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Phenotypic plasticity of the Drosophila transcriptome.

ABSTRACT: Phenotypic plasticity is the ability of a single genotype to produce different phenotypes in response to changing environments. We assessed variation in genome-wide gene expression and four fitness-related phenotypes of an outbred Drosophila melanogaster population under 20 different physiological, social, nutritional, chemical, and physical environments; and we compared the phenotypically plastic transcripts to genetically variable transcripts in a single environment. The environmentally sensitive transcriptome consists of two transcript categories, which comprise ?15% of expressed transcripts. Class I transcripts are genetically variable and associated with detoxification, metabolism, proteolysis, heat shock proteins, and transcriptional regulation. Class II transcripts have low genetic variance and show sexually dimorphic expression enriched for reproductive functions. Clustering analysis of Class I transcripts reveals a fragmented modular organization and distinct environmentally responsive transcriptional signatures for the four fitness-related traits. Our analysis suggests that a restricted environmentally responsive segment of the transcriptome preserves the balance between phenotypic plasticity and environmental canalization.

SUBMITTER: Zhou S

PROVIDER: S-EPMC3315458 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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Phenotypic plasticity of the Drosophila transcriptome.

Zhou Shanshan S Campbell Terry G TG Stone Eric A EA Mackay Trudy F C TF Anholt Robert R H RR

PLoS genetics 20120329 3

Phenotypic plasticity is the ability of a single genotype to produce different phenotypes in response to changing environments. We assessed variation in genome-wide gene expression and four fitness-related phenotypes of an outbred Drosophila melanogaster population under 20 different physiological, social, nutritional, chemical, and physical environments; and we compared the phenotypically plastic transcripts to genetically variable transcripts in a single environment. The environmentally sensit ...[more]

PMID: 22479193

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Project description:Phenotypic plasticity, the ability for a single genotype to generate different phenotypes in response to environmental conditions, is biologically ubiquitous, and yet almost nothing is known of the developmental mechanisms that regulate the extent of a plastic response. In particular, it is unclear why some traits or individuals are highly sensitive to an environmental variable while other traits or individuals are less so. Here we elucidate the developmental mechanisms that regulate the expression of a particularly important form of phenotypic plasticity: the effect of developmental nutrition on organ size. In all animals, developmental nutrition is signaled to growing organs via the insulin-signaling pathway. Drosophila organs differ in their size response to developmental nutrition and this reflects differences in organ-specific insulin-sensitivity. We show that this variation in insulin-sensitivity is regulated at the level of the forkhead transcription factor FOXO, a negative growth regulator that is activated when nutrition and insulin signaling are low. Individual organs appear to attenuate growth suppression in response to low nutrition through an organ-specific reduction in FOXO expression, thereby reducing their nutritional plasticity. We show that FOXO expression is necessary to maintain organ-specific differences in nutritional-plasticity and insulin-sensitivity, while organ-autonomous changes in FOXO expression are sufficient to autonomously alter an organ's nutritional-plasticity and insulin-sensitivity. These data identify a gene (FOXO) that modulates a plastic response through variation in its expression. FOXO is recognized as a key player in the response of size, immunity, and longevity to changes in developmental nutrition, stress, and oxygen levels. FOXO may therefore act as a more general regulator of plasticity. These data indicate that the extent of phenotypic plasticity may be modified by changes in the expression of genes involved in signaling environmental information to developmental processes.

Project description:BackgroundAs global climate change and exponential human population growth intensifies pressure on agricultural systems, the need to effectively manage invasive insect pests is becoming increasingly important to global food security. Drosophila suzukii is an invasive pest that drastically expanded its global range in a very short time since 2008, spreading to most areas in North America and many countries in Europe and South America. Preliminary ecological modeling predicted a more restricted distribution and, for this reason, the invasion of D. suzukii to northern temperate regions is especially unexpected. Investigating D. suzukii phenology and seasonal adaptations can lead to a better understanding of the mechanisms through which insects express phenotypic plasticity, which likely enables invasive species to successfully colonize a wide range of environments.ResultsWe describe seasonal phenotypic plasticity in field populations of D. suzukii. Specifically, we observed a trend of higher proportions of flies with the winter morph phenotype, characterized by darker pigmentation and longer wing length, as summer progresses to winter. A laboratory-simulated winter photoperiod and temperature (12:12 L:D and 10 °C) were sufficient to induce the winter morph phenotype in D. suzukii. This winter morph is associated with increased survival at 1 °C when compared to the summer morph, thus explaining the ability of D. suzukii to survive cold winters. We then used RNA sequencing to identify gene expression differences underlying seasonal differences in D. suzukii physiology. Winter morph gene expression is consistent with known mechanisms of cold-hardening such as adjustments to ion transport and up-regulation of carbohydrate metabolism. In addition, transcripts involved in oogenesis and DNA replication were down-regulated in the winter morph, providing the first molecular evidence of a reproductive diapause in D. suzukii.ConclusionsTo date, D. suzukii cold resistance studies suggest that this species cannot overwinter in northern locations, e.g. Canada, even though they are established pests in these regions. Combining physiological investigations with RNA sequencing, we present potential mechanisms by which D. suzukii can overwinter in these regions. This work may contribute to more accurate population models that incorporate seasonal variation in physiological parameters, leading to development of better management strategies.

Project description:Spotted wing drosophila, Drosophila suzukii Matsumura, is a major pest of small fruit worldwide in temperate and subtropical growing regions. In Northern climates, D. suzukii likely overwinters locally under leaf litter and snow pack, but our understanding of the factors affecting thermal susceptibility is limited. While previous investigations of thermal susceptibility in this species have employed conventional static acclimation protocols, we aimed to determine whether gradual cooling, or dynamic acclimation, may extend the limits of known thermal tolerance by more closely approximating naturally occurring shifts in temperature. First, we assessed survival among adult and pupal D. suzukii using static acclimation. Then, we re-assessed survival using a novel dynamic acclimation method. We found that while static acclimation was sufficient to induce cold tolerance, dynamic acclimation significantly improved survival at temperatures as low as -7.5 °C. Following static acclimation, the lower lethal limit of adult D. suzukii was -1.1 °C in winter morphotype (WM) adults compared to 1.7 °C in non-acclimated summer morphotype (SM) adults. Dynamic acclimation reduced the lower limit to -5 °C in SM flies. At the end of our study 50% of WM flies survived 72 h at -7.5 °C. Below 0 °C pupal survival declined significantly regardless of acclimation procedure. However, pupal acclimation improved survival outcomes significantly compared to non-acclimated pupae, suggesting that while juvenile diapause is unlikely, cold hardening likely benefits those flies which may develop into the overwintering WM population. These data suggest that the degree of cold hardening is proportional to the thermal environment, a finding previously unrecognized in this species. Given the economic impact of this pest, these data may have important implications for offseason population monitoring and management. We discuss how phenotypic plasticity may drive geographical range expansion, and the impact of climate change on the spread of this species.

Project description:Phenotypic plasticity is the ability of a genotype to produce contrasting phenotypes in different environments. Although many examples have been described, the responsible mechanisms are poorly understood. In particular, it is not clear how phenotypic plasticity is related to buffering, the maintenance of a constant phenotype against genetic or environmental variation. We investigate here the genetic basis of a particularly well described plastic phenotype: the abdominal pigmentation in female Drosophila melanogaster. Cold temperature induces a dark pigmentation, in particular in posterior segments, while higher temperature has the opposite effect. We show that the homeotic gene Abdominal-B (Abd-B) has a major role in the plasticity of pigmentation in the abdomen. Abd-B plays opposite roles on melanin production through the regulation of several pigmentation enzymes. This makes the control of pigmentation very unstable in the posterior abdomen, and we show that the relative spatio-temporal expression of limiting pigmentation enzymes in this region of the body is thermosensitive. Temperature acts on melanin production by modulating a chromatin regulator network, interacting genetically with the transcription factor bric-à-brac (bab), a target of Abd-B and Hsp83, encoding the chaperone Hsp90. Genetic disruption of this chromatin regulator network increases the effect of temperature and the instability of the pigmentation pattern in the posterior abdomen. Colocalizations on polytene chromosomes suggest that BAB and these chromatin regulators cooperate in the regulation of many targets, including several pigmentation enzymes. We show that they are also involved in sex comb development in males and that genetic destabilization of this network is also strongly modulated by temperature for this phenotype. Thus, we propose that phenotypic plasticity of pigmentation is a side effect reflecting a global impact of temperature on epigenetic mechanisms. Furthermore, the thermosensitivity of this network may be related to the high evolvability of several secondary sexual characters in the genus Drosophila.

Project description:Phenotypic plasticity is the ability of a given genotype to produce different phenotypes in response to distinct environmental conditions. Phenotypic plasticity can be adaptive. Furthermore, it is thought to facilitate evolution. Although phenotypic plasticity is a widespread phenomenon, its molecular mechanisms are only beginning to be unravelled. Environmental conditions can affect gene expression through modification of chromatin structure, mainly via histone modifications, nucleosome remodelling or DNA methylation, suggesting that phenotypic plasticity might partly be due to chromatin plasticity. As a model of phenotypic plasticity, we study abdominal pigmentation of Drosophila melanogaster females, which is temperature sensitive. Abdominal pigmentation is indeed darker in females grown at 18°C than at 29°C. This phenomenon is thought to be adaptive as the dark pigmentation produced at lower temperature increases body temperature. We show here that temperature modulates the expression of tan (t), a pigmentation gene involved in melanin production. t is expressed 7 times more at 18°C than at 29°C in female abdominal epidermis. Genetic experiments show that modulation of t expression by temperature is essential for female abdominal pigmentation plasticity. Temperature modulates the activity of an enhancer of t without modifying compaction of its chromatin or level of the active histone mark H3K27ac. By contrast, the active mark H3K4me3 on the t promoter is strongly modulated by temperature. The H3K4 methyl-transferase involved in this process is likely Trithorax, as we show that it regulates t expression and the H3K4me3 level on the t promoter and also participates in female pigmentation and its plasticity. Interestingly, t was previously shown to be involved in inter-individual variation of female abdominal pigmentation in Drosophila melanogaster, and in abdominal pigmentation divergence between Drosophila species. Sensitivity of t expression to environmental conditions might therefore give more substrate for selection, explaining why this gene has frequently been involved in evolution of pigmentation.

Project description:BackgroundInsect females undergo a huge transition in energy homeostasis after mating to compensate for nutrient investment during reproduction. To manage with this shift in metabolism, mated females experience extensive morphological, behavioral and physiological changes, including increased food intake and altered digestive processes. However, the mechanisms by which the digestive system responds to mating in females remain barely characterized. Here we performed transcriptomic analysis of the main digestive organ, the midgut, to investigate how gene expression varies with female mating status in Drosophila suzukii, a destructive and invasive soft fruit pest.ResultsWe sequenced 15,275 unique genes with an average length of 1,467 bp. In total, 652 differentially expressed genes (DEGs) were detected between virgin and mated D. suzukii female midgut libraries. The DEGs were functionally annotated utilizing the GO and KEGG pathway annotation methods. Our results showed that the major GO terms associated with the DEGs from the virgin versus mated female midgut were largely appointed to the metabolic process, response to stimulus and immune system process. We obtained a mass of protein and lipid metabolism genes which were up-regulated and carbohydrate metabolism and immune-related genes which were down-regulated at different time points after mating in female midgut by qRT-PCR. These changes in metabolism and immunity may help supply the female with the nutrients and energy required to sustain egg production.ConclusionOur study characterizes the transcriptional mechanisms driven by mating in the D. suzukii female midgut. Identification and characterization of the DEGs between virgin and mated females midgut will not only be crucial to better understand molecular research related to intestine plasticity during reproduction, but may also provide abundant target genes for the development of effective and ecofriendly pest control strategies against this economically important species.

Dataset Information

Phenotypic plasticity of the Drosophila transcriptome.

Publications

Phenotypic plasticity of the Drosophila transcriptome.

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