Cell cycle arrest as a hallmark of insect diapause: Changes in gene transcription during diapause induction in the drosophilid fly, Chymomyza costata

Košťál, Vladimı́r; Šimůnková, Petra; Kobelková, Alena; Shimada, Koji

doi:10.1016/j.ibmb.2009.10.004

Cited by 52 publications

(40 citation statements)

References 37 publications

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“…The Wnt pathway is one of the short-range, organ-autonomous (paracrine) signaling systems controlling final cell numbers in larval imaginal discs and thereby controlling organ size in the adult (53). Because the suppression of imaginal disc proliferation is a hallmark of diapause in C. costata (54), the Wnt pathway is clearly an important candidate for diapause regulation. However, our custom array represents only nine genes putatively belonging to Wnt pathway in C. costata, limiting any speculations about their role in diapause.…”

Section: Resultsmentioning

confidence: 99%

Conceptual framework of the eco-physiological phases of insect diapause development justified by transcriptomic profiling

Košťál

Štětina

Poupardin

et al. 2017

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

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137

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Insects often overcome unfavorable seasons in a hormonally regulated state of diapause during which their activity ceases, development is arrested, metabolic rate is suppressed, and tolerance of environmental stress is bolstered. Diapausing insects pass through a stereotypic succession of eco-physiological phases termed “diapause development.” The phasing is varied in the literature, and the whole concept is sometimes criticized as being too artificial. Here we present the results of transcriptional profiling using custom microarrays representing 1,042 genes in the drosophilid fly, Chymomyza costata. Fully grown, third-instar larvae programmed for diapause by a photoperiodic (short-day) signal were assayed as they traversed the diapause developmental program. When analyzing the gradual dynamics in the transcriptomic profile, we could readily distinguish distinct diapause developmental phases associated with induction/initiation, maintenance, cold acclimation, and termination by cold or by photoperiodic signal. Accordingly, each phase is characterized by a specific pattern of gene expression, supporting the physiological relevance of the concept of diapause phasing. Further, we have dissected in greater detail the changes in transcript levels of elements of several signaling pathways considered critical for diapause regulation. The phase of diapause termination is associated with enhanced transcript levels in several positive elements stimulating direct development (the 20-hydroxyecdysone pathway: Ecr, Shd, Broad; the Wnt pathway: basket, c-jun) that are countered by up-regulation in some negative elements (the insulin-signaling pathway: Ilp8, PI3k, Akt; the target of rapamycin pathway: Tsc2 and 4EBP; the Wnt pathway: shaggy). We speculate such up-regulations may represent the early steps linked to termination of diapause programming.

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Section: Resultsmentioning

confidence: 99%

Conceptual framework of the eco-physiological phases of insect diapause development justified by transcriptomic profiling

Košťál

Štětina

Poupardin

et al. 2017

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

Self Cite

137

100

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“…We identified five putative target genes related to cell cycle regulation and apoptosis, two pathways typically downregulated during diapause (Hwang et al ., ; Koštál et al ., ; MacRae, ; Poupardin et al ., ). In Ae.…”

Section: Discussionmentioning

confidence: 99%

MicroRNAs are differentially abundant during Aedes albopictus diapause maintenance but not diapause induction

Batz

Goff

Armbruster

2017

Insect Molecular Biology

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Diapause is a programmed dormancy that allows organisms to tolerate predictable periods of unfavorable conditions by temporarily halting development and reducing metabolism. Diapause is widespread among insects and is crucial for allowing organisms to coordinate their growth and reproduction with favorable environmental conditions. While the adaptive significance of diapause is well-understood, the molecular mechanisms underpinning diapause remain unresolved. We performed high-throughput sequencing to investigate the role of microRNAs in the diapause of the Asian tiger mosquito, Aedes albopictus. We first investigate miRNAs in diapause induction by characterizing maternally-provisioned miRNAs in mature oocytes of Ae. albopictus under diapause-inducing and diapause-averting conditions. Second, we investigate miRNAs in diapause maintenance by characterizing miRNAs in diapause and non-diapause pharate larvae. We identified 162 miRNAs, 152 previously known and 10 putatively novel. We identified no differentially abundant miRNAs in mature oocytes and seven differentially abundant miRNAs in pharate larvae. The predicted targets of differentially abundant miRNAs include genes affecting several processes related to diapause maintenance including ecdysone regulation, immune response, lipid metabolism, and regulation of development. Our results suggest that Ae. albopictus does not maternally-provision a unique set of miRNAs during diapause induction but miRNAs are a component of diapause maintenance in this species.

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“…Cell-cycle arrest contributes to developmental arrest in diapausing insects, but its manifestation and regulation during diapause are not well understood [39]. Previous gene expression studies of cell-cycle regulators are consistent with a decrease or halt of cell cycle and DNA replication processes in diapause, which resume once diapause is terminated [39][40][41][42][43].…”

Section: (D) Enriched Functional Categories At 3-day Postovipositionmentioning

confidence: 99%

“…PCNA expression decreases during larval diapause in the fly Chymomyza costata [39], and increases following pupal diapause termination in flesh flies [40] and the apple maggot fly, R. pomonella [43]. In Ae.…”

Section: (D) Enriched Functional Categories At 3-day Postovipositionmentioning

confidence: 99%

Deep sequencing reveals complex mechanisms of diapause preparation in the invasive mosquito, Aedes albopictus

et al. 2013

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Seasonal environments present fundamental physiological challenges to a wide range of insects. Many temperate insects surmount the exigencies of winter by undergoing photoperiodic diapause, in which photoperiod provides a token cue that initiates an alternative developmental programme leading to dormancy. Pre-diapause is a crucial preparatory phase of this process, preceding developmental arrest. However, the regulatory and physiological mechanisms of diapause preparation are largely unknown. Using high-throughput gene expression profiling in the Asian tiger mosquito, Aedes albopictus, we reveal major shifts in endocrine signalling, cell proliferation, metabolism, energy production and cellular structure across pre-diapause development. While some hallmarks of diapause, such as insulin signalling and stress response, were not important at the transcriptional level, two genes, Pepck and PCNA, appear to show diapause-induced transcriptional changes across insect taxa. These processes demonstrate physiological commonalities between Ae. albopictus pre-diapause and diapause strategies across insects, and support the idea of a genetic 'toolkit' for diapause. Observations of gene expression trends from a comparative developmental perspective suggest that individual physiological processes are delayed against a background of a fixed morphological ontogeny. Our results demonstrate how deep sequencing can provide new insights into elusive molecular bases of complex ecological adaptations.

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Cell cycle arrest as a hallmark of insect diapause: Changes in gene transcription during diapause induction in the drosophilid fly, Chymomyza costata

Cited by 52 publications

References 37 publications

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

MicroRNAs are differentially abundant during Aedes albopictus diapause maintenance but not diapause induction

Deep sequencing reveals complex mechanisms of diapause preparation in the invasive mosquito, Aedes albopictus

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