalist and specialist herbivores

Most herbivores are specialized on particular host plants but some are generalists that can exploit distinct hosts. Generalists may have evolved adaptive transcriptional plasticity to cope with the defenses of the different hosts. However, the fundamental differences in plant-induced transcriptional plasticity between generalists and specialists remain poorly understood. Here, we investigated transcriptional plasticity of the generalist aphid Myzus persicae and two specialist aphids, Brevicoryne brassicae and Rhopalosiphum padi, by transferring them between Brassica napus (a host for B. brassicae but not for R. padi) and Zea mays (a host for R. padi but not for B. brassicae), both suitable hosts for M. persicae. Generalist and specialist aphids exhibited transcriptional plasticity coordinately in response to different plant species, but their gene expression patterns often diverged. Generalists suppressed plant-defense salicylic acid (SA) signaling in the host plants, while specialist aphids provoked it in nonhost plants. SA signaling had limited effects on gene expression in the generalist aphids, but significantly shaped transcriptional responses of the specialists. These findings underscore the fundamental differences in plant-induced transcriptional plasticity between generalists and specialists and highlight the critical role of plasticity directionality in insect adaptation. Significance statementMost insects specialize in feeding on just a few specific plants, but some generalists can thrive on many plant species. This study compares the gene expression of green peach aphid Myzus persicae, a generalist, with two specialist aphids in response to different types of plants. Generalists showed adaptive plasticity in their gene responses, while specialists often exhibited opposite gene expression changes. Interestingly, generalists appeared to suppress plant defense signals like salicylic acid, while specialists tended to trigger them. These findings highlight how gene expression plasticity enables generalists to adapt and survive, providing new insights into the evolution of insect-plant interactions.

plant biology↗

bioRxiv2024

Chromosome-level Assemblies of Three Candidatus Liberibacter solanacearum Vectors: Dyspersa apicalis, Dyspersa pallida, and Trioza urticae (Hemiptera: Psylloidea)

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. SignificancePsyllid 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.

genomics↗

bioRxiv2024

Genomes of two invasive Adelges species (hemlock woolly adelgid and pineapple gall adelgid) enable characterization of nicotinic acetylcholine receptors

Two invasive hemipteran adelgids are associated with widespread damage to several North American conifer species. Adelges tsugae, hemlock woolly adelgid, was introduced from Japan and reproduces parthenogenetically in North America, where it has rapidly decimated Tsuga canadensis and Tsuga caroliniana (the eastern and Carolina hemlocks, respectively). Adelges abietis, eastern spruce gall adelgid, introduced from Europe, forms distinctive pineapple-shaped galls on several native spruce species. While not considered a major forest pest, it weakens trees and increases susceptibility to additional stressors. Broad-spectrum insecticides that are often used to control adelgid populations can have off-target impacts on beneficial insects. Whole genome sequencing was performed on both species to aid in development of targeted solutions that may minimize ecological impact. Adelges abietis was sequenced using Illumina Linked-Read technology from 30 pooled individuals, with Hi-C scaffolding performed using data from a single individual collected from the same host plant. Adelges tsugae used Oxford Nanopore long-read sequencing from pooled nymphs. The assembled A. tsugae and A. abietis genomes, pooled from several parthenogenetic females, are 220.75 Mbp and 253.16 Mbp, respectively. Each consists of eight autosomal chromosomes, as well as two sex chromosomes (X1/X2), supporting the XX-XO sex determination system. The genomes are over 96% complete based on BUSCO assessment. Genome annotation identified 11,424 and 12,060 protein-coding genes in A. tsugae and A. abietis, respectively. Comparative analysis of proteins across 29 hemipteran species and 14 arthropod outgroups identified 31,666 putative gene families. Gene family evolution analysis with CAFE revealed lineage-specific expansions in immune-related aminopeptidases (ERAP1) and juvenile hormone binding proteins (JHBP), contractions in juvenile hormone acid methyltransferases (JHAMT), and conservation of nicotinic acetylcholine receptors (nAChR). These genes were explored as candidate families towards a long-term objective of developing adelgid-selective insecticides. Structural comparisons of proteins across seven focal species (Adelges tsugae, Adelges abietis, Adelges cooleyi, Rhopalosiphum maidis, Apis mellifera, Danaus plexippus, and Drosophila melanogaster) revealed high conservation of nAChR and ERAP1, while JHAMT exhibited species-specific structural divergence. The potential of JHAMT as a lineage-specific target for pest control was explored through virtual drug and pesticide screening.

genomics↗

bioRxiv2024

Aphid effectors suppress plant immunity via recruiting defence proteins to processing bodies

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.

plant biology↗

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↗

bioRxiv2023

Bimodular Architecture of Bacterial Effector SAP05 Drives Ubiquitin-Independent Targeted Protein Degradation

In eukaryotes, targeted protein degradation (TPD) typically depends on a series of interactions among ubiquitin ligases that transfer ubiquitin molecules to substrates leading to degradation by the 26S proteasome. We previously discovered that the bacterial effector protein SAP05 mediates ubiquitin-independent TPD. SAP05 forms a ternary complex via interactions with the von Willebrand Factor Type A (vWA) domain of the proteasomal ubiquitin receptor Rpn10 and the Zinc-finger (ZnF) domains of the SQUAMOSA-PROMOTER BINDING PROTEIN-LIKE (SPL) and GATA BINDING FACTOR (GATA) transcription factors (TFs). This leads to direct TPD of the TFs by the 26S proteasome. Here, we report the crystal structures of the SAP05-vWA complex at 2.17 [A] resolution and of the SAP05-ZnF(SPL5) complex at 2.20 [A] resolution. Structural analyses revealed that SAP05 displays a unique bimodular architecture with two distinct non-overlapping surfaces, a loop surface with three protruding loops that form electrostatic interactions with ZnF, and a sheet surface featuring two {beta}-sheets, loops and -helices that establish polar interactions with vWA. SAP05 binding to ZnF TFs involves single amino acids responsible for multiple contacts, while SAP05 binding to vWA is more stable due to the necessity of multiple mutations to break the interaction. In addition, positioning of the SAP05 complex on the 26S proteasome points to a mechanism of protein degradation. Collectively, our findings demonstrate how a small bacterial bimodular protein can bypass the canonical UPS cellular proteolysis pathway, enabling ubiquitin-independent TPD in eukaryotic cells. This knowledge holds significant potential for the creation of novel TPD technologies.

biochemistry↗

bioRxiv2022

Hybridisation has shaped a recent radiation of grass-feeding aphids

Aphids are common crop pests. These insects reproduce by facultative parthenogenesis involving several rounds of clonal reproduction interspersed with an occasional sexual cycle. Furthermore, clonal aphids give birth to live apterous or winged young that are already pregnant. Together, these qualities enable rapid population growth and have facilitated the colonisation of crops globally. In several cases so-called "super clones" have come to dominate agricultural systems. However, the extent to which the sexual stage of the aphid life cycle has shaped global pest populations has remained largely unclear, as have the origins of successful lineages. Here, we used chromosome-scale genome assemblies to disentangle the evolution of two of the most significant global pests of cereals - the English (Sitobion avenae) and Indian (Sitobion miscanthi) grain aphids. We found that genome-wide divergence between S. avenae and S. miscanthi is low and that S. avenae sensu stricto is part of a larger cryptic species complex that includes multiple diverged S. miscanthi lineages. Moreover, comparison of haplotype-resolved assemblies reveals that the S. miscanthi isolate used for genome sequencing is likely a hybrid, with one of its diploid genome copies being closely related to S. avenae ([~]0.5% divergence) and the second being substantially more divergent (> 1%). Analyses of genotyping-by-sequencing (GBS) data of grain aphids from the UK and China revealed that S. avenae and S. miscanthi are part of a species complex with many highly differentiated lineages that predate the origins of agriculture. The complex consists of hybrid lineages that display a tangled history of hybridisation and genetic introgression. These data demonstrate that hybridisation has substantially contributed to grain aphid diversity, and hence, to the evolutionary potential of this important pest species.

evolutionary biology↗

bioRxiv2022

Interfering with plant developmental timing promotes susceptibility to insect vectors of a bacterial parasite

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.

plant biology↗

bioRxiv2021

Novel effector recognition capacity engineered into a paired NLR complex

The Arabidopsis RRS1-R Resistance gene confers recognition of the bacterial acetyltransferase PopP2 and another bacterial effector, AvrRps4. The RRS1-S allele recognizes AvrRps4 but not PopP2. RRS1- R/RRS1-S heterozygotes cannot recognize PopP2. RRS1-R and RRS1-S also suppress the constitutive RPS4-dependent autoactivity of RRS1-Rslh1. Phytoplasmas cause important plant diseases, and their effectors can cause degradation of specific host proteins. We tested whether attaching a pathogen effector-dependent degron to RRS1-R, enabling its degradation by phytoplasma effector SAP05, could derepress RRS1-Rslh1 autoactivity, resulting in SAP05-dependent resistance. In transient assays in tobacco, RRS1-R-derived constructs can confer a hypersensitive response (HR) to SAP05. However, phytoplasma infection assays in transgenic Arabidopsis resulted in delayed disease symptoms but not full resistance. We provide a proof-of-concept strategy utilizing the recessiveness of a plant immune receptor gene to engineer recognition of a pathogen effector that promotes degradation of a specific host protein.

plant biology↗

bioRxiv2021

Characterisation of the symbionts in the Mediterranean fruitfly gut

Symbioses between bacteria and their insect hosts can range from very loose associations through to obligate interdependence. While fundamental evolutionary insights have been gained from the in-depth study of obligate mutualisms, there is increasing interest in the evolutionary potential of flexible symbiotic associations between hosts and their gut microbiomes. Understanding relationships between microbes and hosts also offers the potential for exploitation for insect control. Here, we investigate the gut microbiome of a global agricultural pest, the Mediterranean fruitfly (Ceratitis capitata). We used 16S rRNA profiling to compare the gut microbiomes of laboratory and wild strains raised on different diets and from flies collected from various natural plant hosts. The results showed that medfly guts harbour a fairly simple microbiome, primarily determined by the larval diet in both wild and laboratory flies. However, regardless of the laboratory diet or natural plant host on which flies were raised, Klebsiella spp dominated the medfly microbiomes and resisted removal by antibiotic treatment. We sequenced the genome of the dominant putative Klebsiella spp (designated Medkleb) isolated from the gut of the Toliman wild type fruitfly strain. Genome-wide ANI analysis placed Medkleb within the K. oxytoca / michiganensis group. Molecular, sequence and phenotypic analyses supported its identity as K. oxytoca. Medkleb has a genome size (5 825 435 bp) which is 1.6 standard deviations smaller than the mean genome size of free-living Klebsiella spp, and lacks some genes involved in environmental sensing. Moreover, the Medkleb genome contains at least two recently acquired unique genomic islands as well as genes that encode pectinolytic enzymes capable of degrading plant cell walls. This may be advantageous given that the medfly diet includes unripe fruits containing high proportions of pectin. These results suggest that the medfly harbours a commensal gut bacterium that may have developed a mutualistic association with its host and provide nutritional benefits.

evolutionary biology↗

bioRxiv2021

Parasite co-opts a ubiquitin receptor to induce a plethora of developmental changes

Obligate parasites can induce complex and substantial phenotypic changes in their hosts in ways that favour their transmission to other trophic levels. However, mechanisms underlying these changes remain largely unknown. Here, we demonstrate how SAP05 protein effectors from insect-vectored plant pathogenic phytoplasmas take control of several plant developmental processes to simultaneously prolong host lifespan and induce witchs broom-like proliferations of leaf and sterile shoots, organs colonized by phytoplasmas and vectors. SAP05 acts by mediating the concurrent degradation of SPL and GATA developmental regulators via a process that uniquely relies on hijacking the plant ubiquitin receptor RPN10 independently of substrate lysine ubiquitination. RPN10 is highly conserved among eukaryotes, but SAP05 does not bind insect vector RPN10. A two-amino-acid substitution within plant RPN10 generates a functional variant that is resistant to SAP05 activities. Therefore, one effector protein enables obligate parasitic phytoplasmas to induce a plethora of developmental phenotypes in their hosts.

molecular biology↗