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. 2017 Feb 7;114(6):1419-1423.
doi: 10.1073/pnas.1617640114. Epub 2017 Jan 23.

Ecdysone Signaling Underlies the Pea Aphid Transgenerational Wing Polyphenism

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Free PMC article

Ecdysone Signaling Underlies the Pea Aphid Transgenerational Wing Polyphenism

Neetha Nanoth Vellichirammal et al. Proc Natl Acad Sci U S A. .
Free PMC article

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.

Keywords: Acyrthosiphon pisum; ecdysone signaling; pea aphid; phenotypic plasticity; wing polyphenism.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. S1.
Fig. S1.
Expression of ecdysone-associated genes correlates with offspring phenotypes. Genes associated with key aspects of 20-OH ecdysone (20E) synthesis and signaling are shown. Gene names in red are those that are at significantly higher levels in wingless offspring producing females, blue are those that are at higher levels in winged offspring producing females, and gray genes are those that were not differentially expressed. βFtz-f1, fushi tarazu 1; BR-C, broad-complex core protein isoform; DARK, apoptotic protease-activating factor 1; Dib, disembodied; DRICE = caspase-1; EcR, ecdysone receptor; EH Paralog 1&2, eclosion hormone paralog1&2; ISWI, ISWI chromatin remodeling complex; Phm, phantom; PTSP, prothoracicostatic peptide; Sad, shadow; Shd, shade; Spo, spook; Spot, Spookiest; Usp, ultraspiracle.
Fig. 1.
Fig. 1.
The addition of ecdysone causes the production of fewer winged offspring, whereas interference with ecdysone receptor activity causes the production of more winged offspring. (A) Adult, wingless aphids were fed on artificial media containing 20E or control media without 20E (n = 18 sets of three aphids for the treatment, n = 19 for the control), or (B) were injected with methoxyfenozide dissolved in acetone or acetone only (n = 20 sets of three aphids for the treatment, n = 19 for the control). (C) Adult, wingless aphids were injected with cucurbitacin B dissolved in Ringer’s solution or a Ringer’s solution control (n = 15 sets of three aphids each for treatment and control), or (D) with dsRNA against EcR or EcR compared with control aphids (n = 15 sets of three aphids each for treatment and control). Each data point is the percentage of winged offspring produced by sets of three aphids. Boxes show the interquartile range, and the line is the median value of each group. Black circles are outliers. Significant differences between treatments are represented by asterisks: P < 0.10; *P < 0.05; ***P < 0.001.
Fig. S2.
Fig. S2.
Injection with double-stranded RNA against EcR (dsEcR) results in lower relative expression of EcR compared with control aphids (dslacZ). Data shown are the relative expression levels of Ecr in dsEcr and dslacZ injected aphids (n = 5 sets of three aphids each for treatment and control; each data point consists of RNA collected from three injected aphids). Boxes are the interquartile range, and the line is the median value of each group. *P < 0.05.
Fig. 2.
Fig. 2.
Summary of ecdysone signaling manipulation experiments. All treatments, indicated along the top, were applied to adult wingless females. The relative effect of each treatment (i.e., the shift in the median of the experimental group relative to the control) is represented by the width of arrows shown along the bottom, and the direction of morph shift in the form of the offspring phenotypes. Arrows correspond to the treatments, coded by different colors. Treatments that manipulated ecdysone signaling in a similar manner are represented within each dotted box.

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