Gall-inducing Insects Research Articles

Integrated insights into the cytological, histochemical, and cell wall composition features of Espinosa nothofagi (Hymenoptera) gall tissues: implications for functionality.

Many insect-induced galls are considered complex structures due to their tissue compartmentalization and multiple roles performed by them. The current study investigates the complex interaction between Nothofagus obliqua host plant and the hymenopteran gall-inducer Espinosa nothofagi, focusing on cell wall properties and cytological features. The E. nothofagi galls present an inner cortex with nutritive and storage tissues, as well as outer cortex with epidermis, chlorenchyma, and water-storing parenchyma. The water-storing parenchyma cells are rich in pectins, heteromannans, and xyloglucans in their walls, and have large vacuoles. Homogalacturonans contribute to water retention, and periplasmic spaces function as additional water reservoirs. Nutritive storage cell walls support nutrient storage, with plasmodesmata facilitating nutrient mobilization crucial for larval nutrition. Their primary and sometimes thick secondary cell walls support structural integrity and act as a carbon reserve. The absent labeling of non-cellulosic epitopes indicates a predominantly cellulosic nature in nutritive cell walls, facilitating larval access to lipid, protein, and reducing sugar-rich contents. The nutritive tissue, with functional chloroplasts and high metabolism-related organelles, displays signs of self-sufficiency, emphasizing its role in larval nutrition and cellular maintenance. Overall, the intricate cell wall composition in E. nothofagi galls showcases adaptations for water storage, nutrient mobilization, and larval nutrition, contributing significantly to our understanding of plant-insect interactions.

Study of Altenia wagneriella (rebel) as a predator associated with Forda marginata from Iran.

The larvae of Altenia spp. and gall aphids are known to feed on plants related to Anacardiaceae. This study documents the aphidophagous habit of Altenia wagneriella, which was verified by molecular techniques, subsequently by the gut dissection test, and direct observation. To identify the moth larvae and adult aphids, two mitochondrial genes, cytochrome c oxidase I (COI) and cytochrome b (Cytb), were amplified by polymerase chain reaction (PCR). Nested PCR with the aphid-specific primer pairs AphidF and AphidR was used to detect aphids in the body of moth larvae. The specificity of the primers was verified by PCR analysis of DNA from moth larvae and adult aphids. The method detected aphids in moth larvae, and a band of approximately 200bp was amplified from moth larvae feeding on aphids. No cross reactions with moth larvae were observed. In the laboratory, all moth larvae feeding on aphids (Forda marginata) were also PCR positive for aphids. Gall-inducing insects are microhabitat engineers that manipulate their host to obtain a better nutrient supply, as well as protection from natural enemies and abiotic factors. This is the first recorded instance worldwide of the carnivorous larva of the moth A. wagneriella acting as an aphid predator, as well as the first record of a host insect for this species. Additionally, it is the first effort to molecularly analyze the predator-prey relationship between the moth larvae and the aphids inside the wild pistachio gall.

Chiral Chemopolymorphism in the Monoterpenes of Pistacia palaestina Leaves and Galls.

Pistacia palaestina Boiss. is a common tree in the Mediterranean maquis. The leaves of this plant accumulate defensive monoterpenes, whose levels greatly increase in galls induced by the aphid Baizongia pistaciae. We previously found a significant chemopolymorphism in monoterpene content among individual trees, but the chirality of these monoterpenes was unknown. Although most plant species specifically accumulate one enantiomeric form of a given compound, P. palaestina individuals display chemopolymorphism in the chirality of the key monoterpenes accumulated. We report here a marked enantiomeric variation for the limonene, α- and β-pinene, camphene, sabinene, δ-3-carene, and terpene-4-ol content in leaves and galls of nine different naturally growing P. palaestina trees. Interestingly, insect-induced gall monoterpene composition is an augmentation of the specific enantiopolymorphism originally displayed by each individual tree.

Who are the superhosts of gall-inducing insects? The need for a conceptual definition

Who are the superhosts of gall-inducing insects? The need for a conceptual definition

Tolerance Mitigates Gall Effects When Susceptible Plants Fail to Elicit Induced Defense.

Variations in plant genotypes and phenotypes are expressed in ways that lead to the development of defensive abilities against herbivory. Induced defenses are mechanisms that affect herbivore insect preferences and performance. We evaluated the performance of resistant and susceptible phenotypes of Bauhinia brevipes (Fabaceae) against attacks by the gall-inducing insect Schizomyia macrocapillata (Diptera). We hypothesized that there is a positive relationship between resistance to S. macrocapillata and host plant performance because resistance can have a high adaptive value. We evaluated plant architecture, nutritional leaf quality, leaf fluctuating asymmetry, and reproductive capacity between phenotypes. Plant performance was evaluated at three ontogenetic stages: seed, seedling, and juvenile. Overall, there were no differences in vegetative and reproductive performance or asymmetry between the resistant and susceptible mature plants. We found no relationship between leaf nutritional quality and resistance to S. macrocapillata. Plant performance was consistent across ontogeny for both phenotypes, except for five variables. Contrary to our expectations, the susceptible plants performed equally well or better than the resistant plants, suggesting that tolerance and overcompensation to herbivory in B. brevipes may be mediated by induced defense. Our study highlights the importance of multiple layers of plant defense against herbivory, where plant tolerance acts as a secondary barrier in plants susceptible to gall-inducing insects.

Rich specialized insect damage on Pliocene leaves from the Mahuadanr Valley (India) growing under a warm climate with weak seasonality.

Plant-insect interactions play a crucial role in shaping terrestrial ecosystems, influencing abundance and distribution of plant species. In the present study, we investigated leaf-mining patterns on fossil leaves from Pliocene strata of the Mahuadanr Valley, Jharkhand, eastern India, deposited under a seasonal tropical climate, and reported complex interactions between plants and insects. We identified 11 distinct mining morphotypes. These morphotypes were mainly found on Dipterocarpaceae, Fabaceae, Lauraceae, and Moraceae; similar mining traces were also observed in the contemporary vegetation surrounding the fossil site. Although mining richness was relatively high, only 2.6% of all leaves in the fossil assemblage were mined. We compared mining richness and abundance values with previously reported values for galling. While richness was slightly lower for galling, almost 50% of all fossil leaves were galled. A literature survey on mining and galling patterns in modern vegetation suggests that there is no global explanation for richness of mining or gall-inducing insects. Thus, low nutrient availability in the ancient forest, dominance of semideciduous leaves with hard texture, and different habitats in the same forest ecosystem, such as well-drained forests and riparian stands, may all have favored different types of specialized plant-insect interactions.

Insect galls of the Chapada Diamantina, Rio de Contas, Bahia, Brazil

We surveyed insect galls and their host plants in areas of Caatinga and Cerrado in the municipality of Rio de Contas, in the extreme south of the Chapada Diamantina (Bahia state), between 703 and 1,897 m altitude, in order to contribute to the knowledge and conservation of local biodiversity. The survey was conducted in eight locations, adopting the random walking methodology for sampling, four in Caatinga and four in Cerrado, covering distinct phytophysiognomies (cerrado sensu stricto, gallery forest, shrubby caatinga, riparian forest, and rocky field). Eighty-four different insect gall morphotypes were reported, 48 (57.14%) of them on 42 host species in Cerrado and 36 (42.86%) on 24 host species in Caatinga. Most galls occurred on leaves (48.72%) and were globoid (53.76%), glabrous (52.92%), isolated (55.44%), usually one-chambered (61.32%), and brown (25.2%). The gall-inducing insects identified belonged to Lepidoptera (n = 1), Thysanoptera (n = 1), Hemiptera (n = 2), and Diptera (Cecidomyiidae) (n = 16). This was the first inventory of galls in the Chapada Diamantina, so all records are new for the region. We also recorded the first occurrences of galls on two Cerrado plant species and on two in the Caatinga. We found a significant positive correlation between gall richness and plant species richness, suggesting that radiation of gall-inducing insects may be associated with plant species richness.

Diversity of insect galls in veredas of the Brazilian Cerrado in Minas Gerais, Brazil

Brazilian veredas are hygrophilous communities with high species diversity, featuring many floristic studies but a still incipient number of faunistic studies. In the present study, we conducted an inventory of insect galls in four different veredas located in the Northern region of Minas Gerais, Brazil. Overall, we found 75 gall morphotypes, distributed across 50 host species representing 37 plant genera and 22 families. Fabaceae was the plant family with the greatest number of insect gall morphotypes (n = 21), followed by Malpighiaceae (n = 10). The plant genera that supported the highest diversity of insect galls were Copaifera (n = 8) and Byrsomima (n = 5). The plant species Copaifera oblongifolia (n = 6) and Anacardium humile (n = 4) exhibited the highest richness of insect galls. The leaves were the most attacked organs (89% of all galls). Most morphotypes are glabrous (83%), green (69%) and lenticular (60%). The taxa of gall-inducing insects were identified for 46 morphotypes (80%), and were recorded inducers from the orders Diptera, Lepidoptera, and Hymenoptera. Cecidomyiidae (Diptera) was the most representative galling group, with 42 morphotypes, making up 93.3% of the recorded inducers. Among the sampled veredas areas, the Vereda do Peruaçu presented the highest richness of insect gall morphotypes and host plant species. The faunistic similarity was higher in the Pedras and Tiririca veredas, followed by Almescla and Peruaçu veredas. This is the first systematic inventory of insect galls and their host plant in Brazilian veredas. The diversity of insect galls in the studied veredas is relatively high when compared to other Brazilian Cerrado vegetation types.

The importance of Brazilian Conservation Units for the diversity of gall-inducing insects: a study on gall-inducing insect richness in the Chapada Diamantina National Park, state of Bahia, Brazil.

Conservation Units (CUs) tend to have a high richness of herbivorous insects, including gall-inducing insects. Despite this, gall surveys carried out in these environments are punctual and some units have never had their galls investigated, such as the Chapada Diamantina National Park, Bahia (Chapada Diamantina Parna). Aiming to reduce this gap and contribute to future studies in CUs, this study aimed to survey the galls of the Chapada Diamantina Parna, Lençóis, as well as to investigate trends in research on galls in CUs in Brazil. For that, collections were carried out on monthly trips for one year. Published gall surveys were compiled. A total of 107 morphotypes induced in 88 host species were recorded. Most galls are formed in leaves, globoid in shape, green in color, and induced by Cecidomyiidae. This park has a relatively high richness of galls compared to other CUs, demonstrating its importance in the conservation of gall-inducing insects. The results also revealed that the number of surveys has been increasing over the years and that the Southeast concentrates the largest number of studies, a region that also gathers the largest number of specialists, demonstrating a geographic bias in the data.

Gall-inducing insects from the Maricá Environmental Protection Area (RJ, Southeastern Brazil)

Gall-inducing insects from the Maricá Environmental Protection Area (RJ, Southeastern Brazil)

Microbiome and plant cell transformation trigger insect gall induction in cassava.

Several specialised insects can manipulate normal plant development to induce a highly organised structure known as a gall, which represents one of the most complex interactions between insects and plants. Thus far, the mechanism for insect-induced plant galls has remained elusive. To study the induction mechanism of insect galls, we selected the gall induced by Iatrophobia brasiliensis (Diptera: Cecidomyiidae) in cassava (Euphorbiaceae: Manihot esculenta Crantz) as our model. PCR-based molecular markers and deep metagenomic sequencing data were employed to analyse the gall microbiome and to test the hypothesis that gall cells are genetically transformed by insect vectored bacteria. A shotgun sequencing discrimination approach was implemented to selectively discriminate between foreign DNA and the reference host plant genome. Several known candidate insertion sequences were identified, the most significant being DNA sequences found in bacterial genes related to the transcription regulatory factor CadR, cadmium-transporting ATPase encoded by the cadA gene, nitrate transport permease protein (nrtB gene), and arsenical pump ATPase (arsA gene). In addition, a DNA fragment associated with ubiquitin-like gene E2 was identified as a potential accessory genetic element involved in gall induction mechanism. Furthermore, our results suggest that the increased quality and rapid development of gall tissue are mostly driven by microbiome enrichment and the acquisition of critical endophytes. An initial gall-like structure was experimentally obtained in M. esculenta cultured tissues through inoculation assays using a Rhodococcus bacterial strain that originated from the inducing insect, which we related to the gall induction process. We provide evidence that the modification of the endophytic microbiome and the genetic transformation of plant cells in M. esculenta are two essential requirements for insect-induced gall formation. Based on these findings and having observed the same potential DNA marker in galls from other plant species (ubiquitin-like gene E2), we speculate that bacterially mediated genetic transformation of plant cells may represent a more widespread gall induction mechanism found in nature.

SOME BIOTIC LIMITING FACTORS OF DRYOCOSMUS KURIPHILUS (HYMENOPTERA CYNIPIDAE): A SURVEY IN CHESTNUT ORCHARDS NEAR FLORENCE (ITALY)

The biological control of the Asian Chinese gall wasp (ACGW) Dryocosmus kuriphilus, is influenced by several factors. In 2013, a survey was carried out in three chestnut orchards near Florence (Italy) to investigate ACGW parasitization by native parasitoids and the introduced Torymus sinensis. The following two methods were adopted: the first based on the dissection of cynipid galls with the aim of inspecting cells within each gall and the second based on monitoring adult emergence from galls. Parasitization patterns due to gall position related to plant height were also evaluated. Native parasitoids were more abundant in the upper part of tree crowns in June, while in July and August their activity was more evident in the middle and lower parts of chestnut trees. Conversely, parasitization of T. sinensis, was detected at all plant heights. Plant position within stands also affected the performance of both native parasitoids and T. sinensis, with parasitization that progressively decreasead moving toward the interior of the orchards. Gall necrosis was equally evaluated as a limiting factor of ACGW survival. Among the isolated fungal species, Gnomoniopsis castaneae (Tamietti), an endophyte fungus harmful to fruits, colonized both healthy and necrotic galls together with ubiquitous components of fungal communities such as Alternaria sp., Aspergillus sp., Fusarium sp. and Colletotrichum fioriniae. Our results evidenced that T. sinensis was able control the ACGW, while native parasitoids played only a secondary, though non-negligible, role. Conversely, gall necroses had a minor impact on pest control, as their efficacy was limited to the early stages of gall development. Key words: biodiversity, gall-inducing insects, native parasitoids, fungal species

Occurrence and characterization of insect galls in two areas of tropical dry forest (caatinga) in São Francisco River Natural Monument, Brazil

The caatinga vegetation is an important natural laboratory for the study of how plants and gall-inducing insects interact in highly variable and stressful moisture regimes. Despite this, only five gall inventories have been conducted and its richness of inducing insects and host plants has been little known. To contribute to our knowledge of galls from caatinga habitats, we registered and characterized the macroscopic aspects of the galls, then identifed the plant hosts and their associated fauna in two areas of caatinga in São Francisco River Natural Monument (MONA). Nineteen morphotypes of galls were recorded on 11 plant belonging to eight genera and six host plant families. Of the total number of galls recorded, most occurred in the rainy season (n=13). Most of the galls are globoid (n=10), pilose (n=10), green (n=15), and isolated (n=12). Most of the gall-inducing insect species found belonged to Diptera (Cecidomyiidae). All morphotypes recorded in this study are the first ones recorded of galls and their host plants in MONA. We also recorded, for the first time, the occurrence of galls in the floral buds of Cnidoscolus obtusifolius Pohl ex Baill. (Euphorbiaceae), demonstrating the importance of conducting studies in areas not yet sampled in the Caatinga biome. It is expected that this study will stimulate future investigations, helping in the protection and conservation of this conservation area and consequently increasing our knowledge about its biodiversity.

Diversity patterns of host plants and their gall-inducing insects in the Brazilian Cerrado: testing ecological and historical hypotheses

Diversity patterns of host plants and their gall-inducing insects in the Brazilian Cerrado: testing ecological and historical hypotheses

INSECT-INDUCED FOLIAR GALLS: A CROSS-TALK AMONG PHYTOHORMONES FOR TISSUE GROWTH AND ENDOGENOUS DEFENSE

Insect-induced gall tissue has a unique ability to influence its hosts' phenotypic expression. When plants are stressed by insects, phytochemical manipulations in galling tissue strengthen the plant's resilience to subsequent herbivore attacks, and as a result, the damaged plant tissue regenerates and rejuvenates. Gall tissue development and differentiation are initiated by changes in and modulation of a variety of phytohormones in the affected galling sites. Such hormonal changes ultimately boost the plant's ability to respond to herbivore invasions. In this study, the insect-induced gall tissues of three model plants—mature and immature galls and non-gall tissue—were evaluated for five phytohormone gradients. Phytohormone gradients are continually altered and compared from non-differentiated (non-gall) tissue to moderately (immature gall) and highly (mature gall) developed tissue. The results indicate that phytohormones serve a dual role in stimulating the plant's endogenous defense and promoting tissue growth, pointing to a complex chemogenesis process in galling tissue associated with developing neoplasm and plant defensive responses. Tissue abnormalities in galls are thought to have resulted from the herbivore's interactions with the plant on which it infests. Insects' ovipositing fluids or oral discharge may have also contributed to the accumulation of phytohormones in the stressed and wounded tissue. Foliar galls are thus a sign of manifestation of insects' adaptation since the herbivore and their hosts are likely to co-evolve in the context of chemical adaptation.

Comparative transcriptome analysis of sensory genes from the antenna and abdomen of Quadrastichus mendeli Kim

Quadrastichus mendeli Kim is one of the most important parasitoids of Leptocybe invasa Fisher et La Salle, which is an invasive gall-making pest in eucalyptus plantations in the world. Gall-inducing insects live within plant tissues and induce tumor-like growths that provide the insects with food, shelter, and protection from natural enemies. Empirical evidences showed that sensory genes play a key role in the host location of parasitoids. So far, what kind of sensory genes regulate parasitoids to locate gall-inducing insects has not been uncovered. In this study, sensory genes in the antenna and abdomen of Q. mendeli were studied using high-throughput sequencing. In total, 181,543 contigs was obtained from the antenna and abdomen transcriptome of Q. mendeli. The major sensory genes (chemosensory proteins, CSPs; gustatory receptors, GRs; ionotropic receptors, IRs; odorant binding proteins, OBPs; odorant receptors, ORs; and sensory neuron membrane proteins, SNMPs) were identified, and phylogenetic analyses were performed with these genes from Q. mendeli and other model insect species. The gene co-expression network constructed by WGCNA method is robust and reliable. There were 10,314 differentially expressed genes (DEGs), and among them, 99 genes were DEGs. A comprehensive sequence resource with desirable quality was built by comparative transcriptome of the antenna and abdomen of Q. mendeli, enriching the genomic platform of Q. mendeli.

Conferring High IAA Productivity on Low-IAA-Producing Organisms with PonAAS2, an Aromatic Aldehyde Synthase of a Galling Sawfly, and Identification of Its Inhibitor.

Gall-inducing insects often contain high concentrations of phytohormones, such as auxin and cytokinin, which are suggested to be involved in gall induction, but no conclusive evidence has yet been obtained. There are two possible approaches to investigating the importance of phytohormones in gall induction: demonstrating either that high phytohormone productivity can induce gall-inducing ability in non-gall-inducing insects or that the gall-inducing ability is inhibited when phytohormone productivity in galling insects is suppressed. In this study, we show that the overexpression of PonAAS2, which encodes an aromatic aldehyde synthase (AAS) responsible for the rate-limiting step in indoleacetic acid (IAA) biosynthesis in a galling sawfly (Pontania sp.) that contains high levels of endogenous IAA, conferred high IAA productivity on Caenorhabditis elegans, as the model system. This result strongly suggests that PonAAS2 can also confer high IAA productivity on low-IAA-producing insects. We also successfully identified an inhibitor of PonAAS2 in a chemical library. This highly selective inhibitor showed stronger inhibitory activity against AAS than against aromatic amino acid decarboxylase, which belongs to the same superfamily as AAS. We also confirm that this inhibitor clearly inhibited IAA productivity in the high-IAA-producing C. elegans engineered here.

Impact of the gall-inducing fly Polymorphomyia basilica Snow (Diptera: Tephritidae) on the growth and reproduction of Chromolaena odorata (L.) R.M.King & H.Rob (Asteraceae) in the laboratory

Gall-inducing insects are a classic example of how insects can impact the morphology and physiology of their host plants by forming galls which act as nutrient sinks. An 8-months laboratory study was conducted to determine the impact of the galls induced by Polymorphomyia basilica oviposition and or the subsequent larval feedingon the growth and reproduction of Chromolaena odorata. Three treatment levels were used, viz. control: 0% of the shoots were exposed, low infestation: 50% of shoots were exposed, and high infestation, where 100% of the shoots were exposed for P. basilica to oviposit for 48 h each month. Results showed that P. basilica oviposition and or the subsequent feeding by larvae reduced the height and flower production of C. odorata plants but promoted lateral growth by increasing the number of shoot tips. Basal stem diameter was not affected by the presence of the galls. The presence of galls also decreased the leaf and root dry biomass on the treated plants but had no significant impact on stem biomass. The difference between the low- and high-infestation treatments was only significant for root biomass, suggesting that more galls are required for the roots to be affected. Overall, the study showed that P. basilica meets the requirements of an effective biocontrol agent against C. odorata in South Africa. Its release should complement the already released agents in reducing the fitness and productivity of C. odorata.

Integrated Transcriptome and Metabolome Dynamic Analysis of Galls Induced by the Gall Mite Aceria pallida on Lycium barbarum Reveals the Molecular Mechanism Underlying Gall Formation and Development.

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.

Abscisic Acid: A Potential Secreted Effector Synthesized by Phytophagous Insects for Host-Plant Manipulation.

Abscisic acid (ABA) is an isoprenoid-derived plant signaling molecule involved in a wide variety of plant processes, including facets of growth and development as well as responses to abiotic and biotic stress. ABA had previously been reported in a wide variety of animals, including insects and humans. We used high-performance liquid chromatography-electrospray ionization tandem mass spectrometry (HPLC-(ESI)-MS/MS) to examine concentrations of ABA in 17 species of phytophagous insects, including gall- and non-gall-inducing species from all insect orders with species known to induce plant galls: Thysanoptera, Hemiptera, Lepidoptera, Coleoptera, Diptera, and Hymenoptera. We found ABA in insect species in all six orders, in both gall-inducing and non-gall-inducing species, with no tendency for gall-inducing insects to have higher concentrations. The concentrations of ABA in insects often markedly exceeded those typically found in plants, suggesting it is highly improbable that insects obtain all their ABA from their host plant via consumption and sequestration. As a follow-up, we used immunohistochemistry to determine that ABA localizes to the salivary glands in the larvae of the gall-inducing Eurosta solidaginis (Diptera: Tephritidae). The high concentrations of ABA, combined with its localization to salivary glands, suggest that insects are synthesizing and secreting ABA to manipulate their host plants. The pervasiveness of ABA among both gall- and non-gall-inducing insects and our current knowledge of the role of ABA in plant processes suggest that insects are using ABA to manipulate source-sink mechanisms of nutrient allocation or to suppress host-plant defenses. ABA joins the triumvirate of phytohormones, along with cytokinins (CKs) and indole-3-acetic acid (IAA), that are abundant, widespread, and localized to glandular organs in insects and used to manipulate host plants.