ABSTRACT
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 ß-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.
Subject(s)
Monoterpenes , Pistacia , Plant Leaves , Plant Leaves/chemistry , Monoterpenes/chemistry , Pistacia/chemistry , Stereoisomerism , Animals , Aphids , Plant Tumors/parasitologyABSTRACT
Galls are plant neoformations induced by specialized parasites. Since gall inducers rely on reactive plant sites for gall development, variations in abiotic factors that affect plant phenology are expected to impact the life cycle of gall inducers. To test the hypothesis that different light conditions affect both host plant and gall inducer life cycles, we studied the system Eugenia uniflora (Myrtaceae) - Clinodiplosis profusa (Cecidomyiidae), comparing plants occurring in sunny and shaded environments. We mapped phenological differences among individuals of E. uniflora occurring in the two environments and related them to the influence of luminosity on the life cycle of the gall inducer. Shade plants showed lower intensity of leaf sprouting throughout the year compared to sun-exposed plants, especially during the rainy season. Young and mature galls are synchronized with the peak of leaf sprouting at the beginning of the rainy season, lasting longer in sun-exposed plants - approximately two months longer compared to shade plants. The greater light intensity positively impacts the formation and growth of leaves and galls, with an extended period available for their induction and growth. Thus, light is an important factor for the development of gallers, considering that variations in luminosity influenced not only the phenology of the host plant, but also determined the life cycle of gall inducers. Furthermore, changes in plant-environment interactions are expected to affect the life cycle and richness of other host plant-gall inducer systems.
Subject(s)
Eugenia , Sunlight , Eugenia/physiology , Animals , Plant Tumors/parasitology , Light , Plant Leaves/parasitology , Plant Leaves/physiology , Seasons , Host-Parasite Interactions/physiology , Life Cycle Stages/physiologyABSTRACT
This is the first study providing long-term data on the dynamics of bees and wasps and their parasitoids for the evidence-based management of reed beds. Ten years ago, we identified Lipara (Chloropidae) - induced galls on common reed (Phragmites australis, Poaceae) as a critically important resource for specialized bees and wasps (Hymenoptera: Aculeata). We found that they were surprisingly common in relatively newly formed anthropogenic habitats, which elicited questions about the dynamics of bees and wasps and their parasitoids in newly formed reed beds of anthropogenic origin. Therefore, in the winter and spring of 2022/23, we sampled reed galls from the same set of reed beds of anthropogenic and natural origin as those in 2012/13. At 10 sites, the number of sampled galls was similar in both time periods (80-122% of the value from 2012/13); 12 sites experienced a moderate decline (30-79% of the value from 2012/13), and the number of galls at six sampling sites was only 3-23% of their abundance in 2012/13. Spontaneous development was associated with increasing populations. After 10 years of spontaneous development, the populations of bees and wasps (including their parasitoids) bound to Lipara-induced reed galls increased in abundance and species richness or remained at their previous levels, which was dependent on the sampling site. The only identified threat consisted of reclamation efforts. The effects of habitat age were limited, and the assemblages in habitats of near-natural and anthropogenic origin largely overlapped. However, several species were consistently present at lower abundances in the anthropogenic habitats and vice versa. In conclusion, we provided evidence-based support for the establishment of oligotrophic reed beds of anthropogenic origin as management tools providing sustainable habitats for specialized reed gall-associated aculeate hymenopteran inquilines, including the threatened species.
Subject(s)
Ecosystem , Wasps , Animals , Wasps/physiology , Hymenoptera/physiology , Poaceae , Bees/parasitology , Plant Tumors/parasitologyABSTRACT
Gall-forming insects induce various types of galls on their host plants by altering gene expression in host plant organs, and recent studies have been conducted for gene expression in galls. However, the evolutionary trajectories of gene expression patterns and the resulting phenotypes have not yet been studied using multiple related species. We investigated the speciation and the diversification process of galls induced by four closely related aphid species (Hormaphidini) on a host plant species (Hamamelis japonica) by examining the phylogenetic congruence between the geographical divergences of aphids and the host plant, and by comparing their gene expression patterns and resulting phenotypes. Phylogenetic analysis of aphids and the host plant showed that geographical isolation among host plant populations has interrupted gene flow in aphids and accelerated the speciation process. The concentration of phenolics and the complexity of the internal structure of galls were correlated with the expression levels of genes for the biosynthesis of phenolics and morphogenesis respectively. These results suggest that the expression levels of genes for the biosynthesis of phenolics and morphogenesis have evolutionarily increased in galls accelerated by the speciation process of aphids due to the distribution change of the host plant, leading to the related phenotypic evolution. Our study showed the evolutionary process of phenotypic traits in galls in the wild from both gene expression and actual phenotype levels.
Subject(s)
Aphids , Phylogeny , Plant Tumors , Aphids/genetics , Animals , Plant Tumors/parasitology , Plant Tumors/genetics , Phenotype , Gene Flow , Biological Evolution , Secondary Metabolism/genetics , Host-Parasite Interactions/genetics , Genetic Speciation , Gene Expression , Phenols/metabolismABSTRACT
Oak gall wasps have evolved strategies to manipulate the developmental pathways of their host to induce gall formation. This provides shelter and nutrients for the developing larva. Galls are entirely host tissue; however, the initiation, development, and physical appearance are controlled by the inducer. The underlying molecular mechanisms of gall formation, by which one or a small number of cells are reprogrammed and commit to a novel developmental path, are poorly understood. In this study, we sought a deeper insight into the molecular underpinnings of this process. Oak gall wasps have two generations each year, one sexual, and one asexual. Galls formed by these two generations exhibit a markedly different appearance. We sequenced transcriptomes of both the asexual and sexual generations of Neuroterus quercusbaccarum and Neuroterus numismalis. We then deployed Nanopore sequencing to generate long-read sequences to test the hypothesis that gall wasps introduce DNA insertions to determine gall development. We detected potential genome rearrangements but did not uncover any non-host DNA insertions. Transcriptome analysis revealed that transcriptomes of the sexual generations of distinct species of wasp are more similar than inter-generational comparisons from the same species of wasp. Our results highlight the intricate interplay between the host leaves and gall development, suggesting that season and requirements of the gall structure play a larger role than species in controlling gall development and structure.
Subject(s)
Plant Tumors , Quercus , Transcriptome , Wasps , Animals , Wasps/physiology , Wasps/genetics , Plant Tumors/parasitology , Plant Tumors/genetics , Quercus/genetics , Quercus/parasitology , Transcriptome/genetics , Reproduction, Asexual/genetics , Host-Parasite Interactions/genetics , Gene Expression ProfilingABSTRACT
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.
Subject(s)
Biodiversity , Insecta , Parks, Recreational , Plant Tumors , Animals , Brazil , Plant Tumors/parasitology , Insecta/classification , Conservation of Natural ResourcesABSTRACT
Root-knot nematodes (RKNs) infect host plants and obtain nutrients such as sugars for their own development. Therefore, inhibiting the nutrient supply to RKNs may be an effective method for alleviating root-knot nematode disease. At present, the pathway by which sucrose is unloaded from the phloem cells to giant cells (GCs) in root galls and which genes related to sugar metabolism and transport play key roles in this process are unclear. In this study, we found that sugars could be unloaded into GCs only from neighboring phloem cells through the apoplastic pathway. With the development of galls, the contents of sucrose, fructose and glucose in the galls and adjacent tissue increased gradually. SUT1, SUT2, SWEET7a, STP10, SUS3 and SPS1 may provide sugar sources for GCs, while STP1, STP2 and STP12 may transport more sugar to phloem parenchyma cells. At the early stage of Meloidogyne incognita infestation, the sucrose content in tomato roots and leaves increased, while the glucose and fructose contents decreased. SWEET7a, SPS1, INV-INH1, INV-INH2, SUS1 and SUS3 likely play key roles in root sugar delivery. These results elucidated the pathway of sugar unloading in tomato galls and provided an important theoretical reference for eliminating the sugar source of RKNs and preventing root-knot nematode disease.
Subject(s)
Plant Roots , Plant Tumors , Solanum lycopersicum , Tylenchoidea , Tylenchoidea/physiology , Animals , Solanum lycopersicum/parasitology , Solanum lycopersicum/metabolism , Plant Roots/parasitology , Plant Roots/metabolism , Plant Tumors/parasitology , Plant Diseases/parasitology , Sucrose/metabolism , Sugars/metabolism , Carbohydrate MetabolismABSTRACT
Globally, gall-forming insects significantly contribute to the degradation of desert ecosystems. Recent studies have demonstrated that Haloxylon persicum suffers less damage from gall-formers compared to Haloxylon aphyllum. However, the mechanisms driving the long-term metabolic responses of these species to gall-forming biotic stress in their natural environment remain unclear. The current study comparatively analyzes the anatomical features and metabolomic changes in H. aphyllum and H. persicum damaged by gall-forming insects. This research aimed to uncover potential metabolic tolerance mechanisms through GC-MS analysis. The study findings indicate that gall-forming insects cause a reduction in nearly all the anatomical structures of Haloxylon shoots, with the effects being less severe in H. persicum than in H. aphyllum. Thus, the metabolic pathways responsible for the biosynthesis of biologically active substances that enhance resistance to gall inducers were different, specifically in H. aphyllum-the biosynthesis of fatty acids (+their derivatives) and γ-tocopherol (vitamin E) and H. persicum-the biosynthesis of fatty acids (+their derivatives), dialkyl ethers, carbohydrates (+their derivatives), aromatic acid derivatives, phytosterols, γ-tocopherol (vitamin E), phenols, and terpenoids. The results suggest that the modulation of metabolic pathways under biotic stress plays a crucial role in the enhanced survival and growth of H. persicum.
Subject(s)
Metabolome , Animals , Plant Tumors/parasitology , Gas Chromatography-Mass Spectrometry , Metabolomics/methodsABSTRACT
Manipulation of host plant physiology by leaf-galling insects is a multifaceted process. Among fundamental knowledge gaps surrounding this scientifically intriguing phenomenon is the appropriation of plant mineral nutrients and moisture for galling advantage. Small, soluble mineral ions and watery cell contents in dense gall tissues risk disruption during routine sample preparations. In this study, an X-ray microanalysis was applied to investigate gall mineral nutrition. Morphologically diverse leaf galls were sampled from three Australian rainforest tree species. Using cryo-analytical scanning electron microscopy, real-time X-ray analytical maps of cellular mineral nutrients and water were integrated with anatomical images of gall and leaf cross-sectional surfaces. A comparison of host-leaf and gall anatomies bore direct evidence of drastic changes to leaf cells through the galling process. Distinct "wet" and "dry" regions within galls were anatomically and/or chemically differentiated, suggesting specific functionality. "Wet" regions comprising hydrated cells including soft gall-cavity linings where larvae are known to feed contained soluble plant mineral nutrients, while C-rich "dry" tissues largely devoid of mineral nutrients likely contribute structural support. Mapping immobile nutrients such as Mn may provide a means of "matching" specific gall cell types to those in ungalled host-leaf tissues. The findings here provided otherwise inaccessible insights into leaf-gall mineral nutrition.
Subject(s)
Insecta , Minerals , Plant Leaves , Plant Tumors , Plant Leaves/chemistry , Animals , Minerals/analysis , Minerals/metabolism , Plant Tumors/parasitology , Insecta/physiology , Electron Probe Microanalysis , Microscopy, Electron, Scanning , Australia , Cold Temperature , TreesSubject(s)
Plant Leaves , Plant Tumors , Quercus , Wasps , Animals , Wasps/physiology , Plant Leaves/parasitology , Plant Leaves/metabolism , Quercus/parasitology , Plant Tumors/parasitology , MetabolomeABSTRACT
Many insects have evolved the ability to manipulate plant growth to generate extraordinary structures called galls, in which insect larva can develop while being sheltered and feeding on the plant. In particular, cynipid (Hymenoptera: Cynipidae) wasps have evolved to form morphologically complex galls and generate an astonishing array of gall shapes, colors, and sizes. However, the biochemical basis underlying these remarkable cellular and developmental transformations remains poorly understood. A key determinant in plant cellular development is cell wall deposition that dictates the physical form and physiological function of newly developing cells, tissues, and organs. However, it is unclear to what degree cell walls are restructured to initiate and support the formation of new gall tissue. Here, we characterize the molecular alterations underlying gall development using a combination of metabolomic, histological, and biochemical techniques to elucidate how valley oak (Quercus lobata) leaf cells are reprogrammed to form galls. Strikingly, gall development involves an exceptionally coordinated spatial deposition of lignin and xylan to form de novo gall vasculature. Our results highlight how cynipid wasps can radically change the metabolite profile and restructure the cell wall to enable the formation of galls, providing insights into the mechanism of gall induction and the extent to which plants can be entirely reprogrammed to form unique structures and organs.
Subject(s)
Cell Wall , Host-Parasite Interactions , Plant Tumors , Wasps , Animals , Cell Wall/metabolism , Wasps/physiology , Plant Tumors/parasitology , Quercus/metabolism , Quercus/parasitology , Plant Leaves/metabolism , Plant Leaves/parasitology , Lignin/metabolismABSTRACT
Plant galls are novel and sometimes dramatic plant organs whose development is initiated and controlled by parasitic microbes, nematodes, insects and mites. For arthropods, galls provide relative safety from enemies and abiotic stresses while providing nutrition. Galls are formed entirely by the plant, whose transcriptional pathways are modified and coopted to produce a structure specific to the galler species; they comprise a classic example of Dawkins' "extended phenotype". Arthropod-elicited galls are unique in that they are often anatomically complex (Figure 1a), with multiple differentiated tissue types (Figure 1b). A growing number of investigators have studied changes in hostplant gene expression to understand arthropod gall development. In this issue of Molecular Ecology, Martinson et al. (2021) report using RNA sequencing to explore tissue-specific gene expression associated with anatomical and functional gall complexity, demonstrating for the first time that gall tissues are as different transcriptionally as they are anatomically.
Subject(s)
Host-Parasite Interactions , Plant Tumors , Animals , Gene Expression , Host-Parasite Interactions/genetics , Insecta/genetics , Plant Tumors/genetics , Plant Tumors/parasitology , Plants/geneticsABSTRACT
Reactive oxygen species (ROS) are considered the first signaling molecules involved in gall development, linked to the establishment of cyto-histological gradients leading to gall tissue redifferentiation. ROS overproduction induces the failure of gall establishment or its premature senescence. Galls could therefore have efficient mechanisms of ROS dissipation and maintenance of homeostasis, such as polyphenol synthesis. The co-occurrence of ROS and polyphenols in the Espinosa nothofagi galls induced on Nothofagus obliqua buds was explored and was related to the antioxidant capacity of the inner (IC) and outer (OC) gall compartments. We hypothesize that: (i) ROS are produced and accumulated in both tissue compartments of E. nothofagi galls in co-occurrence with polyphenolic, flavonols, and lignin, conferring high antioxidant activity to inner and outer gall tissue compartment; (ii) antioxidant activity is higher in IC related to a higher polyphenol concentration in this compartment. The results show that ROS and polyphenols, mainly flavonols, are produced and accumulated in IC and OC, while lignin accumulated mainly in the IC. In both gall compartments, polyphenols mediate ROS elimination, confirmed by histochemical and spectrophotometry techniques. The IC extract has the highest antioxidant capacity, probably due to lignin deposition and a higher polyphenol concentration in this compartment.
Subject(s)
Antioxidants/metabolism , Fagales/metabolism , Fagales/parasitology , Host-Parasite Interactions/drug effects , Insecta/metabolism , Oxidative Stress/drug effects , Phenols/metabolism , Plant Tumors/parasitology , Animals , Chile , Signal Transduction/drug effectsABSTRACT
Galls, neo-formed plant structures that can occur in different organs, are generated by species-specific interaction with an inducing organism. Inducers manipulate the metabolism of its host. Microgramma vacciniifolia (Langsd. & Fisch.) Copel. is a Neotropical epiphytic fern that hosted two stem galls, one induced by a midge species (Diptera) and other by a micromoth species (Lepidoptera). The aim of this study was to evaluate the impact of these two gall-inducing insects on the biochemistry of phenolic acids and the cyanogenesis in galls, stems and leaves of M. vacciniifolia. High performance liquid chromatography (HPLC) indicated a total of 14 phenol derivatives, including caffeic and coumaric acid. Principal Coordinates Analysis (PCoA) of the phenolic substances indicated three groups consisting (1) non-galled stems and micromoth-induced galls; (2) midge-induced galls; (3) midge induced galls with parasitoids. Regarding the frequency of cyanogenesis assessed by the picrate paper test, the chi-squared test showed significant difference between fertile leaves (8.3%), sterile leaves (27.7%), non-galled stems (0%) and galls. Among galls, only the midge-induced galls analyzed were cyanogenic (15%). Our results indicated that the different gall-inducers (midge and micromoth) promote species-specific alterations to the phenolic substance composition of the host fern.
Galhas são estruturas vegetais neo-formadas que ocorrem em diferentes órgãos. Elas são geradas por uma interação espécie-específica com um organismo indutor. Os indutores manipulam o metabolismo do hospedeiro. Microgramma vacciniifolia (Langsd. & Fisch.) Copel. é uma samambaia epífita neotropical que hospeda duas galhas caulinares, uma induzida por uma espécie de mosquito (Diptera) e outra por uma micromariposa (Lepidoptera). O objetivo deste estudo foi avaliar o impacto desses dois insetos indutores de galhas na bioquímica dos ácidos fenólicos e da cianogênese em galhas, caules e folhas de M. vacciniifolia. Em análise de cromatografia líquida de alta eficiência (CLAE) foi possível indicar a presença de um total de 14 derivados fenólicos, incluindo ácido cafeico e ácido cumárico. Análise das Coordenadas Principais (ACoP) indicou três grupos (1) caules não galhados e galhas induzidas pela micromariposa; (2) galhas induzidas pelo mosquito; (3) galhas induzidas pelo mosquito com parasitoides. Em relação a frequência da cianogênese analisada com o teste do papel picrato, o teste do qui-quadrado apresentou diferença significativa entre as folhas férteis (8,3%), folhas estéreis (27,7%), caules não galhados (0%) e galhas. Entre as galhas, somente aquelas induzidas pelo mosquito foram cianogênicas (15%). Os resultados encontrados indicam, ao menos para as substâncias fenólicas, que os insetos indutores de galha (mosquito e micromariposa) promovem alterações espécie-específica na composição química da samambaia hospedeira.
Subject(s)
Phenolic Compounds/analysis , Diptera , Ferns/parasitology , Lepidoptera , Plant Tumors/parasitologyABSTRACT
In recent years, the Asian gall wasp Dryocosmus kuriphilus has invaded chestnut trees and significantly affected the Portuguese chestnut production. Studies in other countries, such as Japan or Italy, have shown that the parasitoid Torymus sinensis can successfully achieve biological control of D. kuriphilus. Mathematical models help us to understand the dynamics of the interaction between the pest D. kuriphilus and its parasitoid T. sinensis and, consequently, they can help to implement measures that enhance crop pest management. In this work, the evolution of the density of D. kuriphilus and T. sinensis across time and space is studied through the numerical solution of models that include parameters based on observations made in Portugal. Simultaneous releases of the parasitoid are simulated at various locations and at different times. The results indicate that, in the case of a small and homogeneous orchard, biological control can be effective, but, in the case of extensive domains, the pest control is much more difficult to achieve. In order for biological control to be efficient, it is necessary to implement, in each chestnut-producing region, a collective strategy based on the annual monitoring of infestation levels.
Subject(s)
Fagaceae/parasitology , Models, Theoretical , Pest Control, Biological/methods , Plant Tumors/parasitology , Wasps/parasitology , Animals , Computer Simulation , Larva/parasitology , Life Cycle Stages , Pest Control, Biological/statistics & numerical data , Population Density , Portugal , Pupa , Seasons , Wasps/growth & developmentABSTRACT
We describe three new genera of cynipid oak gall wasps from the Nearctic: Burnettweldia Pujade-Villar, Melika Nicholls, gen. nov., Nichollsiella Melika, Pujade-Villar Stone, gen. nov., and Disholandricus Melika, Pujade-Villar Nicholls, gen. nov. (Hymenoptera: Cynipidae: Cynipini). Burnettweldia includes five species, B. californicordazi Cuesta-Porta, Melika Pujade-Villar, sp. nov., B. conalis (Weld), comb. nov., B. corallina (Bassett), comb. nov., B. plumbella (Kinsey), comb. nov., B. washingtonensis (Gillette), comb. nov.. Nichollsiella includes three species, N. arizonica (Cockerell), comb. nov., N. sulcata (Ashmead), comb. nov., and N. puigi Melika, Cuesta-Porta Pujade-Villar, sp. nov.. Disholandricus includes four species, D. chrysolepidis (Ashmead), comb. nov., D. lasius (Ashmead), comb. nov., D. reniformis (McCracken Egbert), comb. nov., D. truckeensis (Ashmead), comb. nov. The genus Paracraspis Weld, comb. rev. is re-established with three species, P. guadaloupensis (Fullaway), P. insolens (Weld), and P. patelloides (Trotter). Descriptions, re-descriptions, diagnoses, keys to genera and species are given, including data on DNA sequences, biology, phenology and distribution.
Subject(s)
Plant Tumors/parasitology , Quercus , Wasps/classification , Animal Distribution , AnimalsABSTRACT
Insect-induced galls are microhabitats distinct from the outer environment that support inhabitants by providing improved nutrients, defence against enemies, and other unique features. It is intriguing as to how insects reprogram and modify plant morphogenesis. Because most of the gall systems are formed on trees, it is difficult to maintain them in laboratories and to comprehend the mechanisms operative in them through experimental manipulations. Herein, we propose a new model insect, Smicronyx madaranus, for studying the mechanisms of gall formation. This weevil forms spherical galls on the shoots of Cuscuta campestris, an obligate parasitic plant. We established a stable system for breeding and maintaining this ecologically intriguing insect in the laboratory, and succeeded in detailed analyses of the gall-forming behaviour, gall formation process, and histochemical and physiological features. Parasitic C. campestris depends on host plants for its nutrients, and usually shows low chlorophyll content and photosynthetic activity. We demonstrate that S. madaranus-induced galls have significantly increased CO2 absorbance. Moreover, chloroplasts and starch accumulated in gall tissues at locations inhabited by the weevil larvae. These results suggest that the gall-inducing weevils enhance the photosynthetic activity in C. campestris, and modify the plant tissue to a nutrient-rich shelter for them.
Subject(s)
Host-Parasite Interactions , Insecta , Photosynthesis , Plant Tumors/etiology , Plants , Animals , Chlorophyll , Disease Susceptibility , Phenotype , Plant Tumors/parasitologyABSTRACT
Chinese galls are the result of hyperplasia in host plants induced by aphids. The metabolism and gene expression of these galls are modified to accommodate the aphids. Here, we highlight the molecular and histologic features of horned galls according to transcriptome and anatomical structures. In primary pathways, genes were found to be unevenly shifted and selectively expressed in the galls and leaves near the galls (LNG). Pathways for amino acid synthesis and degradation were also unevenly shifted, favoring enhanced accumulation of essential amino acids in galls for aphids. Although galls enhanced the biosynthesis of glucose, which is directly available to aphids, glucose content in the gall tissues was lower due to the feeding of aphids. Pathways of gall growth were up-regulated to provide enough space for aphids. In addition, the horned gall has specialized branched schizogenous ducts and expanded xylem in the stalk, which provide a broader feeding surface for aphids and improve the efficiency of transportation and nutrient exchange. Notably, the gene expression in the LNG showed a similar pattern to that of the galls, but on a smaller scale. We suppose the aphids manipulate galls to their advantage, and galls lessen competition by functioning as a medium between the aphids and their host plants.
Subject(s)
Aphids/physiology , Gene Expression Regulation, Plant , Host-Parasite Interactions , Plant Leaves/physiology , Plant Proteins/metabolism , Plant Tumors/genetics , Animals , Gene Expression Profiling , Plant Leaves/parasitology , Plant Proteins/genetics , Plant Tumors/parasitologyABSTRACT
On infection, plant-parasitic nematodes establish feeding sites in roots from which they take up carbohydrates among other nutrients. Knowledge on how carbohydrates are supplied to the nematodes' feeding sites is limited. Here, gene expression analyses showed that RNA levels of OsSWEET11 to OsSWEET15 were extremely low in both Meloidogyne graminicola (Mg)-caused galls and noninoculated roots. All the rice sucrose transporter genes, OsSUT1 to OsSUT5, were either down-regulated in Mg-caused galls compared with noninoculated rice roots or had very low transcript abundance. OsSUT1 was the only gene up-regulated in galls, at 14 days postinoculation (dpi), after being highly down-regulated at 3 and 7 dpi. OsSUT4 was down-regulated at 3 dpi. No noticeable OsSUTs promoter activities were detected in Mg-caused galls of pOsSUT1 to -5::GUS rice lines. Loading experiments with carboxyfluorescein diacetate (CFDA) demonstrated that symplastic connections exist between phloem and Mg-caused giant cells (GCs). According to data from OsGNS5- and OsGSL2-overexpressing rice plants that had decreased and increased callose deposition, respectively, callose negatively affected Mg parasitism and sucrose supply to Mg-caused GCs. Our results suggest that plasmodesmata-mediated sucrose transport plays a pivotal role in sucrose supply from rice root phloem to Mg-caused GCs, and OsSWEET11 to -15 and OsSUTs are not major players in it, although further functional analysis is needed for OsSUT1 and OsSUT4.
Subject(s)
Membrane Transport Proteins/metabolism , Oryza/metabolism , Plant Diseases/parasitology , Plant Proteins/metabolism , Plasmodesmata/metabolism , Sucrose/metabolism , Tylenchoidea/physiology , Animals , Biological Transport , Gene Expression , Genes, Reporter , Glucans/metabolism , Membrane Transport Proteins/genetics , Oryza/parasitology , Phloem/metabolism , Phloem/parasitology , Plant Proteins/genetics , Plant Roots/metabolism , Plant Roots/parasitology , Plant Tumors/parasitologyABSTRACT
In an elaborate form of inter-species exploitation, many insects hijack plant development to induce novel plant organs called galls that provide the insect with a source of nutrition and a temporary home. Galls result from dramatic reprogramming of plant cell biology driven by insect molecules, but the roles of specific insect molecules in gall development have not yet been determined. Here, we study the aphid Hormaphis cornu, which makes distinctive "cone" galls on leaves of witch hazel Hamamelis virginiana. We found that derived genetic variants in the aphid gene determinant of gall color (dgc) are associated with strong downregulation of dgc transcription in aphid salivary glands, upregulation in galls of seven genes involved in anthocyanin synthesis, and deposition of two red anthocyanins in galls. We hypothesize that aphids inject DGC protein into galls and that this results in differential expression of a small number of plant genes. dgc is a member of a large, diverse family of novel predicted secreted proteins characterized by a pair of widely spaced cysteine-tyrosine-cysteine (CYC) residues, which we named BICYCLE proteins. bicycle genes are most strongly expressed in the salivary glands specifically of galling aphid generations, suggesting that they may regulate many aspects of gall development. bicycle genes have experienced unusually frequent diversifying selection, consistent with their potential role controlling gall development in a molecular arms race between aphids and their host plants.