A new galling insect model enhances photosynthetic activity in an obligate holoparasitic plant.
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ABSTRACT:
SUBMITTER: Murakami R
PROVIDER: S-EPMC8217554 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Some insects can redirect plant development to form unique organs called galls, which provide these insects with unique, enhanced food and protection from enemies and the elements. Many galls resemble flowers or fruits, suggesting that elements of reproductive development may be involved. We addressed this possibility using RNA sequencing (RNAseq) to quantify the transcriptional responses of wild grapevine (Vitis riparia Michx.) leaves to a galling parasite, phylloxera (Daktulosphaira vitifoliae (Fitch 1855)). If development of reproductive structures is part of gall formation, we expected to find significantly elevated expression of genes involved in flower and/or fruit development in developing galls as opposed to ungalled leaves. We found that reproductive gene ontology classes were significantly enriched in developing galls, and that expression of many putative genes involved in flower formation was significantly increased, particularly in later gall stages. The patterns of gene expression found in galls suggest that phylloxera exploits vascular cambium to provide meristematic tissue and redirects leaf development towards formation of carpels. The phylloxera leaf gall, and perhaps other similar galls, appears to be phenotypically and transcriptionally convergent on the plant carpel.
2018-08-16 | GSE118569 | GEO
Project description:Many insect species have acquired the ability to redirect plant development to form unique organs called galls, which provide these insects with unique, enhanced food and protection from enemies and the elements. Many galls resemble flowers or fruits, suggesting that elements of reproductive development may be involved. We tested this hypothesis using RNA sequencing to quantify the transcriptional responses of wild grapevine (Vitis riparia) leaves to a galling parasite, phylloxera (Daktulosphaira vitifoliae). If development of reproductive structures is part of gall formation, we expected to find significantly elevated expression of genes involved in flower and/or fruit development in developing galls as opposed to ungalled leaves. We found that reproductive gene ontology categories were significantly enriched in developing galls, and that expression of many candidate genes involved in floral development were significantly increased, particularly in later gall stages. The patterns of gene expression found in galls suggest that phylloxera exploits vascular cambium to provide meristematic tissue and redirects leaf development towards formation of carpels. The phylloxera leaf gall appears to be phenotypically and transcriptionally similar to the carpel, due to the parasite hijacking underlying genetic machinery in the host plant.
| S-EPMC6372598 | biostudies-literature
Project description:Host plants may harbor a variable number of galling insect species, with some species being able to harbor a high diversity of these insects, being therefore called superhost plants. In the present study, we tested the hypothesis that the occurrence of superhost plant species of genus Qualea (Vochysiaceae) affects the structure of plant-galling insect ecological networks in Brazilian Cerrado. We sampled a total of 1882 plants grouped in 131 species and 43 families, of which 64 species and 31 families of host plants hosted 112 galling insect species. Our results showed that occurrence of superhosts of genus Qualea increased the linkage density of plant species, number of observed interactions, and the size of plant-galling insect networks and negatively affected the network connectance (but had no effect on the residual connectance). Although the occurrence of Qualea species did not affect the plant species richness, these superhosts increased the species richness and the number of interactions of galling insects. Our study represents a step forward in relation to previous studies that investigated the effects of plant diversity on the plant-insect networks, showing that few superhost plant species alter the structure of plant-herbivore networks, even without having a significant effect on plant diversity.
| S-EPMC6843997 | biostudies-literature
Project description:Herbivorous insect species are constantly challenged with reactive oxygen species (ROS) generated from endogenous and exogenous sources. ROS produced within insects because of stress and prooxidant allelochemicals produced by host plants in response to herbivory require a complex mode of antioxidant defense during insect/plant interactions. Some insect herbivores have a midgut-based defense against the suite of ROS encountered. Because the Hessian fly (Mayetiola destructor) is the major insect pest of wheat worldwide, and an emerging model for all gall midges, we investigated its antioxidant responses during interaction with its host plant. Quantitative data for two phospholipid glutathione peroxidases (MdesPHGPX-1 and MdesPHGPX-2), two catalases (MdesCAT-1 and MdesCAT-2), and two superoxide dismutases (MdesSOD-1 and MdesSOD-2) revealed high levels of all of the mRNAs in the midgut of larvae on susceptible wheat (compatible interaction). During development of the Hessian fly on susceptible wheat, a differential expression pattern was observed for all six genes. Analysis of larvae on resistant wheat (incompatible interaction) compared with larvae on susceptible wheat showed increased levels of mRNAs in larvae on resistant wheat for all of the antioxidant genes except MdesSOD-1 and MdesSOD-2. We postulate that the increased mRNA levels of MdesPHGPX-1, MdesPHGPX-2, MdesCAT-1, and MdesCAT-2 reflect responses to ROS encountered by larvae while feeding on resistant wheat seedlings and/or ROS generated endogenously in larvae because of stress/starvation. These results provide an opportunity to understand the cooperative antioxidant defense responses in the Hessian fly/wheat interaction and may be applicable to other insect/plant interactions.
| S-EPMC1783901 | biostudies-literature
Project description:Evolutionary key innovations give organisms access to new ecological resources and cause rapid, sometimes spectacular adaptive radiation. The well known obligate pollination mutualism between yuccas and yucca moths is a major model system for studies of coevolution, and it relies on the key innovation in the moths of complex tentacles used for pollen collecting and active pollination. These structures lack apparent homology in other insects, making them a rare example of a novel limb. We performed anatomical and behavioral studies to determine their origin and found evidence of a remarkably simple mechanism. Morphological analyses of the tentacles and adjacent mouthparts in pollinators and closely related taxa showed that the tentacle appears abruptly in female pollinating yucca moths. Several morphological synapomorphies between the galeae, which constitute the characteristic lepidopteran proboscis, and the tentacle suggest that the tentacle evolved quickly through expression of the genetic template for the galea at an apical growth bud on the first segment of the maxillary palp. Behavioral data indicate that tentacle and proboscis movements are controlled by a shared hydraulic extension mechanism, thus no new mechanism was needed for tentacle function. Known developmental paths from other insects can explain the origin of this sex-specific key innovation in a few steps.
| S-EPMC122798 | biostudies-literature
Project description:BackgroundAll eukaryotes share a conserved network of processes regulated by the proteasome and fundamental to growth, development, or perception of the environment, leading to complex but often predictable responses to stress. As a specialized component of the ubiquitin-proteasome system (UPS), the RING finger domain mediates protein-protein interactions and displays considerable versatility in regulating many physiological processes in plants. Many pathogenic organisms co-opt the UPS through RING-type E3 ligases, but little is known about how insects modify these integral networks to generate novel plant phenotypes.ResultsUsing a combination of transcriptome sequencing and genome annotation of a grapevine galling species, Daktulosphaira vitifoliae, we identified 138 putatively secretory protein RING-type (SPRINGs) E3 ligases that showed structure and evolutionary signatures of genes under rapid evolution. Moreover, the majority of the SPRINGs were more expressed in the feeding stage than the non-feeding egg stage, in contrast to the non-secretory RING genes. Phylogenetic analyses indicated that the SPRINGs formed clusters, likely resulting from species-specific gene duplication and conforming to features of arthropod host-manipulating (effector) genes. To test the hypothesis that these SPRINGs evolved to manipulate cellular processes within the plant host, we examined SPRING interactions with grapevine proteins using the yeast two-hybrid assay. An insect SPRING interacted with two plant proteins, a cellulose synthase, CSLD5, and a ribosomal protein, RPS4B suggesting secretion reprograms host immune signaling, cell division, and stress response in favor of the insect. Plant UPS gene expression during gall development linked numerous processes to novel organogenesis.ConclusionsTaken together, D. vitifoliae SPRINGs represent a novel gene expansion that evolved to interact with Vitis hosts. Thus, a pattern is emerging for gall forming insects to manipulate plant development through UPS targeting.
| S-EPMC6892190 | biostudies-literature
Project description:BACKGROUND:Transformation and subsequent regeneration of holoparasitic plants has never been reported, in part due to challenges in developing transformation protocols, but also because regeneration of obligate parasites is difficult since their survival depends completely on successful haustorium penetration of a host and the formation of vascular connections. The recent completion of a massive transcriptome sequencing project (the Parasitic Plant Genome Project) will fuel the use of genomic tools for studies on parasitic plants. A reliable system for holoparasite transformation is needed to realize the full value of this resource for reverse genetics and functional genomics studies. RESULTS:Here we demonstrate that transformation of Phelipanche aegyptiaca is achieved by infection of 3 month-old in vitro grown P. aegyptiaca calli with Agrobacterium rhizogenes harboring the yellow fluorescent protein (YFP). Four months later, YFP-positive regenerated calli were inoculated onto tomato plants growing in a minirhizotron system. Eight days after inoculation, transgenic parasite tissue formed lateral haustoria that penetrated the host and could be visualized under UV illumination through intact host root tissue. YFP-positive shoot buds were observed one month after inoculation. CONCLUSIONS:This work constitutes a breakthrough in holoparasitic plant research methods. The method described here is a robust system for transformation and regeneration of a holoparasitic plant and will facilitate research on unique parasitic plant capabilities such as host plant recognition, haustorial formation, penetration and vascular connection.
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Project description:Symbiosis, the close association of unrelated organisms, has been pivotal in biological diversification. In the obligate symbioses found in many insect hosts, organisms that were once independent are permanently and intimately associated, resulting in expanded ecological capabilities. The primary model for this kind of symbiosis is the association between the bacterium Buchnera and the pea aphid (Acyrthosiphon pisum). A longstanding obstacle to efforts to illuminate genetic changes underlying obligate symbioses has been the inability to experimentally disrupt and reconstitute symbiont-host partnerships. Our experiments show that Buchnera can be experimentally transferred between aphid matrilines and, furthermore, that Buchnera replacement has a massive effect on host fitness. Using a recipient pea aphid matriline containing Buchnera that are heat sensitive because of an allele eliminating the heat shock response of a small chaperone, we reduced native Buchnera through heat exposure and introduced a genetically distinct Buchnera from another matriline, achieving complete replacement and stable inheritance. This transfer disrupted 100 million years (? 1 billion generations) of continuous maternal transmission of Buchnera in its host aphids. Furthermore, aphids with the Buchnera replacement enjoyed a dramatic increase in heat tolerance, directly demonstrating a strong effect of symbiont genotype on host ecology.
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Project description:Drought is a major threat to crop production worldwide and is accentuated by global warming. Plant responses to this abiotic stress involve physiological changes overlapping, at least partially, the defense pathways elicited both by viruses and their herbivore vectors. Recently, a number of theoretical and empirical studies anticipated the influence of climate changes on vector-borne viruses of plants and animals, mainly addressing the effects on the virus itself or on the vector population dynamics, and inferring possible consequences on virus transmission. Here, we directly assess the effect of a severe water deficit on the efficiency of aphid-transmission of the Cauliflower mosaic virus (CaMV) or the Turnip mosaic virus (TuMV). For both viruses, our results demonstrate that the rate of vector-transmission is significantly increased from water-deprived source plants: CaMV transmission reproducibly increased by 34% and that of TuMV by 100%. In both cases, the enhanced transmission rate could not be explained by a higher virus accumulation, suggesting a more complex drought-induced process that remains to be elucidated. The evidence that infected plants subjected to drought are much better virus sources for insect vectors may have extensive consequences for viral epidemiology, and should be investigated in a wide range of plant-virus-vector systems.
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Project description:Somatic embryogenesis (SE), a clonal propagation method utilizing somatic cells, occurs under conditions that activate plant stress adaptation mechanisms such as production of protective secondary metabolites. Surprisingly, possible differences in susceptibility to insect pests between SE-generated and conventionally cultivated plants have not been previously explored. Here, we recorded frequencies and levels of bark-feeding damage by pine weevils (Hylobius abietis) in two large field trials, consisting of emblings (SE-propagated plants) and seedlings from 50 half-sib Norway spruce (Picea abies) families. We found that emblings were less frequently attacked by pine weevils, and when attacked, they were damaged to a lesser extent than seedlings. Moreover, we detected significant additive genetic variation in damage levels received by plants, indicating a heritable component to differences in resistance to insect herbivory among half-sib families. We present first-time evidence that emblings can be more resistant than seedlings to herbivorous insect damage, thus, SE appears to confer a previously unknown plant protection advantage. This finding indicates novel avenues to explore mechanisms underlying plant resistance and new approaches to develop non-toxic measures against insect pests.
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