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Early Transcriptional Events Linked to Induction of Diapause Revealed By Poupardin et al. BMC Genomics (2015) 16:720 DOI 10.1186/s12864-015-1907-4 RESEARCH ARTICLE Open Access Early transcriptional events linked to induction of diapause revealed by RNAseq in larvae of drosophilid fly, Chymomyza costata Rodolphe Poupardin1, Konrad Schöttner1, Jaroslava Korbelová1, Jan Provazník1,2, David Doležel1, Dinko Pavlinic3, Vladimír Beneš3 and Vladimír Koštál1* Abstract Background: Diapause is a developmental alternative to directontogenyinmanyinvertebrates.Itsprimary adaptive meaning is to secure survival over unfavourable seasons in a state of developmental arrest usually accompanied by metabolic suppression and enhanced tolerance to environmental stressors. During photoperiodically triggered diapause of insects, the ontogeny is centrally turned off under hormonal control, the molecular details of this transition being poorly understood. Using RNAseq technology, we characterized transcription profiles associated with photoperiodic diapause induction in the larvae of the drosophilid fly Chymomyza costata with the goal of identifying candidate genes and processes linked to upstream regulatory events that eventually lead to a complex phenotypic change. Results: Short day photoperiod triggering diapause was associated to inhibition of 20-hydroxy ecdysone (20-HE) signalling during the photoperiod-sensitive stage of C. costata larval development. The mRNA levels of several key genes involved in 20-HE biosynthesis, perception, and signalling were significantly downregulated under short days. Hormonal change was translated into downregulation of a series of other transcripts with broad influence on gene expression, protein translation, alternative histone marking by methylation and alternative splicing. These changes probably resulted in blockade of direct development and deep restructuring of metabolic pathways indicated by differential expression of genes involved in cell cycle regulation, metabolism, detoxification, redox balance, protection against oxidative stress, cuticle formation and synthesis of larval storage proteins. This highly complex alteration of gene transcription was expressed already during first extended night, within the first four hours after the change of the photoperiodic signal from long days to short days. We validated our RNAseq differential gene expression results in an independent qRT-PCR experiment involving wild-type (photoperiodic) and NPD-mutant (non-photoperiodic) strains of C. costata. Conclusions: Our study revealed several strong candidate genes for follow-up functional studies. Candidate genes code for upstream regulators of a complex change of gene expression, which leads to phenotypic switch from direct ontogeny to larval diapause. Keywords: Fruit fly, Photoperiodism, Development, Dormancy, Gene expression, Cell cycle, Ecdysteroids, Epigenetics factors * Correspondence: [email protected] 1Biology Centre CAS, Institute of Entomology, Branišovská 31, 37005 České Budějovice, Czech Republic Full list of author information is available at the end of the article © 2015 Poupardin et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Poupardin et al. BMC Genomics (2015) 16:720 Page 2 of 19 Background Increasing accessibility of omic technologies and their Diapause is an environmentally programmed and hor- applicability to non-model insects brought an important monally regulated period of dormancy in invertebrates momentum for diapause research [28]. Many authors [1, 2]. Why study diapause? In an attempt to answer used transcriptomics to characterise gene expression this question, Denlinger [3] provides various good ex- changes in response to diapause. Their major motiva- planations. First and foremost, diapause represents a tions were twofold: to describe a holistic picture of the central part of the life-cycle in many species and se- complex diapause syndrome and to reveal specific candi- cures their survival over unfavourable seasons [3, 4]. date genes and processes that critically regulate diapause More generally, diapause offers an excellent possibility transitions. These aims are complicated by the fact that to probe fundamental questions about the regulation different insect species enter diapause in different onto- of organismal development [3]. Environmental seasonal genetic stages (embryos, larvae, pupae and adults), which cues, most often photoperiod, are perceived during a widely differ in their hormonal milieu and tissue com- species-specific sensitive stage and transduced into one of plexity. Although the common phenotypic features of two ontogenetic alternatives: direct development versus diapause (developmental arrest, metabolic suppression, diapause development [5]. During diapause development, environmental stress resistance, etc.) are similar in most the active lifestyle and the ontogenetic processes are tran- species, there may be diverse transcriptional strategies siently (for the harsh season) but dramatically turned off. for producing them [14]. Most previous studies on tran- The cell division cycles in proliferative tissues stop, the scriptomic signatures of insect diapause compared the growth and morphogenesis slow down or cease, and, in nondiapausing insects to diapausing individuals in which adults, the development of gametes and reproduction be- the diapause syndrome was already fully expressed in haviour disappear [6–8]. In contrast, other processes the phase of diapause maintenance [29–39]. In other might be bolstered, such as metabolic pathways linked to studies, the insects were exposed to stimuli known to the building of energy reserves [9, 10], and cellular pro- terminate diapause and their transition from diapause to tective systems to prevent aging [11], oxidative damage post-diapause quiescence and/or the resumption of de- [12], or injury caused by a wide range of environmental velopment was studied [40–43]. Some previous studies stressors linked to harsh seasons [4, 13, 14]. The period of specifically addressed the events during the initiation developmental arrest during diapause is not static but phase of diapause, alternatively called “early” diapause rather represents a dynamic succession of more or less [14, 42, 44–49], and only very few studies focused on the clearly expressed ecophysiological phases of induction, earliest phase of diapause induction. The study by [50], preparation, initiation, maintenance and termination [6]. for instance, detected only a few transcripts that were Despite the indisputable importance of diapause for differentially regulated (4 upregulated, 22 downregu- insect science/applications and its great potential for lated) in the heads of photoperiod-sensitive generation basic research, molecular and physiological regulation of pea aphids, Acyrthosiphon pisum in response to acute of diapause remains mostly unknown [15]. This is par- shortening of daylength, which induces the egg diapause tially caused by the fact that diapause is very weakly in the offspring of after-next generation. In contrast, the expressed in the classic model insect, Drosophila mela- recent study [51] of maternal diapause induction in the nogaster [16]. Nevertheless, it is well established that mosquito Aedes albopictus identified differential expression switching between direct development and diapause is of 2251 genes in response to diapause-inducing short-day controlled by the alteration of hormonal signalling. In photoperiods. Some other papers examined induction- most insects, the decrease or absence of secretion of linked expression in a limited number of genes only. For basic developmental hormones, juvenoids and ecdyster- instance, we [7] previously assessed changes in the relative oids induces diapause [17–19]. Very briefly, these hor- abundances of seven genes coding for cell cycle regulatory mones are synthesized in endocrine glands, corpora factors in the photoperiod-sensitive 3rd instar larvae of allata and prothoracic gland, respectively, which are Chymomyza costata, and [52] studied eight genes related under the control of neuropeptides produced by spe- to small RNA biogenesis in the photoperiod-sensitive 1st cific brain neurons [20, 21], which, in turn, receive instar larvae of the flesh fly, Sarcophaga bullata. However, information about environmental cues from sensory the most important regulatory events during early stages of neurons or light-sensitive cells including, most prob- diapause induction, which decide about the future develop- ably, central circadian clock neurons [22–24]. Recent mental destiny, remained underexplored. discoveries in mosquito, Culex pipiens and fruit fly, D. In this study, we characterize global patterns of gene melanogaster indicate that this transduction pathway expression associated with very early stages of diapause communicates with insuling signalling pathway [25–27] in the larvae of drosophilid fly, Chymomyza costata but the details of this crosstalk only start to emerge and using RNAseq technology. Our main goal was to identify will need verification in
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