Abstract
Background Aedes albopictus is a vector of increasing public health concern due to its rapid global range expansion and ability to transmit Dengue virus, Chikungunya virus and a wide range of additional arboviruses. Traditional vector control strategies have been largely ineffective against Ae. albopictus and novel approaches are urgently needed. Photoperiodic diapause is a crucial ecological adaptation in a wide range of temperate insects. Therefore, targeting the molecular regulation of photoperiodic diapause or diapause-associated physiological processes could provide the basis of novel approaches to vector control.Methodology/Principal FindingsWe investigated the global transcriptional profiles of diapause induction in Ae. albopictus by performing paired-end RNA-Seq of biologically replicated libraries. We sequenced RNA from whole bodies of adult females reared under diapause-inducing and non-diapause-inducing photoperiods either with or without a blood meal. We constructed a comprehensive transcriptome assembly that incorporated previous assemblies and represents over 14,000 annotated dipteran gene models. Mapping of sequence reads to the transcriptome identified differential expression of 2,251 genes in response to diapause-inducing short-day photoperiods. In non-blood-fed females, potential regulatory elements of diapause induction were transcriptionally up-regulated, including two of the canonical circadian clock genes, timeless and cryptochrome 1. In blood-fed females, genes in metabolic pathways related to energy production and offspring provisioning were differentially expressed under diapause-inducing conditions, including the oxidative phosphorylation pathway and lipid metabolism genes.Conclusions/SignificanceThis study is the first to utilize powerful RNA-Seq technologies to elucidate the transcriptional basis of diapause induction in any insect. We identified candidate genes and pathways regulating diapause induction, including a conserved set of genes that are differentially expressed as part of the diapause program in a diverse group of insects. These genes provide candidates whose diapause-associated function can be further interrogated using functional genomics approaches in Ae. albopictus and other insects.
Highlights
Dengue virus (DENV) and Chikungunya virus (CHIKV) areemerging arboviruses transmitted primarily by the mosquitoes Aedes aegypti and Aedes albopictus
Ae. aegypti has historically been considered the primary vector of both DENV and CHIKV, Ae. albopictus has been implicated as the primary vector in at least five DENV outbreaks between 2001–2010, including one in the temperate location of Croatia [9,10], and Ae. albopictus was the primary vector of the CHIKV outbreak on La Réunion, which coincided with a CHIKV mutation from Alanine to Valine at position 226 of the E1 viral envelope protein which confers increased transmission efficiency of CHIKV by Ae. albopictus [11,12]
Our analysis of differential gene expression proceeded in the following three steps: A) we validated key transcriptional responses to a blood meal under both diapause-inducing and non-diapause-inducing conditions, B) we identified potential regulatory elements during diapause induction by analyzing differential gene expression in females reared under diapauseinducing vs. non-diapause-inducing photoperiods without a blood meal, C) we identified genes and pathways related to maternal provisioning of diapause eggs by analyzing differential gene expression in females reared under diapause-inducing vs. non-diapause-inducing photoperiods with a blood meal
Summary
Dengue virus (DENV) and Chikungunya virus (CHIKV) are (re)emerging arboviruses transmitted primarily by the mosquitoes Aedes aegypti and Aedes albopictus. Levels of CHIKV infection are much lower, a 2005–2006 CHIKV outbreak on La Réunion island in the Indian Ocean infected over 266,000 individuals [3], and was followed by an outbreak in northern Italy in 2007 [4]. This latter event generated considerable concern because it represents the first temperate outbreak of CHIKV, which had previously been restricted to tropical areas. Aedes albopictus is a vector of increasing public health concern due to its rapid global range expansion and ability to transmit Dengue virus, Chikungunya virus and a wide range of additional arboviruses. Targeting the molecular regulation of photoperiodic diapause or diapause-associated physiological processes could provide the basis of novel approaches to vector control
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