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Ecdysone signaling underlies the pea aphid transgenerational wing polyphenism.

ABSTRACT: The wing polyphenism of pea aphids is a compelling laboratory model with which to study the molecular mechanisms underlying phenotypic plasticity. In this polyphenism, environmental stressors such as high aphid density cause asexual, viviparous adult female aphids to alter the developmental fate of their embryos from wingless to winged morphs. This polyphenism is transgenerational, in that the pea aphid mother experiences the environmental signals, but it is her offspring that are affected. Previous research suggested that the steroid hormone ecdysone may play a role in this polyphenism. Here, we analyzed ecdysone-related gene expression patterns and found that they were consistent with a down-regulation of the ecdysone pathway being involved in the production of winged offspring. We therefore predicted that reduced ecdysone signaling would result in more winged offspring. Experimental injections of ecdysone or its analog resulted in a decreased production of winged offspring. Conversely, interfering with ecdysone signaling using an ecdysone receptor antagonist or knocking down the ecdysone receptor gene with RNAi resulted in an increased production of winged offspring. Our results are therefore consistent with the idea that ecdysone plays a causative role in the regulation of the proportion of winged offspring produced in response to crowding in this polyphenism. Our results also show that an environmentally regulated maternal hormone can mediate phenotype production in the next generation, as well as provide significant insight into the molecular mechanisms underlying the functioning of transgenerational phenotypic plasticity.

SUBMITTER: Vellichirammal NN

PROVIDER: S-EPMC5307454 | biostudies-other | 2017 Feb

REPOSITORIES: biostudies-other

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The genomewide transcriptional response underlying the pea aphid wing polyphenism.

Project description:Phenotypic plasticity is a key life history strategy used by many plants and animals living in heterogeneous environments. A multitude of studies have investigated the costs and limits of plasticity, as well as the conditions under which it evolves. Much less well understood are the molecular genetic mechanisms that enable an organism to sense its environment and respond in a plastic manner. The pea aphid wing polyphenism is a compelling laboratory model to study these mechanisms. In this polyphenism, environmental stressors like high density cause asexual, viviparous adult female aphids to change the development of their embryos from wingless to winged morphs. The life history trade-offs between the two morphs have been intensively studied, but the molecular mechanisms underlying this process remain largely unknown. We therefore performed a genomewide study of the maternal transcriptome at two time points with and without a crowding stress to discover the maternal molecular changes that lead to the development of winged vs. wingless offspring. We observed significant transcriptional changes in genes associated with odorant binding, neurotransmitter transport, hormonal activity and chromatin remodelling in the maternal transcriptome. We also found that titres of serotonin, dopamine and octopamine were higher in solitary compared to crowded aphids. We use these results to posit a model for how maternal signals inform a developing embryo to be winged or wingless. Our findings add significant insights into the identity of the molecular mechanisms that underlie environmentally induced morph determination and suggest a possible role for biogenic amine regulation in polyphenisms generally.

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Deciphering the Function of Octopaminergic Signaling on Wing Polyphenism of the Pea Aphid <i>Acyrthosiphon pisum</i>.

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Two developmental switch points for the wing polymorphisms in the pea aphid Acyrthosiphon pisum.

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A novel gene <i>REPTOR2</i> activates the autophagic degradation of wing disc in pea aphid.

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iTRAQ-Based Comparative Proteomic Analysis Reveals Molecular Mechanisms Underlying Wing Dimorphism of the Pea Aphid, Acyrthosiphon pisum.

Project description:Wing dimorphism is a widespread phenomenon in insects with an associated trade-off between flight capability and fecundity. Despite the molecular underpinnings of phenotypic plasticity that has already been elucidated, it is still not fully understood. In this study, we focused on the differential proteomics profiles between alate and apterous morphs of the pea aphid, Acyrthosiphon pisum at the fourth instar nymph and adult stages, using isobaric tags for relative and absolute quantitation (iTRAQ) in a proteomic-based approach. A total of 5,116 protein groups were identified and quantified in the three biological replicates, of which 836 were differentially expressed between alate and apterous morphs. A bioinformatics analysis of differentially expressed protein groups (DEPGs) was performed based on gene ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG). KEGG enrichment analysis showed that DEPGs mainly participated in energy metabolism, amino acid biosynthesis and metabolism, and signal sensing and transduction. To verify the reliability of proteomics data, the transcriptional expression of 29 candidates of differentially expressed proteins were analyzed by quantitative real-time PCR (qRT-PCR), showing that 26 genes were consistent with those at proteomic levels. In addition, differentially expressed proteins between winged and wingless morphs that were linked to olfactory sense were investigated. Quantitative real-time PCR revealed the tissue- and morph-biased expression profiles. These results suggested that olfactory sense plays a key role in wing dimorphism of aphids. The comparative proteomic analysis between alate and apterous morphs of the pea aphid provides a novel insight into wing development and dimorphism in aphids and will help facilitate our understanding of these concepts at molecular levels.

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A large genomic insertion containing a duplicated follistatin gene is linked to the pea aphid male wing dimorphism.

Project description:Wing dimorphisms have long served as models for examining the ecological and evolutionary tradeoffs associated with alternative phenotypes. Here, we investigated the genetic cause of the pea aphid (Acyrthosiphon pisum) male wing dimorphism, wherein males exhibit one of two morphologies that differ in correlated traits that include the presence or absence of wings. We mapped this trait difference to a single genomic region and, using third generation, long-read sequencing, we identified a 120 kb insertion in the wingless allele. This insertion includes a duplicated follistatin gene, which is a strong candidate gene in the minimal mapped interval to cause the dimorphism. We found that both alleles were present prior to pea aphid biotype lineage diversification, we estimated that the insertion occurred millions of years ago, and we propose that both alleles have been maintained in the species, likely due to balancing selection.

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A case for a joint strategy of diversified bet hedging and plasticity in the pea aphid wing polyphenism.

Project description:Phenotypic plasticity and diversified bet hedging are strategies for coping with variable environments. Plasticity is favoured when an organism can predict future conditions using environmental cues, while bet hedging is favoured when predictive cues are not available. Theoretical analyses suggest that many organisms should use a mixture of both strategies, because environments often present both scenarios. Here, we examine if the pea aphid wing polyphenism, a well-known case of plasticity, is potentially a mixture of plasticity and bet hedging. In this polyphenism, asexual females produce more winged offspring in crowded conditions, and wingless offspring in uncrowded conditions. We find that pea aphids use plasticity to respond to crowding and we find considerable genetic variation for this response. We further show that individual aphids produce both winged and wingless offspring, consistent with the variability expected in a bet hedging trait. We conclude that the pea aphid wing polyphenism system is probably a mixture of plasticity and bet hedging. Our study adds to a limited list of empirical studies examining mixed strategy usage, and suggests that mixed strategies may be common in dispersal traits.

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Common genome-wide patterns of transcript accumulation underlying the wing polyphenism and polymorphism in the pea aphid

Project description:The pea aphid, Acyrthosiphon pisum, exhibits several environmentally cued polyphenisms, in which discrete, alternative phenotypes are produced. At low density parthenogenetic females produce unwinged female progeny, but at high density females produce progeny that develop with wings. These alternative phenotypes represent a solution to the competing demands of dispersal and reproduction. Males also develop as either winged or unwinged, but these alternatives are determined by a genetic polymorphism. Winged and unwinged males are morphologically less distinct from each other than winged and unwinged females, possibly because males experience fewer trade-offs between dispersal and reproduction. To assess whether shared physiological differences mirror the shared morphological differences that characterize the wing polyphenism and polymorphism, we used a cDNA microarray representing an estimated 10% of the coding genome (1734 genes) to examine differential transcript accumulation between winged and unwinged females and males. We identified several transcripts that differentially accumulate between winged and unwinged morphs in both sexes, the majority of which are involved in energy production. Unexpectedly, the extent of differential transcript accumulation between winged and unwinged morphs was greater for adult males than for adult females. Together, these results suggest not only that similar physiological differences underlie the polyphenism and polymorphism, but that male morphs, like females, are subject to trade-offs between reproduction and dispersal that are reflected in levels of transcript accumulation and possibly genome-wide patterns of gene regulation. These data also provide a baseline for future studies of the molecular and physiological basis of life history trade-offs. Keywords: Transcript levels were compared between winged and unwinged male and female pea aphids, for both nymphs and adults.

2007-06-05 | GSE8008 | GEO

Project description:In aphids there is a fecundity-dispersal trade-off between wingless and winged morphs. Recent research on the molecular mechanism of wing morphs associated with dispersal reveals that insulin receptors in the insulin signaling (IS) pathway regulate alternation of wing morphs in planthoppers. However, little is known about whether genes in the IS pathway are involved in developmental regulation in aphid nymphs with different wing morphs. In this study, we show that expression of the insulin-related peptide 5 gene (Apirp5) affects biochemical composition and embryo development of wingless pea aphids, Acyrthosiphon pisum. After comparing expression levels of major genes in the IS pathway between third instar winged and wingless nymphs, we found that Apirp5 showed higher expression in head and thorax in the wingless nymphs than in the winged nymphs. Although microinjection treatment affects physical performance in aphids, nymphs with RNA interference of Apirp5 had less weight, smaller embryos, and higher carbohydrate and protein contents compared to the control group. Comparison between winged and wingless nymphs showed a similar trend. These results indicate that Apirp5 is involved in embryo development and metabolic regulation in wing dimorphic pea aphid.

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Pea aphid parthenogenetic development

Project description:Transcription profiling of pea aphid embryos developmental stages and of early larval 1 stage

2012-06-30 | E-MTAB-796 | biostudies-arrayexpress