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The structural and ultrastructural characteristics of galls induced by three species of insects parasitizing on oak leaves (Quercus robur L.) were examined utilizing light and fluorescent microscopes, as well as scanning and transmission electron microscopes. The tissues of the investigated galls exhibited marked differences from those of a typical oak leaf. In the Cynips quercusfolii L. gall, the larval chamber in its final stage was formed from the remnants of dead cells that remained after larval feeding on the gall nutritive tissue. The cells of the gall nutritive tissue and the cells of the gall parenchyma exhibited diametrical differences: the former contained dense cytoplasm and had large nuclei and nucleoli, whereas the latter displayed sparse cytoplasm, prominent vacuoles, and very small nuclei. The region of coalescence between the gall stalk and leaf tissues has been described. In Neuroterus numismalis Geoffroy gall, the early developmental phases have been described in detail. The external gall tissues resembled periderm, whereas periderm does not normally occur in leaves. In the cytoplasm of Cynips longiventris Hartig gall, different bodies were found, including organized smooth endoplasmic reticulum; however, not all of the observed structures were definitively classified.

Anatomy and surface ultrastructure of the galls induced on oak leaves by the insects – Neuroterus numismalis (Ol.) and Cynips (Diplolepis) quercusfolii L. – were investigated using a scanning electron microscope (SEM) and a light microscope (LM). The observations in SEM and in LM enabled a detailed description of these galls and comparison of their structure with that of the typical oak leaf. In N. numismalis gall, the external distal tissues were classified as similar to phellem (cork), phellogen, and phelloderm, and a lateral marginal tissue as parenchyma with the likely role of a storage tissue. In the young C. quercusfolii gall, the cells of internal, nutritive tissue, on which the larva is grazing, formed globules rising above the surface of larval chamber. Many of them seemed to be destroyed by the larval action. In the gall which attained half of its final size, the tissues near the larval chamber were already partly lignified. The microorganisms (mainly fungi) which live in the oak phyllosphere, occurred also on the galls. We believe that the deep changes in the morphogenetic program of a leaf, which are caused by the gall-forming insects, are impossible without the transfer and the integration of the insect genetic material with that of the host plant. We also postulate that a larva secrets as yet hypothetical substances, which redirect the nutrients transport from the leaf blade towards the gall and support its vital functions.

A variety of insect species induce galls on host plants. Several studies have implicated phytohormones in insect-induced gall formation. However, it has not been determined whether insects can synthesize phytohormones. It has also never been established that phytohormones function in gall tissues. Liquid chromatography and tandem mass spectrometry (LC/MS/MS) were used to analyse concentrations of endogenous cytokinins and the active auxin IAA in the gall-inducing sawfly (Pontania sp.) and its host plant, Salix japonica. Feeding experiments demonstrated the ability of sawfly larvae to synthesize IAA from tryptophan. Gene expression analysis was used to characterize hormonal signalling in galls. Sawfly larvae contain high concentrations of IAA and t-zeatin, and produce IAA from tryptophan. The glands of adult sawflies, the contents of which are injected into leaves upon oviposition and are involved in the initial stages of gall formation, contain an extraordinarily high concentration of t-zeatin riboside. Transcript levels of some auxin-and cytokinin-responsive genes are significantly higher in gall tissue than in leaves. The abnormally high concentration of t-zeatin riboside in the glands strongly suggests that the sawfly can synthesize cytokinins as well as IAA. Gene expression profiles indicate high levels of auxin and cytokinin activities in growing galls.

Complex defense signaling pathways, controlled by different hormones, are involved in the reaction of plants to a wide range of biotic and abiotic stress factors. We studied the ability of salicylic acid, jasmonate (JA), and ethylene (ET) to induce systemic defense in rice (Oryza sativa) against the root knot nematode Meloidogyne graminicola. Exogenous ET (ethephon) and JA (methy1 jasmonate) supply on the shoots induced a strong systemic defense response in the roots, exemplified by a major up-regulation of pathogenesis-related genes OsPR1a and OsPR1b, while the salicylic acid analog BTH (benzo-1,2,3-thiadiazole-7-carbothioic acid S-methy1 ester) was a less potent systemic defense inducer from shoot to root. Experiments with JA biosynthesis mutants and ET-insensitive transgenics showed that ET-induced defense requires an intact JA pathway, while JA-induced defense was still functional when ET signaling was impaired. Pharmacological inhibition of JA and ET biosynthesis confirmed that JA biosynthesis is needed for ET-induced systemic defense, and quantitative real-time reverse transcription-polymerase chain reaction data revealed that ET application onto the shoots strongly activates JA biosynthesis and signaling genes in the roots. All data provided in this study point to the JA pathway to play a pivotal role in rice defense against root knot nematodes. The expression of defense-related genes was monitored in root galls caused by M. graminicola. Different analyzed defense genes were attenuated in root galls caused by the nematode at early time points after infection. However, when the exogenous defense inducers ethephon and methy1 jasmonate were supplied to the plant, the nematode was less effective in counteracting root defense pathways, hence making the plant more resistant to nematode infection.

With about 2000 different galls (implies that almost the same number of inducing-insect species exists), the Indian subcontinent displays a rich variety in gall flora. Gallinducing insects of peninsular India are endemic, whereas those in the temperate Himalayan slopes and in the Indo-Gangetic plains show affinity to Central Asian and European gall-inducing elements. Fossil records indicate that galls existed in India from the late Cenozoic period. Throughout the Indian subcontinent, species richness in gall midges (Diptera: Cecidomyiidae) is almost uniform, inducing different types of galls, including the incredible 'cylinder–piston' gall, which, however, has been recorded only in the natural areas around Coimbatore. In the light of the global pattern, cecidomyiid-induced galls should be the major component in Indian gall flora, although much needs to be known about the identities of midges and the nature of galls they induce. Gall-inducing cynipids (Hymenoptera: Cynipidae) and aphids (Hemiptera: Aphididae) are restricted to the Himalayan slopes, whereas gallinducing thrips (Thysanoptera) are confined to peninsular India. Against such a confusing but interesting distributional pattern, this review brings into focus several biological, ecological, and evolutionary questions that remain unanswered in the background of what a gall is, how galls are initiated and what factors trigger gall growth, what designs are evident among gallinducing insects in terms of host dependence, and biogeographical patterns in the distribution of gall-susceptible plants vis-à-vis gall-inducing insects, referring specifically to the gall flora of the Indian subcontinent.

Galls have become the best model for exploring plant–gall inducer relationships, with most studies focusing on gall-inducing insects but few on gall mites. The gall mite Aceria pallida is a major pest of wolfberry, usually inducing galls on its leaves. For a better understanding of gall mite growth and development, the dynamics of the morphological and molecular characteristics and phytohormones of galls induced by A. pallida were studied by histological observation, transcriptomics and metabolomics. The galls developed from cell elongation of the epidermis and cell hyperplasia of mesophylls. The galls grew quickly, within 9 days, and the mite population increased rapidly within 18 days. The genes involved in chlorophyll biosynthesis, photosynthesis and phytohormone synthesis were significantly downregulated in galled tissues, but the genes associated with mitochondrial energy metabolism, transmembrane transport, carbohydrates and amino acid synthesis were distinctly upregulated. The levels of carbohydrates, amino acids and their derivatives, and indole-3-acetic acid (IAA) and cytokinins (CKs), were markedly enhanced in galled tissues. Interestingly, much higher contents of IAA and CKs were detected in gall mites than in plant tissues. These results suggest that galls act as nutrient sinks and favor increased accumulation of nutrients for mites, and that gall mites may contribute IAA and CKs during gall formation.

Background The induction of alcohol fermentation in roots is a plant adaptive response to flooding stress and oxygen deprivation. Available transcriptomic data suggest that fermentation-related genes are also frequently induced in roots infected with gall forming pathogens, but the biological significance of this induction is unclear. In this study, we addressed the role of hypoxia responses in Arabidopsis roots during infection by the clubroot agent Plasmodiophora brassicae . Results The hypoxia-related gene markers PYRUVATE DECARBOXYLASE 1 ( PDC1) , PYRUVATE DECARBOXYLASE 2 ( PDC2) and ALCOHOL DEHYDROGENASE 1 ( ADH1) were induced during secondary infection by two isolates of P. brassicae , eH and e2. PDC2 was highly induced as soon as 7 days post inoculation (dpi), i.e., before the development of gall symptoms, and GUS staining revealed that ADH1 induction was localised in infected cortical cells of root galls at 21 dpi. Clubroot symptoms were significantly milder in the pdc1 and pdc2 mutants compared with Col-0, but a null T-DNA insertional mutation of ADH1 did not affect clubroot susceptibility. The Arg/N-end rule pathway of ubiquitin-mediated proteolysis controls oxygen sensing in plants. Mutants of components of this pathway, ate1 ate2 and prt6 , that both exhibit constitutive hypoxia responses, showed enhanced clubroot symptoms. In contrast, gall development was reduced in quintuple and sextuple mutants where the activity of all oxygen-sensing Group VII Ethylene Response Factor transcription factors (ERFVIIs) is absent ( erfVII and prt6 erfVII ). Conclusions Our data demonstrate that the induction of PDC1 and PDC2 during the secondary infection of roots by P. brassicae contributes positively to clubroot development, and that this is controlled by oxygen-sensing through ERFVIIs. The absence of any major role of ADH1 in symptom development may also suggest that PDC activity could contribute to the formation of galls through the activation of a PDH bypass.

Biological invasions are a major threat to biodiversity and as such understanding their impacts is a research priority. Ecological networks provide a valuable tool to explore such impacts at the community level, and can be particularly insightful for planning and monitoring biocontrol programmes, including the potential for their seldom evaluated indirect non-target effects. Acacia longifolia is among the worst invasive species in Portugal, and has been recently targeted for biocontrol by a highly specific gall-wasp. Here we use an ambitious replicated network approach to: (1) identify the mechanisms by which direct and indirect impacts of A. longifolia can cascade from plants to higher trophic levels, including gallers, their parasitoids and inquilines; (2) reveal the structure of the interaction networks between plants, gallers, parasitoids and inquilines before the biocontrol; and (3) explore the potential for indirect interactions among gallers, including those established with the biocontrol agent, via apparent competition. Over a 15-month period, we collected 31,737 galls from native plants and identified all emerging insects, quantifying the interactions between 219 plant-, 49 galler-, 65 parasitoid- and 87 inquiline-species—one of the largest ecological networks to date. No galls were found on any of the 16 alien plant species. Invasion by A. longifolia caused an alarming simplification of plant communities, with cascading effects to higher trophic levels, namely: a decline of overall gall biomass, and on the richness, abundance and biomass of galler insects, their parasitoids, and inquilines. Correspondingly, we detected a significant decline in the richness of interactions between plants and galls. The invasion tended to increase overall interaction evenness by promoting the local extinction of the native plants that sustained more gall species. However, highly idiosyncratic responses hindered the detection of further consistent changes in network topology. Predictions of indirect effects of the biocontrol on native gallers via apparent competition ranged from negligible to highly significant. Such scenarios are incredibly hard to predict, but even if there are risks of indirect effects it is critical to weigh them carefully against the consequences of inaction and invasive species spread.

Endoparasitism by gall-forming insects dramatically alters the plant phenotype by altering growth patterns and modifying plant organs in ways that appear to directly benefit the gall former. Because these morphological and physiological changes are linked to the presence of the insect, the induced phenotype is said to function as an extension of the parasite, albeit by unknown mechanisms. Here we report the gall-forming aphid-like parasite phylloxera, Daktulosphaira vitifoliae, induces stomata on the adaxial surface of grape leaves where stomata typically do not occur. We characterized the function of the phylloxera-induced stomata by tracing transport of assimilated carbon. Because induction of stomata suggests a significant manipulation of primary metabolism, we also characterized the gall transcriptome to infer the level of global reconfiguration of primary metabolism and the subsequent changes in downstream secondary metabolism. Phylloxera feeding induced stomata formation in proximity to the insect and promoted the assimilation and importation of carbon into the gall. Gene expression related to water, nutrient, and mineral transport; glycolysis; and fermentation increased in leaf-gall tissues. This shift from an autotrophic to a heterotrophic profile occurred concurrently with decreased gene expression for nonmevalonate and terpenoid synthesis and increased gene expression in shikimate and phenylpropanoid biosynthesis, secondary metabolite systems that alter defense status in grapes. These functional insect-induced stomata thus comprise part of an extended phenotype, whereby D. vitifoliae globally reprograms grape leaf development to alter patterns of primary metabolism, nutrient mobilization, and defense investment in favor of the galling habit.

Plant endoparasitic nematodes induce the formation of their feeding cells by injecting effectors from the esophageal glands into root cells. Although vascular cylinder cells seem to be involved in the formation of root-knot nematode (RKN) feeding structures, molecular evidence is scarce. We address the role during gall development of LATERAL ORGAN BOUNDARIES-DOMAIN 16 (LBD16), a key component of the auxin pathway leading to the divisions in the xylem pole pericycle (XPP) for lateral root (LR) formation. Arabidopsis T-DNA tagged J0192 and J0121 XPP marker lines, LBD16 and DR5::GUS promoter lines, and isolated J0192 protoplasts were assayed for nematode-dependent gene expression. Infection tests in LBD16 knock-out lines were used for functional analysis. J0192 and J0121 lines were activated in early developing galls and giant cells (GCs), resembling the pattern of the G2/M-transition specific ProCycB1;1:CycB1;1(NT)-GUS line. LBD16 was regulated by auxins in galls as in LRs, and induced by RKN secretions. LBD16 loss of function mutants and a transgenic line with defective XPP cells showed a significantly reduced infection rate. The results show that genes expressed in the dividing XPP, particularly LBD16, are important for gall formation, as they are for LR development.