Phenotypic Plasticity of the Drosophila Transcriptome

Zhou, Shanshan; Campbell, Terry G.; Stone, Eric A.; Mackay, Trudy F. C.; Anholt, Robert R. H.

doi:10.1371/journal.pgen.1002593

Cited by 103 publications

(129 citation statements)

References 37 publications

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“…The strongest response was to acetal, which yielded a mean RI greater than 0.75, whereas the weakest response was to geranyl acetate, which elicited a mean RI less than 0.1. We note that an earlier study observed a repellent effect of geranyl acetate (8); we do not know the basis of this difference, but repellency has been found to be sensitive to larval age (37) and could also be sensitive to other factors that differed between the two studies (38). Aversive responses to CO 2 are mediated by neurons of another larval organ, the terminal organ, that coexpress Gr21a and Gr63a (2,(39)(40)(41)(42), and it is possible that other unidentified neurons also mediate airborne aversive responses.…”

Section: Discussionmentioning

confidence: 67%

Functional diversity among sensory receptors in a Drosophila olfactory circuit

Mathew

Martelli

Kelley-Swift

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

107

184

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The ability of an animal to detect, discriminate, and respond to odors depends on the function of its olfactory receptor neurons (ORNs), which in turn depends ultimately on odorant receptors. To understand the diverse mechanisms used by an animal in olfactory coding and computation, it is essential to understand the functional diversity of its odor receptors. The larval olfactory system of Drosophila melanogaster contains 21 ORNs and a comparable number of odorant receptors whose properties have been examined in only a limited way. We systematically screened them with a panel of ∼500 odorants, yielding >10,000 receptor-odorant combinations. We identify for each of 19 receptors an odorant that excites it strongly. The responses elicited by each of these odorants are analyzed in detail. The odorants elicited little cross-activation of other receptors at the test concentration; thus, low concentrations of many of these odorants in nature may be signaled by a single ORN. The receptors differed dramatically in sensitivity to their cognate odorants. The responses showed diverse temporal dynamics, with some odorants eliciting supersustained responses. An intriguing question in the field concerns the roles of different ORNs and receptors in driving behavior. We found that the cognate odorants elicited behavioral responses that varied across a broad range. Some odorants elicited strong physiological responses but weak behavioral responses or weak physiological responses but strong behavioral responses.T he olfactory system of the Drosophila larva achieves remarkable function with minimal structure. It detects and responds to spatial and temporal gradients of odorants, transforming chemical information into navigation via an elegant repertoire of head sweeps, runs, and turns (1-3). Its sophisticated function is based on the activities of 21 olfactory receptor neurons (ORNs), which innervate the dorsal organ of the head and send axons to the antennal lobe of the brain (4). The activities of the ORNs are in turn based on the responses of odor receptors (Ors). Thus, to understand the molecular basis of larval olfactory navigation, it is necessary to understand the function of the receptors.ORNs together express 25 members of the Or family of odor receptors and the Orco coreceptor (5-8). In each ORN, an Or and Orco together form a ligand-gated ion channel (9-11). Most ORNs express a single Or, although one ORN coexpresses Or94a and Or94b and another ORN coexpresses Or33b and Or47a (7). The significance of this coexpression remains speculative, but the response profiles of some coexpressed adult Ors are additive (12).The responses of the larval Or repertoire to a limited odorant panel was previously examined in an in vivo expression system known as the empty neuron system (8, 13). With the use of this system, 21 of the larval Ors were found to be functional. However, studies of the larval Or repertoire have been limited not only in the number of odorants examined, but also in their consideration of receptor sensitivity, tempor...

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Section: Discussionmentioning

confidence: 67%

Functional diversity among sensory receptors in a Drosophila olfactory circuit

Mathew

Martelli

Kelley-Swift

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

107

184

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“…Indeed, a substantial fraction of the Drosophila transcriptome is plastic and sensitive to changing environments (48). However, the genetic basis of such plasticity is yet to be determined.…”

Section: Discussionmentioning

confidence: 99%

Genetic basis of transcriptome diversity in Drosophila melanogaster

Huang

Carbone

Magwire

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

127

129

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Understanding how DNA sequence variation is translated into variation for complex phenotypes has remained elusive but is essential for predicting adaptive evolution, for selecting agriculturally important animals and crops, and for personalized medicine. Gene expression may provide a link between variation in DNA sequence and organismal phenotypes, and its abundance can be measured efficiently and accurately. Here we quantified genome-wide variation in gene expression in the sequenced inbred lines of the Drosophila melanogaster Genetic Reference Panel (DGRP), increasing the annotated Drosophila transcriptome by 11%, including thousands of novel transcribed regions (NTRs). We found that 42% of the Drosophila transcriptome is genetically variable in males and females, including the NTRs, and is organized into modules of genetically correlated transcripts. We found that NTRs often were negatively correlated with the expression of protein-coding genes, which we exploited to annotate NTRs functionally. We identified regulatory variants for the mean and variance of gene expression, which have largely independent genetic control. Expression quantitative trait loci (eQTLs) for the mean, but not for the variance, of gene expression were concentrated near genes. Notably, the variance eQTLs often interacted epistatically with local variants in these genes to regulate gene expression. This comprehensive characterization of population-scale diversity of transcriptomes and its genetic basis in the DGRP is critically important for a systems understanding of quantitative trait variation.

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“…Such findings will also show how phenotypic plasticity itself is likely to evolve in the face of rapidly changing environments. To date, we lack descriptions of how phenotypic plasticity is mediated via changes in the transcriptome, epigenome, and proteome (Gilbert 2005;Aubin-Horth and Renn 2009;Ellers and Stuefer 2010;Zhou et al 2012). In part, this may be because behavior is inherently complex, often with an underlying polygenic basis (Bell and Aubin-Horth 2010).…”

Section: Introductionmentioning

confidence: 99%

Genomic responses to the socio-sexual environment in male Drosophila melanogaster exposed to conspecific rivals

Mohorianu

Bretman

Smith

et al. 2017

RNA

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Socio-sexual environments have profound effects on fitness. Local sex ratios can alter the threat of sexual competition, to which males respond via plasticity in reproductive behaviors and ejaculate composition. In Drosophila melanogaster, males detect the presence of conspecific, same-sex mating rivals prior to mating using multiple, redundant sensory cues. Males that respond to rivals gain significant fitness benefits by altering mating duration and ejaculate composition. Here we investigated the underlying genome-wide changes involved. We used RNA-seq to analyze male transcriptomic responses 2, 26, and 50 h after exposure to rivals, a time period that was previously identified as encompassing the major facets of male responses to rivals. The results showed a strong early activation of multiple sensory genes in the head-thorax (HT), prior to the expression of any phenotypic differences. This gene expression response was reduced by 26 h, at the time of maximum phenotypic change, and shut off by 50 h. In the abdomen (A), fewer genes changed in expression and gene expression responses appeared to increase over time. The results also suggested that different sets of functionally equivalent genes might be activated in different replicates. This could represent a mechanism by which robustness is conferred upon highly plastic traits. Overall, our study reveals that mRNA-seq can identify subtle genomic signatures characteristic of flexible behavioral phenotypes.

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Phenotypic Plasticity of the Drosophila Transcriptome

Cited by 103 publications

References 37 publications

Functional diversity among sensory receptors in a Drosophila olfactory circuit

Functional diversity among sensory receptors in a Drosophila olfactory circuit

Genetic basis of transcriptome diversity in Drosophila melanogaster

Genomic responses to the socio-sexual environment in male Drosophila melanogaster exposed to conspecific rivals

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