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Microbiome Structure of the Aphid Myzus persicae (Sulzer) Is Shaped by Different Solanaceae Plant Diets.

ABSTRACT: Myzus persicae (Sulzer) is an important insect pest in agriculture that has a very broad host range. Previous research has shown that the microbiota of insects has implications for their growth, development, and environmental adaptation. So far, there is little detailed knowledge about the factors that influence and shape the microbiota of aphids. In the present study, we aimed to investigate diet-induced changes in the microbiome of M. persicae using high-throughput sequencing of bacterial 16S ribosomal RNA gene fragments in combination with molecular and microbiological experiments. The transfer of aphids to different plants from the Solanaceae family resulted in a substantial decrease in the abundance of the primary symbiont Buchnera. In parallel, a substantial increase in the abundance of Pseudomonas was observed; it accounted for up to 69.4% of the bacterial community in M. persicae guts and the attached bacteriocytes. In addition, we observed negative effects on aphid population dynamics when they were transferred to pepper plants (Capsicum annuum L.). The microbiome of this treatment group showed a significantly lower increase in the abundance of Pseudomonas when compared with the other Solanaceae plant diets, which might be related to the adaptability of the host to this diet. Molecular quantifications of bacterial genera that were substantially affected by the different diets were implemented as an additional verification of the microbiome-based observations. Complementary experiments with bacteria isolated from aphids that were fed with different plants indicated that nicotine-tolerant strains occur in Solanaceae-fed specimens, but they were not restricted to them. Overall, our mechanistic approach conducted under controlled conditions provided strong indications that the aphid microbiome shows responses to different plant diets. This knowledge could be used in the future to develop environmentally friendly methods for the control of insect pests in agriculture.

SUBMITTER: He B

PROVIDER: S-EPMC8287905 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundAphid attack induces defense responses in plants activating several signaling cascades that led to the production of toxic, repellent or antinutritive compounds and the consequent reorganization of the plant primary metabolism. Pepper (Capsicum annuum L.) leaf proteomic response against Myzus persicae (Sulzer) has been investigated and analyzed by LC-MS/MS coupled with bioinformatics tools.ResultsInfestation with an initially low density (20 aphids/plant) of aphids restricted to a single leaf taking advantage of clip cages resulted in 6 differentially expressed proteins relative to control leaves (3 proteins at 2 days post-infestation and 3 proteins at 4 days post-infestation). Conversely, when plants were infested with a high density of infestation (200 aphids/plant) 140 proteins resulted differentially expressed relative to control leaves (97 proteins at 2 days post-infestation, 112 proteins at 4 days post-infestation and 105 proteins at 7 days post-infestation). The majority of proteins altered by aphid attack were involved in photosynthesis and photorespiration, oxidative stress, translation, protein folding and degradation and amino acid metabolism. Other proteins identified were involved in lipid, carbohydrate and hormone metabolism, transcription, transport, energy production and cell organization. However proteins directly involved in defense were scarce and were mostly downregulated in response to aphids.ConclusionsThe unexpectedly very low number of regulated proteins found in the experiment with a low aphid density suggests an active mitigation of plant defensive response by aphids or alternatively an aphid strategy to remain undetected by the plant. Under a high density of aphids, pepper leaf proteome however changed significantly revealing nearly all routes of plant primary metabolism being altered. Photosynthesis was so far the process with the highest number of proteins being regulated by the presence of aphids. In general, at short times of infestation (2 days) most of the altered proteins were upregulated. However, at longer times of infestation (7 days) the protein downregulation prevailed. Proteins involved in plant defense and in hormone signaling were scarce and mostly downregulated.

Project description:Myzus persicae (Sulzer), commonly known as the green peach aphid, is a notorious pest that causes substantial losses to a range of crops and can transmit several plant viruses, including potato virus Y (PVY). Chemical insecticides provide only partial control of this pest and their use is not environmentally sustainable. In recent years, many genes related to growth, development, and reproduction have been used as targets for pest control. These include Gustavus (Gus), a highly conserved gene that has been reported to play an essential part in the genesis of germline cells and, hence, in fecundity in the model insect Drosophila melanogaster. We hypothesized that the Gustavus (Gus) gene was a potential target that could be used to regulate the M. persicae population. In this study, we report the first investigation of an ortholog of Gus in M. persicae, designated MpGus, and describe its role in the fecundity of this insect. First, we identified the MpGus mRNA sequence in the M. persicae transcriptome database, verified its identity with reverse transcription-polymerase chain reaction (RT-PCR), and then evaluated the transcription levels of MpGus in M. persicae nymphs of different instars and tissues with real-time quantitative PCR (RT-qPCR). To investigate its role in regulating the fecundity of M. persicae, we used RNA interference (RNAi) to silence the expression of MpGus in adult insects; this resulted in a significant reduction in the number of embryos (50.6%, P < 0.01) and newborn nymphs (55.7%, P < 0.01) in the treated aphids compared with controls. Interestingly, MpGus was also significantly downregulated in aphids fed on tobacco plants that had been pre-infected with PVY N , concomitant with a significant reduction (34.1%, P < 0.01) in M. persicae fecundity. Collectively, these data highlight the important role of MpGus in regulating fecundity in M. persicae and indicate that MpGus is a promising RNAi target gene for control of this pest species.

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Microbiome Structure of the Aphid Myzus persicae (Sulzer) Is Shaped by Different Solanaceae Plant Diets.

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