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Conceptual Framework of the Eco-Physiological Phases of Insect Diapause Development Justified by Transcriptomic Profiling

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Conceptual Framework of the Eco-Physiological Phases of Insect Diapause Development Justified by Transcriptomic Profiling Conceptual framework of the eco-physiological phases of insect diapause development justified by transcriptomic profiling Vladimír Koštála,1, Tomáš St etina a,b, Rodolphe Poupardina,2, Jaroslava Korbelováa, and Alexander William Bruceb aBiology Centre, Institute of Entomology, Academy of Sciences of the Czech Republic, 37005 Budweis, Czech Republic; and bFaculty of Science, University of South Bohemia, 37005 Budweis, Czech Republic Edited by David L. Denlinger, Ohio State University, Columbus, OH, and approved June 29, 2017 (received for review May 3, 2017) Insects often overcome unfavorable seasons in a hormonally ecdysteroids (8, 9). However, any further generalizations about regulated state of diapause during which their activity ceases, insect diapause are strongly complicated by three facts. First, the development is arrested, metabolic rate is suppressed, and toler- insect taxon is enormously rich and diverse. It is believed that ance of environmental stress is bolstered. Diapausing insects pass diapause responses evolve polyphyletically and very rapidly in through a stereotypic succession of eco-physiological phases termed different insect lineages as they encounter diverse environmental “diapause development.” The phasing is varied in the literature, and adversity (10–13). Second, different insect species enter diapause the whole concept is sometimes criticized as being too artificial. in different ontogenetic stages that differ widely in the com- Here we present the results of transcriptional profiling using custom plexity of body architecture and physiology (9). Third, different microarrays representing 1,042 genes in the drosophilid fly, Chymo- insect species enter diapause under various environmental con- myza costata. Fully grown, third-instar larvae programmed for dia- texts. Thus, hibernation is widespread in polar and temperate pause by a photoperiodic (short-day) signal were assayed as they regions, aestivation often occurs in Mediterranean and other dry climate zones, and tropical diapauses may respond to seasonality traversed the diapause developmental program. When analyzing – the gradual dynamics in the transcriptomic profile, we could readily primarily in biotic interactions (14 16). Despite this diversity in distinguish distinct diapause developmental phases associated with insect diapause responses, several phenotypic features occur al- induction/initiation, maintenance, cold acclimation, and termination most ubiquitously: developmental arrest, metabolic suppression, and environmental stress resistance (17), so that some authors by cold or by photoperiodic signal. Accordingly, each phase is char- have proposed the notion of a common genetic “toolkit” for acterized by a specific pattern of gene expression, supporting the diapause (18, 19). According to this scheme, some common physiological relevance of the concept of diapause phasing. Further, diapause-induced gene-expression profiles might be shared we have dissected in greater detail the changes in transcript levels across insect (or even across invertebrate) taxa. However, when of elements of several signaling pathways considered critical for comparing transcriptional profiles linked to dormancy in three diapause regulation. The phase of diapause termination is associ- invertebrate species (flesh fly, fruit fly, and nematode), Ragland ated with enhanced transcript levels in several positive elements et al. (20) found little support for the genetic toolkit hypothesis stimulating direct development (the 20-hydroxyecdysone pathway: and concluded that there may be many transcriptional strate- Ecr, Shd, Broad; the Wnt pathway: basket, c-jun) that are countered gies for producing physiologically similar dormancy responses. by up-regulation in some negative elements (the insulin-signaling One additional generalization on insect diapause posits that pathway: Ilp8, PI3k, Akt; the target of rapamycin pathway: Tsc2 and diapausing insects, although developmentally arrested, pass through 4EBP; the Wnt pathway: shaggy). We speculate such up-regulations a stereotypic succession of eco-physiological phases called may represent the early steps linked to termination of diapause programming. Significance insects | diapause | development | transcriptomics | microarrays Here we reassess the conceptual framework of insect diapause ’ as a dynamic succession of endogenously and exogenously he obligatory diapause is a fixed component of the insect s driven changes in physiology (“physiogenesis”)byassayingthe Tontogenetic program, whereas the facultative diapause rep- gradual dynamics in the transcriptome as insects traverse the resents an optional alternative pathway to direct ontogeny. diapause developmental program. We show the objectivity and Facultative diapause (herein referred to as “diapause”) is a state eco-physiological relevance of the different phases of diapause of environmentally programmed and centrally regulated devel- opmental arrest, usually accompanied by metabolic suppression, development by describing unique transcriptional profiles in which secures survival over unfavorable seasons and synchro- each phase. Accordingly, the concept should serve future re- nizes the insect life cycle to the seasonality of abiotic environ- searchers as a general platform for the unification of timing “ ” mental factors and biotic interactions (1–5). An improved scales and the interpretation of various -omics data obtained knowledge of diapause is essential for understanding insect life in diverse insect species encountering different ecological situ- cycles and for the development of management strategies for ations. We argue such standardized phasing of diapause devel- economically important insect pests (6) and accurate predictions opment is critical for further molecular dissection of the mechanistic of insect populations’ responses to climate change (7). basis of insect diapause. At a specific sensitive stage, insects perceive environmental token stimuli (any stimulus that signals the upcoming seasonal Author contributions: V.K. designed research; T.S., R.P., and J.K. performed research; change in advance, most often the photoperiod) that reliably A.W.B. contributed new reagents/analytic tools; V.K. and R.P. analyzed data; and V.K. wrote the paper. mark seasonal time (calendar) and switch from direct develop- ment to the diapause pathway, typically long before the adverse The authors declare no conflict of interest. period arrives. (Note: in this paper, “direct development” refers This article is a PNAS Direct Submission. to an ontogenetic pathway without intervening diapause.) It is 1To whom correspondence should be addressed. Email: [email protected]. well established that switching between direct development 2Present address: Institut für Populationsgenetik, Vetmeduni Vienna, 1210 Vienna, Austria. and diapause is controlled by the decrease or absence of sig- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. naling of the basic developmental hormones, juvenoids and/or 1073/pnas.1707281114/-/DCSupplemental. 8532–8537 | PNAS | August 8, 2017 | vol. 114 | no. 32 www.pnas.org/cgi/doi/10.1073/pnas.1707281114 Downloaded by guest on September 25, 2021 “diapause development” or “physiogenesis” (1). This general- (PCA) (Fig. 1A). Early third-instar larvae (nd1 and id1) are most ization also has caused controversies in the past (4, 21, 22); in sensitive to photoperiodic signal. The nd1 larvae will continue in particular, the separation of and naming of the successive phases direct development, whereas the id1 larvae are destined to remains unstandardized and is sometimes criticized as artificial diapause development (24). We found 79 genes differentially (for a review, see ref. 23). expressed (DE) in the id1 and nd1 samples (Dataset S1,Excel We used custom microarrays to compare gene-expression sheet id1 vs. nd1), comprising 7.7% of the total number of profiles for 1,042 mRNA transcripts in the larvae of the droso- 1,042 sequences printed on a custom microarray. In an earlier philid fly Chymomyza costata. The genes were arbitrarily selected study (25) we compared the transcriptional profiles of similar to cover broadly the major structures and processes known or larvae (at the same ontogenetic stages) using RNA sequencing suggested to be involved in insect diapause expression: biological (RNA-seq) and found 1,313 DE sequences, comprising 6.2% of clocks, hormones and signaling cascades, regulators of the cell a total 21,327 sequences. Further, the identity of DE sequences division cycle, energy metabolism and detoxification, response to showed good overlap between two studies: 37 of 45 (82.2%) up- temperature stimulus and cryoprotection, cytoskeleton, biologi- regulated DE sequences in this study were also up-regulated in cal membranes, and transport systems. In addition to comparing the earlier study; similarly, 26 of 34 (76.5%) down-regulated diapause and nondiapause animals, we focused mainly on compar- DE sequences in this study were also down-regulated in the ing the successive eco-physiological phases of diapause develop- earlier study (with a 1.5-fold difference as a threshold for up- or ment, namely, induction, initiation, maintenance, and termination down-regulation). In the RNA-seq study, the short-day–reared, (sensu ref. 23). We also distinguished between the natural (horotelic, diapause-destined larvae (designated as “id1” in this study) sensu ref. 2) and the unnatural (tachytelic, sensu ref. 2) mecha- showed down-regulation
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