Biology subjects

Hogenhout, S. A.

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

28 records · Page 2Linked to original sources

bioRxiv2021

Plant pathogens convergently evolved to counteract redundant nodes of an NLR immune receptor network

In plants, NLR (nucleotide-binding domain and leucine-rich repeat-containing) proteins can form receptor networks to confer hypersensitive cell death and innate immunity. One class of NLRs, known as NRCs (NLR required for cell death), are central nodes in a complex network that protects against multiple pathogens and comprises up to half of the NLRome of solanaceous plants. Given the prevalence of this NLR network, we hypothesized that pathogens convergently evolved to secrete effectors that target NRC activities. To test this, we screened a library of 167 bacterial, oomycete, nematode and aphid effectors for their capacity to suppress the cell death response triggered by the NRC-dependent disease resistance proteins Prf and Rpi-blb2. Among five of the identified suppressors, one cyst nematode protein and one oomycete protein suppress the activity of autoimmune mutants of NRC2 and NRC3, but not NRC4, indicating that they specifically counteract a subset of NRC proteins independently of their sensor NLR partners. Whereas the cyst nematode effector SPRYSEC15 binds the nucleotide-binding domain of NRC2 and NRC3, the oomycete effector AVRcap1b suppresses the response of these NRCs via the membrane trafficking-associated protein NbTOL9a (Target of Myb 1-like protein 9a). We conclude that plant pathogens have evolved to counteract central nodes of the NRC immune receptor network through different mechanisms. Coevolution with pathogen effectors may have driven NRC diversification into functionally redundant nodes in a massively expanded NLR network.

plant biology↗

bioRxiv2020

Herbivore-induced activation of viral phosphatase disarms plant antiviral immunities for pathogen transmission

The survival of pathogens depends on their ability to overcome host immunity, especially arthropod-borne viruses (arboviruses) which must withstand the immune responses of both the host and the arthropod vector. Successful arboviruses often modify host immunity to accelerate pathogen transmission; however, few studies have explored the underlying mechanism. Here we report attracted herbivore infestation on the virus-infected plants promote transmission by the associated vector herbivore. This herbivore-induced defense suppression underpins a subversive mechanism used by Begomovirus, the largest genus of plant viruses, to compromise host defense for pathogen transmission. Begomovirus-infected plants accumulated {beta}C1 proteins in the phloem where they were bound to host defense regulators, transcription factor WRKY20 and two mitogen-activated protein kinases MPK3 and MPK6. Once perceiving whitefly herbivory or endogenous secreted peptide PEP1, the plants started dephosphorylation on serine33 and stimulated {beta}C1 protein as a phosphatase. {beta}C1 dephosphorylated MPK3/6 and WRKY20, the latter negatively regulated salicylic acid signaling and vascular callose deposition. This viral hijacking of WRKY20 accumulated more vascular callose by which enforced whitefly prolonged salivation and phloem sap ingestion, therefore impelling more virus transmission among plants. We present a scenario in which viruses dynamically respond to the presence of their vectors, suppressing host immunity and promoting pathogen transmission only when needed.

microbiology↗

bioRxiv2020

A chromosome-level genome assembly of the woolly apple aphid, Eriosoma lanigerum (Hausmann) (Hemiptera: Aphididae)

Woolly apple aphid (WAA, Eriosoma lanigerum Hausmann) (Hemiptera: Aphididae), is a major pest of apple trees (Malus domestica, order Rosales) and is critical to the economics of the apple industry in most parts of the world. Here, we generated a chromosome-level genome assembly of WAA - representing the first genome sequence from the aphid subfamily Eriosomatinae - using a combination of 10X Genomics linked-reads and in vivo Hi-C data. The final genome assembly is 327 Mb, with 91% of the assembled sequences anchored into six chromosomes. The contig and scaffold N50 values are 158 kb and 71 Mb, respectively, and we predicted a total of 28,186 protein-coding genes. The assembly is highly complete, including 97% of conserved arthropod single-copy orthologues based on BUSCO analysis. Phylogenomic analysis of WAA and nine previously published aphid genomes, spanning four aphid tribes and three subfamilies, reveals that the tribe Eriosomatini (represented by WAA) is recovered as a sister group to Aphidini + Macrosiphini (subfamily Aphidinae). We identified syntenic blocks of genes between our WAA assembly and the genomes of other aphid species and find that two WAA chromosomes (El5 and El6) map to the conserved Macrosiphini and Aphidini X chromosome. Our high-quality WAA genome assembly and annotation provides a valuable resource for research in a broad range of areas such as comparative and population genomics, insect-plant interactions and pest resistance management.

genomics↗

bioRxiv2020

Chromosome-scale genome assemblies of aphids reveal extensively rearranged autosomes and long-term conservation of the X chromosome

Large-scale chromosome rearrangements are arguably the most dramatic type of mutations, often leading to rapid evolution and speciation. However, chromosome dynamics have only been studied at the sequence level in a small number of model systems. In insects, Diptera (flies and mosquitoes) and Lepidoptera (butterflies and moths) have high levels of chromosome conservation. Whether this truly reflects the diversity of insect genome evolution is questionable given that many species exhibit rapid karyotype evolution. Here, we investigate chromosome evolution in aphids - an important group of hemipteran plant pests - using newly generated chromosome-scale genome assemblies of the green peach aphid (Myzus persicae) and the pea aphid (Acyrthosiphon pisum), and a previously published chromosome-scale assembly of the corn-leaf aphid (Rhopalosiphum maidis). We find that aphid autosomes have undergone dramatic reorganisation over the last 30 million years, to the extent that chromosome homology cannot be determined between aphids from the tribes Macrosiphini (M. persicae and A. pisum) and Aphidini (R. maidis). In contrast, gene content of the aphid sex (X) chromosome remained unchanged despite rapid sequence evolution, low gene expression and high transposable element load. To test whether rapid evolution of genome structure is a hallmark of Hemiptera, we compared our aphid assemblies to chromosome-level assemblies of two blood-feeding Hemiptera (Rhodnius prolixus and Triatoma rubrofasciata). Despite being more diverged, the blood-feeding hemipterans have conserved synteny and we detect only two chromosome fusion or fission events. The exceptional rate of structural evolution of aphid autosomes renders them an important emerging model system for studying the role of large-scale genome rearrangements in evolution.

genomics↗

bioRxiv2020

Widespread targeting of development-related host transcription factors by phytoplasma effectors

Phytoplasmas are pathogenic bacteria that reprogram plant host development for their own benefit. Previous studies have characterized a few different phytoplasma effector proteins that destabilize specific plant transcription factors. However, these are only a small fraction of the potential effectors used by phytoplasmas; therefore, the molecular mechanisms through which phytoplasmas modulate their hosts require further investigation. To obtain further insights into the phytoplasma infection mechanisms, we generated a protein-protein interaction network between a broad set of phytoplasma effectors and a large, unbiased collection of Arabidopsis thaliana transcription factors and transcriptional regulators. We found widespread, but specific, interactions between phytoplasma effectors and host transcription factors, especially those related to host developmental processes. In particular, many unrelated effectors target specific sets of TCP transcription factors, which regulate plant development and immunity. Comparison with other host-pathogen protein interaction networks shows that phytoplasma effectors have unusual targets, indicating that phytoplasmas have evolved a unique and unusual infection strategy. This study contributes a rich and solid data source that guides further investigations of the functions of individual effectors, as demonstrated for some herein. Moreover, the dataset provides insights into the underlying molecular mechanisms of phytoplasma infection.

plant biology↗

bioRxiv2020

Species boundaries and molecular markers for classification among 16SrI phytoplasmas informed by genome analysis

Phytoplasmas are plant-pathogenic bacteria that impact agriculture worldwide. The commonly adopted classification system for phytoplasmas is based on the restriction fragment length polymorphism (RFLP) analysis of their 16S rRNA genes. With the increased availability of phytoplasma genome sequences, the classification system can now be refined. This work examined 11 strains in the 16SrI group within the genus Candidatus Phytoplasma and investigated the possible species boundaries. We confirmed that the RFLP classification method is problematic due to intragenomic variation of the 16S rRNA genes and uneven weighing of different nucleotide positions. Importantly, our results based on the molecular phylogeny, differentiations in chromosomal segments and gene content, and divergence in homologous sequences, all supported that these strains may be classified into multiple operational taxonomic units (OTUs) equivalent to species. Strains assigned to the same OTU share >97% genome-wide average nucleotide identity (ANI) and >78% of their protein-coding genes. In comparison, strains assigned to different OTUs share <94% ANI and <75% of their genes. Reduction in homologous recombination between OTUs is one possible explanation for the discontinuity in genome similarities, and these findings supported the proposal that 95% ANI could serve as a cutoff for distinguishing species in bacteria. Additionally, critical examination of these results and the raw sequencing reads led to the identification of one genome that was presumably mis-assembled by combining two sequencing libraries built from phytoplasmas belonging to different OTUs. This finding provided a cautionary tale for working on uncultivated bacteria. Based on the new understanding of phytoplasma divergence and the current genome availability, we developed five molecular markers that could be used for multilocus sequence analysis (MLSA). By selecting markers that are short yet highly informative, and are distributed evenly across the chromosome, these markers provided a cost-effective system that is robust against recombination. Finally, examination of the effector gene distribution further confirmed the rapid gains and losses of these genes, as well as the involvement of potential mobile units (PMUs) in their molecular evolution. Future improvements on the taxon sampling of phytoplasma genomes will allow further expansions of similar analysis, and thus contribute to phytoplasma taxonomy and diagnostics.

genomics↗

bioRxiv2019

An aphid host-responsive RNA transcript that migrates systemically in plants promotes aphid reproduction

Aphids are sap-feeding insects that colonize a broad range of plant species and often cause feeding damage and transmit plant pathogens, including bacteria, viruses and viroids. These insects feed from the plant vascular tissue, predominantly the phloem. However, it remains largely unknown how aphids, and other sap-feeding insects, establish intimate long-term interactions with plants. To identify aphid virulence factors, we took advantage of the ability of the green peach aphid Myzus persicae to colonize divergent plant species. We found that a M. persicae clone of near-identical females establishes stable colonies on nine plant species of five representative plant eudicot and monocot families that span the angiosperm phylogeny. Members of the novel aphid Ya family are differentially expressed in aphids on the nine plant species, are co-regulated and organized as tandem repeats in aphid genomes. Interestingly, aphids translocate Ya transcripts into plants and some transcripts migrate systemically within several plant species. RNAi-mediated knock down of Ya genes reduces M. persicae fecundity and M. persicae produces more progeny on transgenic plants that heterologously produce one of the systemically migrating Ya transcripts as a long non-coding (lnc)RNA. Taken together, our work led to the discovery of a new host-responsive aphid gene family that operate as virulence factors. Transcripts of this family translocate into plants, including a lncRNA that migrates systemically and promotes aphid reproduction.\n\nSignificance StatementThe green peach aphid Myzus persicae causes yield losses of a diverse range of economically important crops primarily as a vector of more than 100 different plant pathogens. We found that a single genotype of M. persicae is able to colonize nine plant species, including diverse dicots and maize, indicating that this aphid is truly polyphagous. Members of a new aphid Ya family undergoes coordinated expression changes in M. persicae depending on the plant species. The aphids translocate Ya transcripts into plants during feeding and these RNAs migrate to systemic leaves. Moreover, heterologous in planta expression of M. persicae Ya1 as a long non-coding RNA promotes aphid reproduction. Our findings indicate that cross kingdom deployment of RNA is more common than thought.

genomics↗

bioRxiv2019

Phytoplasma SAP11 effector destabilization of TCP transcription factors differentially impact development and defence of Arabidopsis versus maize

Phytoplasmas are insect-transmitted bacterial pathogens that colonize a wide range of plant species, including vegetable and cereal crops, and herbaceous and woody ornamentals. Phytoplasma-infected plants often show dramatic symptoms, including proliferation of shoots (witchs brooms), changes in leaf shapes and production of green sterile flowers (phyllody). Aster Yellows phytoplasma Witches Broom (AY-WB) infects dicots and its effector, secreted AYWB protein 11 (SAP11), was shown to be responsible for the induction of shoot proliferation and leaf shape changes of plants. SAP11 acts by destabilizing TEOSINTE BRANCHED 1-CYCLOIDEA-PROLIFERATING CELL FACTOR (TCP) transcription factors, particularly the class II TCPs of the CYCLOIDEA/TEOSINTE BRANCHED 1 (CYC/TB1) and CINCINNATA (CIN)-TCP clades. SAP11 homologs are also present in phytoplasmas that cause economic yield losses in monocot crops, such as maize, wheat and coconut. Here we show that a SAP11 homolog of Maize Bushy Stunt Phytoplasma (MBSP), which has a range primarily restricted to maize, destabilizes only TB1/CYC TCPs. SAP11MBSP and SAP11AYWB both induce axillary branching and SAP11AYWB also alters leaf development of Arabidopsis thaliana and maize. However, only in maize, SAP11MBSP prevents female inflorescence development, phenocopying maize tb1 lines, whereas SAP11AYWB prevents male inflorescence development and induces feminization of tassels. SAP11AYWB promotes fecundity of the AY-WB leafhopper vector on A. thaliana and modulates the expression of A. thaliana leaf defence response genes that are induced by this leafhopper, in contrast to SAP11MBSP. Neither of the SAP11 effectors promote fecundity of AY-WB and MBSP leafhopper vectors on maize. These data provide evidence that class II TCPs have overlapping but also distinct roles in regulating development and defence in a dicot and a monocot plant species that is likely to shape SAP11 effector evolution depending on the phytoplasma host range.\n\nAuthor summaryPhytoplasmas are parasites of a wide range of plant species and are transmitted by sap-feeding insects, such as leafhoppers. Phytoplasma-infected plants are often easily recognized because of their dramatic symptoms, including shoot proliferations (witchs brooms) and altered leaf shapes, leading to severe economic losses of crops, ornamentals and trees worldwide. We previously found that the virulence protein SAP11 of aster yellows witches broom phytoplasma (AY-WB) interferes with a specific group of plant transcription factors, named TCPs, leading to witches brooms and leaf shape changes of the model plant Arabidopsis thaliana. SAP11 has been characterized in a number of other phytoplasmas. However, it is not known how phytoplasmas and their SAP11 proteins modulate processes in crops, including cereals such as maize. We identified a SAP11 homolog in Maize bushy stunt phytoplasma (MBSP), a pathogen that can cause severe yield losses of maize. We found that SAP11 interactions with TCPs are conserved between maize and Arabidopsis, and that MBSP SAP11 interferes with less TCPs compared to AY-WB SAP11. This work provides new insights into how phytoplasmas change maize architecture and corn production. Moreover, we found that TCPs regulate leaf defence responses to phytoplasma leafhopper vectors in Arabidopsis, but not in maize.

evolutionary biology↗

bioRxiv2018

Sex-specific changes in the aphid DNA methylation landscape

Aphids present an ideal system to study epigenetics as they can produce diverse, but genetically identical, morphs in response to environmental stimuli. Here, using whole genome bisulphite sequencing and transcriptome sequencing of the green peach aphid (Myzus persicae), we present the first detailed analysis of cytosine methylation in an aphid and investigate differences in the methylation and transcriptional landscapes of male and asexual female morphs. We find that methylation primarily occurs in a CG dinucleotide (CpG) context and that exons are highly enriched for methylated CpGs, particularly at the 3 end of genes. Methylation is positively associated with gene expression, and methylated genes are more stably expressed than un-methylated genes. Male and asexual female morphs have distinct methylation profiles. Strikingly, these profiles are divergent between the sex chromosome and the autosomes; autosomal genes are hypo-methylated in males compared to asexual females, whereas genes belonging to the sex chromosome, which is haploid in males, are hyper-methylated. Overall, we find correlated changes in methylation and gene expression between males and asexual females, and this correlation is particularly strong for genes located on the sex chromosome. Our results suggest that differential methylation of sex-biased genes plays a role in M. persicae sexual differentiation.

genomics↗

bioRxiv2017

Chemosensory proteins in the CSP4 clade evolved as plant immunity suppressors before two suborders of plant-feeding hemipteran insects diverged

Chemosensory proteins (CSPs) are small globular proteins with hydrophobic binding pockets that have a role in detection of chemicals, regulation of development and growth and host seeking behaviour and feeding of arthropods. Here, we show that a CSP has evolved to modulate plant immune responses. Firstly, we found that the green peach aphid Myzus persicae CSP Mp10, which is delivered into the cytoplasm of plant cells, suppresses the reactive oxygen species (ROS) bursts to both aphid and bacterial elicitors in Arabidopsis thaliana and Nicotiana benthamiana. Aphid RNA interference studies demonstrated that Mp10 modulates the first layer of the plant defence response, specifically the BAK1 pathway. We identified Mp10 homologs in diverse plant-sucking insect species, including aphids, whiteflies, psyllids and leafhoppers, but not in other insect species, including blood-feeding hemipteran insects. We found that Mp10 homologs from other splant-sucking insect species are also capable of suppressing plant ROS. Together, these data and phylogenetic analyses provides evidence that an ancestral Mp10-like sequence acquired plant ROS suppression activity before the divergence of plant-sucking insect species over 250 million years ago.\n\nSignificanceAphids, whiteflies, psyllids, leafhoppers and planthoppers are plant-sucking insects of the order Hemiptera that cause dramatic crop losses via direct feeding damage and vectoring of plant pathogens. Chemosensory proteins (CSPs) regulate behavioural and developmental processes in arthropods. Here we show that the CSP Mp10 of the green peach aphid Myzus persicae is an effector that suppresses plant reactive oxygen species (ROS) bursts and the first layer of plant defence responses. Surprisingly, Mp10 homologs are present in diverse plant-feeding hemipteran species, but not blood-feeding ones. An ancestral Mp10-like sequence most likely acquired ROS suppression activity before the divergence of plant-sucking insect species 250 million years ago.

evolutionary biology↗