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We explored the genome of the Wolbachia strain, wEsol, symbiotic with the plant-gall-inducing fly Eurosta solidaginis with the goal of determining if wEsol contributes to gall induction by its insect host. Gall induction by insects has been hypothesized to involve the secretion of the phytohormones cytokinin and auxin and/or proteinaceous effectors to stimulate cell division and growth in the host plant. We sequenced the metagenome of E. solidaginis and wEsol and assembled and annotated the genome of wEsol. The wEsol genome has an assembled length of 1.66 Mbp and contains 1878 protein-coding genes. The wEsol genome is replete with proteins encoded by mobile genetic elements and shows evidence of seven different prophages. We also detected evidence of multiple small insertions of wEsol genes into the genome of the host insect. Our characterization of the genome of wEsol indicates that it is compromised in the synthesis of dimethylallyl pyrophosphate (DMAPP) and S-adenosyl L-methionine (SAM), which are precursors required for the synthesis of cytokinins and methylthiolated cytokinins. wEsol is also incapable of synthesizing tryptophan, and its genome contains no enzymes in any of the known pathways for the synthesis of indole-3-acetic acid (IAA) from tryptophan. wEsol must steal DMAPP and L-methionine from its host and therefore is unlikely to provide cytokinin and auxin to its insect host for use in gall induction. Furthermore, in spite of its large repertoire of predicted Type IV secreted effector proteins, these effectors are more likely to contribute to the acquisition of nutrients and the manipulation of the host's cellular environment to contribute to growth and reproduction of wEsol than to aid E. solidaginis in manipulating its host plant. Combined with earlier work that shows that wEsol is absent from the salivary glands of E. solidaginis, our results suggest that wEsol does not contribute to gall induction by its host.
Assuntos
Tephritidae , Wolbachia , Animais , Wolbachia/genética , Triptofano , Tephritidae/metabolismo , Insetos/metabolismo , Ácidos Indolacéticos/metabolismo , Citocininas , GenômicaRESUMO
Gut bacteria play a crucial role in the several metabolic activity of the insects. In the present work, effort has been made to decipher the gut microbiota associated with the developmental stages of Gynaikothrips uzeli a gall inducing thrips along with their predicted functional role. Further, an effort has been made to correlate the bacterial communities with plant pathogenesis and thelytoky behaviour of G. uzeli. Findings obtained revealed that genus Arsenophonus dominated the total bacterial diversity and was transmitted vertically through the developmental stages. Further, it was observed that the high abundance of genus Arsenophonus promotes the thelytoky behaviour in G. uzeli and results in the killing of males. Furthermore, strong connecting link between Arsenophonus abundance and gall induction in F. benjamina was observed in the current dataset. G. uzeli being in the category of phloem sucking insect was known for the induction of galls and the current findings for the first time unveiled the facts that high abundance of genus Arsenophonus a well-known plant pathogen may be one of the major reason for inducing galls in F. benjamina. Moreover, PICRUSt2 analysis revealed that predicted functional pathways like biosynthesis of amino acids, and metabolism of carbon, nitrogen, carbohydrates and amino acids (e.g. Arginine, Alanine, Aspartate, Glutamate, Proline, Cysteine, Methionine, Glycine, Threonine, and Serine) were frequently noticed in profiles associated with all the developmental stages of G. uzeli. More to this, the high abundance of Arsenophonus in G. uzeli suggest that representatives of this genus may be resistant and/or tolerant to different antibacterial agents, alkaloids, flavonoids, and glycosides (e.g. quercetin). The correlation of bacterial diversity in pathogenicity can be extrapolated in different pest and vector species of other arthropods.
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The phytohormone production hypothesis suggests that organisms, including insects, induce galls by producing and secreting plant growth hormones. Auxins and cytokinins are classes of phytohormones that induce cell growth and cell division, which could contribute to the plant tissue proliferation which constitutes the covering gall. Bacteria, symbiotic with insects, may also play a part in gall induction by insects through the synthesis of phytohormones or other effectors. Past studies have shown that concentrations of cytokinins and auxins in gall-inducing insects are higher than in their host plants. However, these analyses have involved whole-body extractions. Using immunolocalization of cytokinin and auxin, in the gall inducing stage of Eurosta solidaginis, we found both phytohormones to localize almost exclusively to the salivary glands. Co-localization of phytohormone label with a nucleic acid stain in the salivary glands revealed the absence of Wolbachia sp., the bacterial symbiont of E. solidaginis, which suggests that phytohormone production is symbiont independent. Our findings are consistent with the hypothesis that phytohormones are synthesized in and secreted from the salivary glands of E. solidaginis into host-plant tissues for the purpose of manipulating the host plant.
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While free-living herbivorous insects are thought to harbor microbial communities composed of transient bacteria derived from their diet, recent studies indicate that insects that induce galls on plants may be involved in more intimate host-microbe relationships. We used 16S rDNA metabarcoding to survey larval microbiomes of 20 nematine sawfly species that induce bud or leaf galls on 13 Salix species. The 391 amplicon sequence variants (ASVs) detected represented 69 bacterial genera in six phyla. Multi-variate statistical analyses showed that the structure of larval microbiomes is influenced by willow host species as well as by gall type. Nevertheless, a "core" microbiome composed of 58 ASVs is shared widely across the focal galler species. Within the core community, the presence of many abundant, related ASVs representing multiple distantly related bacterial taxa is reflected as a statistically significant effect of bacterial phylogeny on galler-microbe associations. Members of the core community have a variety of inferred functions, including degradation of phenolic compounds, nutrient supplementation, and production of plant hormones. Hence, our results support suggestions of intimate and diverse interactions between galling insects and microbes and add to a growing body of evidence that microbes may play a role in the induction of insect galls on plants.
Assuntos
Bactérias/classificação , Bactérias/genética , Microbiota/genética , Microbiota/fisiologia , Filogenia , Salix/microbiologia , Animais , Biodiversidade , Interações entre Hospedeiro e Microrganismos , Especificidade de Hospedeiro , Insetos , Larva , Reguladores de Crescimento de Plantas , Folhas de Planta , RNA Ribossômico 16S/genéticaRESUMO
Gall wasps (Hymenoptera: Cynipidae) induce complex galls on oaks, roses, and other plants, but the mechanism of gall induction is still unknown. Here, we take a comparative genomic approach to revealing the genetic basis of gall induction. We focus on Synergus itoensis, a species that induces galls inside oak acorns. Previous studies suggested that this species evolved the ability to initiate gall formation recently, as it is deeply nested within the genus Synergus, whose members are mostly inquilines that develop inside the galls of other species. We compared the genome of S. itoensis with that of three related Synergus inquilines to identify genomic changes associated with the origin of gall induction. We used a novel Bayesian selection analysis, which accounts for branch-specific and gene-specific selection effects, to search for signatures of selection in 7,600 single-copy orthologous genes shared by the four Synergus species. We found that the terminal branch leading to S. itoensis had more genes with a significantly elevated dN/dS ratio (positive signature genes) than the other terminal branches in the tree; the S. itoensis branch also had more genes with a significantly decreased dN/dS ratio. Gene set enrichment analysis showed that the positive signature gene set of S. itoensis, unlike those of the inquiline species, is enriched in several biological process Gene Ontology terms, the most prominent of which is "Ovarian Follicle Cell Development." Our results indicate that the origin of gall induction is associated with distinct genomic changes, and provide a good starting point for further characterization of the genes involved.
Assuntos
Evolução Biológica , Genoma de Inseto , Tumores de Planta/parasitologia , Seleção Genética , Vespas/fisiologia , Animais , Duplicação Gênica , Modelos Genéticos , Quercus/parasitologiaRESUMO
To gain insight into wasp factors that might be involved in the initial induction of galls on woody plants, we performed high throughput (454) transcriptome analysis of ovaries and venom glands of two cynipid gall wasps, Biorhiza pallida and Diplolepis rosae, inducing galls on oak and rose, respectively. De novo assembled and annotated contigs were compared to sequences from phylogenetically related parasitoid wasps. The relative expression levels of contigs were estimated to identify the most expressed gene sequences in each tissue. We identify for the first time a set of maternally expressed gall wasp proteins potentially involved in the interaction with the plant. Some genes highly expressed in venom glands and ovaries may act to suppress early plant defense signaling. We also identify gall wasp cellulases that could be involved in observed local lysis of plant tissue following oviposition, and which may have been acquired from bacteria by horizontal gene transfer. We find no evidence of virus-related gene expression, in contrast to many non-cynipid parasitoid wasps. By exploring gall wasp effectors, this study is a first step toward understanding the molecular mechanisms underlying cynipid gall induction in woody plants, and the recent sequencing of oak and rose genomes will enable study of plant responses to these factors.
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Gall-inducing insects are capable of exerting a high level of control over their hosts' cellular machinery to the extent that the plant's development, metabolism, chemistry, and physiology are all altered in favour of the insect. Many gallers are devastating pests in global agriculture and the limited understanding of their relationship with their hosts prevents the development of robust management strategies. Omics technologies are proving to be important tools in elucidating the mechanisms involved in the interaction as they facilitate analysis of plant hosts and insect effectors for which little or no prior knowledge exists. In this review, we examine the mechanisms behind insect gall development using evidence from omics-level approaches. The secretion of effector proteins and induced phytohormonal imbalances are highlighted as likely mechanisms involved in gall development. However, understanding how these components function within the system is far from complete and a number of questions need to be answered before this information can be used in the development of strategies to engineer or breed plants with enhanced resistance.
Assuntos
Interações Hospedeiro-Parasita , Insetos/fisiologia , Tumores de Planta/parasitologia , Plantas/parasitologia , Animais , Perfilação da Expressão Gênica , Genômica , Metabolômica , Plantas/genética , Plantas/metabolismo , Proteômica , Biologia de SistemasRESUMO
Biologists who study insect-induced plant galls are faced with the overwhelming diversity of plant forms and insect species. A challenge is to find common themes amidst this diversity. We discuss common themes that have emerged from our cytological and histochemical studies of diverse neotropical insect-induced galls. Gall initiation begins with recognition of reactive plant tissues by gall inducers, with subsequent feeding and/or oviposition triggering a cascade of events. Besides, to induce the gall structure insects have to synchronize their life cycle with plant host phenology. We predict that reactive oxygen species (ROS) play a role in gall induction, development and histochemical gradient formation. Controlled levels of ROS mediate the accumulation of (poly)phenols, and phytohormones (such as auxin) at gall sites, which contributes to the new cell developmental pathways and biochemical alterations that lead to gall formation. The classical idea of an insect-induced gall is a chamber lined with a nutritive tissue that is occupied by an insect that directly harvests nutrients from nutritive cells via its mouthparts, which function mechanically and/or as a delivery system for salivary secretions. By studying diverse gall-inducing insects we have discovered that insects with needle-like sucking mouthparts may also induce a nutritive tissue, whose nutrients are indirectly harvested as the gall-inducing insects feeds on adjacent vascular tissues. Activity of carbohydrate-related enzymes across diverse galls corroborates this hypothesis. Our research points to the importance of cytological and histochemical studies for elucidating mechanisms of induced susceptibility and induced resistance.
Assuntos
Insetos/fisiologia , Células Vegetais/parasitologia , Tumores de Planta/parasitologia , Plantas/parasitologia , Adaptação Fisiológica , Animais , Interações Hospedeiro-Parasita , Reguladores de Crescimento de Plantas/fisiologiaRESUMO
The maize orange leafhopper, Cicadulina bipunctata, is a multivoltine insect that induces galls on various plants of the Poaceae. A previous study revealed that galls produced by this leafhopper were induced by dose-dependent stimulation on distant leaves from the feeding site, probably by chemical(s) injected from adults during feeding. In this paper, we examined the gall-inducing ability of C. bipunctata nymphs. The degree of gall induction gradually increased depending on the number of feeding nymphs and there were no significant differences from the positive control (feeding by five male adults) when seedlings were exposed to five or more nymphs. These results indicate that both adults and nymphs of C. bipunctata have the ability to induce galls on their host plants, a unique feature among gallinducing insects. This feature may be related to the free-living, multivoltine and polyphagous habits of C. bipunctata.
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The influence of temperature, shoot age, and medium on gall induction by Subanguina picridis on Russian knapweed (Acroptilon repens) was examined in vitro. The optimal temperature for gall formation was 20 C. Gall induction was delayed as the temperature decreased, and decreased as shoot age increased. Bud primordia (0-day-old shoots and 5-day-old shoots) with an average length of 4.2 mm and 7.9 mm were the most suitable tissues for nematode development and gall formation. Gall formation was more effective on B5G medium than on MSG. Young shoots under slow growth were most suitable for mass rearing of S. picridis.