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Current Biology : CB May 2021In 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...
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.
Topics: Animals; Anthocyanins; Aphids; Female; Hamamelis; Host-Parasite Interactions; Insect Proteins; Male; Plant Leaves; Plant Tumors
PubMed: 33657407
DOI: 10.1016/j.cub.2021.01.104 -
Journal of Plant Research Jul 2023Oaks serve as host plants for numerous insects, including those forming galls. Galls induced on oaks are completely dependent on leaf resources. Many other folivores...
Oaks serve as host plants for numerous insects, including those forming galls. Galls induced on oaks are completely dependent on leaf resources. Many other folivores damage veins of leaves, which may result in cutting galls off from sources of assimilates, nutrients and water. We hypothesised that the disruption of the continuity of leaf vascular tissues stops gall development, leading to the death of the larva. Leaves of sessile oak (Quercus petraea) with Cynips quercusfolii galls in the initial stage of development were marked. The diameter of the galls was measured, and the vein on which the gall was present was cut. Four experimental treatments were established: control - with no cutting, cutting the vein distal to the gall relative to the petiole, cutting the vein basal to the gall and cutting both sides. The average survival rate (live galls at the end of the experiment including healthy larvae, pupae or imagines inside) - was 28.9%. The rate varied depending on the treatment and was 13.6% in the treatment with the vein cut on both sides and about 30% in the remaining treatments. However, this difference was not statistically significant. The growth dynamics of galls are highly dependent on the experimental treatment. The largest galls grew in the control treatment, and the smallest galls were in the treatments with the veins cut on both sides. Unexpectedly, even cutting veins on both sides did not result in the immediate dieback of the galls. The results suggest that the galls are very strong nutrient and water sinks. The functions of the cut vein are likely taken over by other lower-order veins, allowing nourishment of the gall to complete larva development.
Topics: Animals; Quercus; Wasps; Plant Tumors; Larva; Plant Leaves
PubMed: 37133571
DOI: 10.1007/s10265-023-01462-8 -
Plant Signaling & Behavior 2019Agrobacterium tumefaciens is a plant pathogen which provokes galls on roots and stems (crown-gall disease) and colonizes them. Two approaches combining omics were used...
Agrobacterium tumefaciens is a plant pathogen which provokes galls on roots and stems (crown-gall disease) and colonizes them. Two approaches combining omics were used to decipher the lifestyle of A. tumefaciens in plant tumors: an integrative approach when omics were used on A. tumefaciens cells collected from plant tumors, a deconvolution approach when omics were used on A. tumefaciens cells exploiting a single tumor metabolite in pure culture assay. This addendum highlights some recent results on the biotroph lifestyle of A. tumefaciens in plant tumors.
Topics: Agrobacterium tumefaciens; Gene Expression Regulation, Plant; Plant Roots; Plant Tumors; Plants, Genetically Modified; Transformation, Genetic
PubMed: 30774017
DOI: 10.1080/15592324.2019.1581562 -
Scientific Reports Feb 2023Insect galls are abnormal plant organs formed by gall-inducing insects to provide shelter and nutrients for themselves. Although insect galls are spatialized complex...
Insect galls are abnormal plant organs formed by gall-inducing insects to provide shelter and nutrients for themselves. Although insect galls are spatialized complex structures with unique shapes and functions, the molecular mechanism of the gall formation and the screening system for the gall inducing effectors remains unknown. Here, we demonstrate that an extract of a gall-inducing aphid, Schlechtendalia chinensis, induces an abnormal structure in the root-tip region of Arabidopsis seedlings. The abnormal structure is composed of stem-like cells, vascular, and protective tissues, as observed in typical insect galls. Furthermore, we confirm similarities in the gene expression profiles between the aphid-treated seedlings and the early developmental stages of Rhus javanica galls formed by S. chinensis. Based on the results, we propose a model system for analyzing the molecular mechanisms of gall formation: the Arabidopsis-based Gall-Forming Assay (Ab-GALFA). Ab-GALFA could be used not only as a model to elucidate the mechanisms underlying gall formation, but also as a bioassay system to isolate insect effector molecules of gall-induction.
Topics: Animals; Arabidopsis; Insecta; Aphids; Transcriptome; Plant Tumors
PubMed: 36781988
DOI: 10.1038/s41598-023-29302-8 -
International Journal of Molecular... May 2021Chinese 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....
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.
Topics: Animals; Aphids; Gene Expression Profiling; Gene Expression Regulation, Plant; Host-Parasite Interactions; Plant Leaves; Plant Proteins; Plant Tumors
PubMed: 34068250
DOI: 10.3390/ijms22105166 -
Environmental Microbiology Mar 2013Ornithine lipids (OLs) are phosphorus-free membrane lipids that are widespread among Gram-negative bacteria. Their basic structure consists of a 3-hydroxy fatty acyl...
Ornithine lipids (OLs) are phosphorus-free membrane lipids that are widespread among Gram-negative bacteria. Their basic structure consists of a 3-hydroxy fatty acyl group attached in amide linkage to the α-amino group of ornithine and a second fatty acyl group ester-linked to the 3-hydroxy position of the first fatty acid. It has been shown that OLs can be hydroxylated within the amide-linked fatty acyl moiety, the secondary fatty acyl moiety or within the ornithine moiety. These modifications have been related to increased stress tolerance and symbiotic proficiency in different organisms such as Rhizobium tropici or Burkholderia cenocepacia. Analysing the membrane lipid composition of the plant pathogen Agrobacterium tumefaciens we noticed that it forms two different OLs. In the present work we studied if OLs play a role in stress tolerance and pathogenicity in A. tumefaciens. Mutants deficient in the OLs biosynthesis genes olsB or olsE were constructed and characterized. They either completely lack OLs (ΔolsB) or only form the unmodified OL (ΔolsE). Here we present a characterization of both OL mutants under stress conditions and in a plant transformation assay using potato tuber discs. Surprisingly, the lack of agrobacterial OLs promotes earlier tumour formation on the plant host.
Topics: Agrobacterium; Lipids; Membrane Lipids; Ornithine; Plant Tubers; Plant Tumors; Solanum tuberosum; Stress, Physiological
PubMed: 22958119
DOI: 10.1111/j.1462-2920.2012.02867.x -
Anais Da Academia Brasileira de Ciencias 2023This study aimed at survey insect galls of an Amazon rainforest area in Rondônia, Brazil. We found 152 gall morphotypes in 103 plant species. Fabaceae were the host...
This study aimed at survey insect galls of an Amazon rainforest area in Rondônia, Brazil. We found 152 gall morphotypes in 103 plant species. Fabaceae were the host with the greatest gall richness. Leaves were the most galled organ. Globose and glabrous galls were the most frequent. Cecidomyiidae were responsible for most of the galls. This is the first record of 110 galls morphotypes and 23 host plants species in this biome. Ten gallers are endemic in Brazil. Five genera of Cecidomyiidae were first recorded in Rondônia as well as Schismatodiplosis lantanae Rübsaamen, 1908.
Topics: Animals; Rainforest; Brazil; Host-Parasite Interactions; Plant Tumors; Insecta; Plants; Plant Leaves
PubMed: 37991097
DOI: 10.1590/0001-3765202320190869 -
Aboveground insect infestation attenuates belowground Agrobacterium-mediated genetic transformation.The New Phytologist Jul 2015Agrobacterium tumefaciens causes crown gall disease. Although Agrobacterium can be popularly used for genetic engineering, the influence of aboveground insect...
Agrobacterium tumefaciens causes crown gall disease. Although Agrobacterium can be popularly used for genetic engineering, the influence of aboveground insect infestation on Agrobacterium induced gall formation has not been investigated. Nicotiana benthamiana leaves were exposed to a sucking insect (whitefly) infestation and benzothiadiazole (BTH) for 7 d, and these exposed plants were inoculated with a tumorigenic Agrobacterium strain. We evaluated, both in planta and in vitro, how whitefly infestation affects crown gall disease. Whitefly-infested plants exhibited at least a two-fold reduction in gall formation on both stem and crown root. Silencing of isochorismate synthase 1 (ICS1), required for salicylic acid (SA) synthesis, compromised gall formation indicating an involvement of SA in whitefly-derived plant defence against Agrobacterium. Endogenous SA content was augmented in whitefly-infested plants upon Agrobacterium inoculation. In addition, SA concentration was three times higher in root exudates from whitefly-infested plants. As a consequence, Agrobacterium-mediated transformation of roots of whitefly-infested plants was clearly inhibited when compared to control plants. These results suggest that aboveground whitefly infestation elicits systemic defence responses throughout the plant. Our findings provide new insights into insect-mediated leaf-root intra-communication and a framework to understand interactions between three organisms: whitefly, N. benthamiana and Agrobacterium.
Topics: Agrobacterium tumefaciens; Animals; Cyclopentanes; Gene Expression Regulation, Plant; Gene Silencing; Genes, Plant; Hemiptera; Models, Biological; Molecular Sequence Data; Oxylipins; Plant Exudates; Plant Roots; Plant Stems; Plant Tumors; Plant Viruses; Salicylic Acid; Nicotiana; Transformation, Genetic
PubMed: 25676198
DOI: 10.1111/nph.13324 -
Annals of Botany Aug 2004Differences in the chemical and physical traits of plants caused by both genetic and habitat characteristics may influence attack by herbivores. Leaves of Qualea...
BACKGROUND AND AIMS
Differences in the chemical and physical traits of plants caused by both genetic and habitat characteristics may influence attack by herbivores. Leaves of Qualea parviflora (Vochysiaceae), a common tree of different habitats in the Brazilian Neotropical savannas (cerrado), are susceptible to severe attack by herbivorous free-living and gall-forming insects. Attack by free-living and gall-forming insects within and between populations of Q. parviflora were examined and it was determined to what extent genetic variability (detected by RAPD markers), phenotypic characteristics of the plants and habit traits influence the number of free-living and gall-forming insect species and individuals attacking the plants, and the intensity of attack.
METHODS
On four occasions in 2000, leaves were sampled from ten individual trees in each of three types of vegetation in the cerrado: campo sujo, cerrado sensu stricto and cerradão at the Ecological Station of Pirapitinga (ESP), in Três Marias, north-western Minas Gerais, Brazil. Genetic variability was detected by RAPD markers, and concentrations of nutrients, phenols and tannins, sclerophylly and pre-dawn water potential of leaves were measured. Water and nutrient contents in the soil below each tree characterized the habitat. The free-living and gall-forming herbivorous insects were determined.
KEY RESULTS
Of 69 RAPD markers analysed, 41 were polymorphic and were used for analyses of genetic variability of Q. parviflora. Most of the variability occurred within habitats, accounting for 97.65 % of the genetic variability. Plants in the cerrado sensu stricto and campo sujo were the most similar. There were no significant associations between genetic similarity and the chemical and physical traits of Q. parviflora, or with habitat, nor was there significant correlation between phenotypic and habitat traits. Increasing concentrations of tannins and sulphur, C : N ratio and sclerophylly correlated with increasing percentage of leaf area damaged by herbivores. Decreased sclerophylly, concentration of tannins and C : N ratio, and increased concentration of nutrients in leaves correlated with increased severity of attack by gall-forming insects.
CONCLUSIONS
Nutrient concentration in the soil had more influence, indirectly, on free-feeding insects than did composition of Q. parviflora leaves. However, gall-forming insects are affected more by leaf quality, attacking fewer sclerophyllous leaves, with larger nutrient but smaller tannin concentrations.
Topics: Animals; Brazil; Carbon; Ecosystem; Environment; Feeding Behavior; Genetic Markers; Genetic Variation; Immunity, Innate; Insecta; Magnoliopsida; Nitrogen; Phenotype; Plant Diseases; Plant Leaves; Plant Tumors; Random Amplified Polymorphic DNA Technique; Soil; Sulfur; Tannins; Water
PubMed: 15234928
DOI: 10.1093/aob/mch136 -
Applied and Environmental Microbiology Sep 2016Crown gall disease of grapevine is caused by virulent Agrobacterium strains and establishes a suitable habitat for agrobacteria and, potentially, other bacteria. The...
UNLABELLED
Crown gall disease of grapevine is caused by virulent Agrobacterium strains and establishes a suitable habitat for agrobacteria and, potentially, other bacteria. The microbial community associated with grapevine plants has not been investigated with respect to this disease, which frequently results in monetary losses. This study compares the endophytic microbiota of organs from grapevine plants with or without crown gall disease and the surrounding vineyard soil over the growing seasons of 1 year. Amplicon-based community profiling revealed that the dominating factor causing differences between the grapevine microbiota is the sample site, not the crown gall disease. The soil showed the highest microbial diversity, which decreased with the distance from the soil over the root and the graft union of the trunk to the cane. Only the graft union microbiota was significantly affected by crown gall disease. The bacterial community of graft unions without a crown gall hosted transient microbiota, with the three most abundant bacterial species changing from season to season. In contrast, graft unions with a crown gall had a higher species richness, which in every season was dominated by the same three bacteria (Pseudomonas sp., Enterobacteriaceae sp., and Agrobacterium vitis). For in vitro-cultivated grapevine plantlets, A. vitis infection alone was sufficient to cause crown gall disease. Our data show that microbiota in crown galls is more stable over time than microbiota in healthy graft unions and that the microbial community is not essential for crown gall disease outbreak.
IMPORTANCE
The characterization of bacterial populations in animal and human diseases using high-throughput deep-sequencing technologies, such as 16S amplicon sequencing, will ideally result in the identification of disease-specific microbiota. We analyzed the microbiota of the crown gall disease of grapevine, which is caused by infection with the bacterial pathogen Agrobacterium vitis. All other Agrobacterium species were found to be avirulent, even though they lived together with A. vitis in the same crown gall tumor. As has been reported for human cancer, the crown gall tumor also hosted opportunistic bacteria that are adapted to the tumor microenvironment. Characterization of the microbiota in various diseases using amplicon sequencing may help in early diagnosis, to serve as a preventative measure of disease in the future.
Topics: Bacteria; Biota; Cluster Analysis; DNA, Bacterial; DNA, Ribosomal; Endophytes; Phylogeny; Plant Diseases; Plant Tumors; RNA, Ribosomal, 16S; Sequence Analysis, DNA; Soil Microbiology; Vitis
PubMed: 27371584
DOI: 10.1128/AEM.01131-16