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1.
BMC Biol ; 22(1): 206, 2024 Sep 13.
Article in English | MEDLINE | ID: mdl-39272107

ABSTRACT

BACKGROUND: Diapause, a pivotal phase in the insect life cycle, enables survival during harsh environmental conditions. Unraveling the gene expression profiles of the diapause process helps uncover the molecular mechanisms that underlying diapause, which is crucial for understanding physiological adaptations. In this study, we utilize RNA-seq and Ribo-seq data to examine differentially expressed genes (DEGs) and translational efficiency during diapause of Asian corn borer (Ostrinia furnacalis, ACB). RESULTS: Our results unveil genes classified as "forwarded", "exclusive", "intensified", or "buffered" during diapause, shedding light on their transcription and translation regulation patterns. Furthermore, we explore the landscape of lncRNAs (long non-coding RNAs) during diapause and identify differentially expressed lncRNAs, suggesting their roles in diapause regulation. Comparative analysis of different types of diapause in insects uncovers shared and unique KEGG pathways. While shared pathways highlight energy balance, exclusive pathways in the ACB larvae indicate insect-specific adaptations related to nutrient utilization and stress response. Interestingly, our study also reveals dynamic changes in the HSP70 gene family and proteasome pathway during diapause. Manipulating HSP protein levels and proteasome pathway by HSP activator or inhibitor and proteasome inhibitor affects diapause, indicating their vital role in the process. CONCLUSIONS: In summary, these findings enhance our knowledge of how insects navigate challenging conditions through intricate molecular mechanisms.


Subject(s)
Diapause, Insect , Moths , Animals , Moths/physiology , Moths/genetics , Diapause, Insect/physiology , Diapause, Insect/genetics , Transcriptome , Protein Biosynthesis , Larva/growth & development , Larva/physiology , Larva/genetics , Diapause/genetics , Diapause/physiology , Genome, Insect , Transcription, Genetic
2.
Proc Natl Acad Sci U S A ; 121(40): e2405391121, 2024 Oct.
Article in English | MEDLINE | ID: mdl-39316052

ABSTRACT

Decisions made over long time scales, such as life cycle decisions, require coordinated interplay between sensory perception and sustained gene expression. The Caenorhabditis elegans dauer (or diapause) exit developmental decision requires sensory integration of population density and food availability to induce an all-or-nothing organismal-wide response, but the mechanism by which this occurs remains unknown. Here, we demonstrate how the Amphid Single Cilium J (ASJ) chemosensory neurons, known to be critical for dauer exit, perform sensory integration at both the levels of gene expression and calcium activity. In response to favorable conditions, dauers rapidly produce and secrete the dauer exit-promoting insulin-like peptide INS-6. Expression of ins-6 in the ASJ neurons integrates population density and food level and can reflect decision commitment since dauers committed to exiting have higher ins-6 expression levels than those of noncommitted dauers. Calcium imaging in dauers reveals that the ASJ neurons are activated by food, and this activity is suppressed by pheromone, indicating that sensory integration also occurs at the level of calcium transients. We find that ins-6 expression in the ASJ neurons depends on neuronal activity in the ASJs, cGMP signaling, and the pheromone components ascr#8 and ascr#2. We propose a model in which decision commitment to exit the dauer state involves an autoregulatory feedback loop in the ASJ neurons that promotes high INS-6 production and secretion. These results collectively demonstrate how insulin-like peptide signaling helps animals compute long-term decisions by bridging sensory perception to decision execution.


Subject(s)
Caenorhabditis elegans , Insulin , Signal Transduction , Animals , Caenorhabditis elegans/metabolism , Caenorhabditis elegans/physiology , Insulin/metabolism , Diapause/physiology , Caenorhabditis elegans Proteins/metabolism , Caenorhabditis elegans Proteins/genetics , Calcium/metabolism , Population Density , Chemoreceptor Cells/metabolism
3.
Proc Natl Acad Sci U S A ; 121(36): e2407057121, 2024 Sep 03.
Article in English | MEDLINE | ID: mdl-39196619

ABSTRACT

Winter diapause in insects is commonly terminated through cold exposure, which, like vernalization in plants, prevents development before spring arrives. Currently, quantitative understanding of the temperature dependence of diapause termination is limited, likely because diapause phenotypes are generally cryptic to human eyes. We introduce a methodology to tackle this challenge. By consecutively moving butterfly pupae of the species Pieris napi from several different cold conditions to 20 °C, we show that diapause termination proceeds as a temperature-dependent rate process, with maximal rates at relatively cold temperatures and low rates at warm and extremely cold temperatures. Further, we show that the resulting thermal reaction norm can predict P. napi diapause termination timing under variable temperatures. Last, we show that once diapause is terminated in P. napi, subsequent development follows a typical thermal performance curve, with a maximal development rate at around 31 °C and a minimum at around 2 °C. The sequence of these thermally distinct processes (diapause termination and postdiapause development) facilitates synchronous spring eclosion in nature; cold microclimates where diapause progresses quickly do not promote fast postdiapause development, allowing individuals in warmer winter microclimates to catch up, and vice versa. The unveiling of diapause termination as one temperature-dependent rate process among others promotes a parsimonious, quantitative, and predictive model, wherein winter diapause functions both as an adaptation against premature development during fall and winter and for synchrony in spring.


Subject(s)
Butterflies , Seasons , Temperature , Butterflies/physiology , Animals , Diapause, Insect/physiology , Cold Temperature , Pupa/growth & development , Pupa/physiology , Models, Biological , Diapause/physiology
4.
Genes (Basel) ; 15(8)2024 Aug 16.
Article in English | MEDLINE | ID: mdl-39202442

ABSTRACT

Embryonic diapause is a common evolutionary adaptation observed across a wide range of organisms. Artemia is one of the classic animal models for diapause research. The current studies of Artemia diapause mainly focus on the induction and maintenance of the embryonic diapause, with little research on the molecular regulatory mechanism of Artemia embryonic reactivation. The first 5 h after embryonic diapause breaking has been proved to be most important for embryonic reactivation in Artemia. In this work, two high-throughput sequencing methods, ATAC-seq and RNA-seq, were integrated to study the signal regulation process in embryonic reactivation of Artemia at 5 h after diapause breaking. Through the GO and KEGG enrichment analysis of the high-throughput datasets, it was showed that after 5 h of diapause breaking, the metabolism and regulation of Artemia cyst were quite active. Several signal transduction pathways were identified in the embryonic reactivation process, such as G-protein-coupled receptor (GPCR) signaling pathway, cell surface receptor signaling pathway, hormone-mediated signaling pathway, Wnt, Notch, mTOR signaling pathways, etc. It indicates that embryonic reactivation is a complex process regulated by multiple signaling pathways. With the further protein structure analysis and RT-qPCR verification, 11 GPCR genes were identified, in which 5 genes function in the embryonic reactivation stage and the other 6 genes contribute to the diapause stage. The results of this work reveal the signal transduction pathways and GPCRs involved in the embryonic reactivation process of Artemia cysts. These findings offer significant clues for in-depth research on the signal regulatory mechanisms of the embryonic reactivation process and valuable insights into the mechanism of animal embryonic diapause.


Subject(s)
Artemia , Diapause , Signal Transduction , Animals , Artemia/genetics , Artemia/embryology , Signal Transduction/genetics , Diapause/genetics , Gene Expression Regulation, Developmental , RNA-Seq/methods , Embryo, Nonmammalian/metabolism , High-Throughput Nucleotide Sequencing/methods , Embryonic Development/genetics
5.
Cell Stem Cell ; 31(9): 1262-1279.e8, 2024 Sep 05.
Article in English | MEDLINE | ID: mdl-39047740

ABSTRACT

Embryonic diapause is a reproductive adaptation that enables some mammalian species to halt the otherwise continuous pace of embryonic development. In this dormant state, the embryo exploits poorly understood regulatory mechanisms to preserve its developmental potential for prolonged periods of time. Here, using mouse embryos and single-cell RNA sequencing, we molecularly defined embryonic diapause at single-cell resolution, revealing transcriptional dynamics while the embryo seemingly resides in a state of suspended animation. Additionally, we found that the dormant pluripotent cells rely on integrin receptors to sense their microenvironment and preserve their viability via Yap/Taz-mediated prosurvival signaling.


Subject(s)
Adaptor Proteins, Signal Transducing , Embryo, Mammalian , Integrins , Signal Transduction , Single-Cell Analysis , YAP-Signaling Proteins , Animals , Mice , Adaptor Proteins, Signal Transducing/metabolism , Adaptor Proteins, Signal Transducing/genetics , Cell Survival , Diapause , Embryo, Mammalian/metabolism , Embryonic Development/genetics , Gene Expression Regulation, Developmental , Integrins/metabolism , Transcription Factors/metabolism , Transcription Factors/genetics , Transcription, Genetic , Transcriptional Coactivator with PDZ-Binding Motif Proteins , YAP-Signaling Proteins/metabolism
6.
Annu Rev Cell Dev Biol ; 40(1): 25-49, 2024 Oct.
Article in English | MEDLINE | ID: mdl-38985838

ABSTRACT

Life on Earth has been through numerous challenges over eons and, one way or another, has always triumphed. From mass extinctions to more daily plights to find food, unpredictability is everywhere. The adaptability of life-forms to ever-changing environments is the key that confers life's robustness. Adaptability has become synonymous with Darwinian evolution mediated by heritable genetic changes. The extreme gene-centric view, while being of central significance, at times has clouded our appreciation of the cell as a self-regulating entity informed of, and informing, the genetic data. An essential element that powers adaptability is the ability to regulate cell growth. In this review, we provide an extensive overview of growth regulation spanning species, tissues, and regulatory mechanisms. We aim to highlight the commonalities, as well as differences, of these phenomena and their molecular regulators. Finally, we curate open questions and areas for further exploration.


Subject(s)
Diapause , Animals , Humans , Diapause/genetics
7.
Nat Commun ; 15(1): 5936, 2024 Jul 15.
Article in English | MEDLINE | ID: mdl-39009560

ABSTRACT

Jellyfish exhibit innovative swimming patterns that contribute to exploring the origins of animal locomotion. However, the genetic and cellular basis of these patterns remains unclear. Herein, we generated chromosome-level genome assemblies of two jellyfish species, Turritopsis rubra and Aurelia coerulea, which exhibit straight and free-swimming patterns, respectively. We observe positive selection of numerous genes involved in statolith formation, hair cell ciliogenesis, ciliary motility, and motor neuron function. The lineage-specific absence of otolith morphogenesis- and ciliary movement-related genes in T. rubra may be associated with homeostatic structural statocyst loss and straight swimming pattern. Notably, single-cell transcriptomic analyses covering key developmental stages reveal the enrichment of diapause-related genes in the cyst during reverse development, suggesting that the sustained diapause state favours the development of new polyps under favourable conditions. This study highlights the complex relationship between genetics, locomotion patterns and survival strategies in jellyfish, thereby providing valuable insights into the evolutionary lineages of movement and adaptation in the animal kingdom.


Subject(s)
Scyphozoa , Single-Cell Analysis , Swimming , Animals , Scyphozoa/genetics , Scyphozoa/physiology , Diapause/genetics , Genomics/methods , Genome/genetics , Transcriptome , Gene Expression Profiling
8.
Insect Biochem Mol Biol ; 172: 104153, 2024 Sep.
Article in English | MEDLINE | ID: mdl-38964485

ABSTRACT

Most insects enter diapause, a state of physiological dormancy crucial for enduring harsh seasons, with photoperiod serving as the primary cue for its induction, ensuring proper seasonal timing of the process. Although the involvement of the circadian clock in the photoperiodic time measurement has been demonstrated through knockdown or knockout of clock genes, the involvement of clock gene cryptochrome 1 (cry1), which functions as a photoreceptor implicated in photoentrainment of the circadian clock across various insect species, remains unclear. In bivoltine strains of the silkworm, Bombyx mori, embryonic diapause is maternally controlled and affected by environmental conditions experienced by mother moths during embryonic and larval stages. Previous research highlighted the role of core clock genes, including period (per), timeless (tim), Clock (Clk) and cycle (cyc), in photoperiodic diapause induction in B. mori. In this study, we focused on the involvement of cry1 gene in B. mori photoperiodism. Phylogenetic analysis and conserved domain identification confirmed the presence of both Drosophila-type cry (cry1) and mammalian-type cry (cry2) genes in the B. mori genome, akin to other lepidopterans. Temporal expression analysis revealed higher cry1 gene expression during the photophase and lower expression during the scotophase, with knockouts of core clock genes (per, tim, Clk and cyc) disrupting this temporal expression pattern. Using CRISPR/Cas9-mediated genome editing, we established a cry1 knockout strain in p50T, a bivoltine strain exhibiting clear photoperiodism during both embryonic and larval stages. Although the wild-type strain displayed circadian rhythm in eclosion under continuous darkness, the cry1 knockout strain exhibited arrhythmic eclosion, implicating B. mori cry1 in the circadian clock feedback loop governing behavior rhythms. Females of the cry1 knockout strain failed to control photoperiodic diapause induction during both embryonic and larval stages, mirroring the diapause phenotype of the wild-type individuals reared under constant darkness, indicating that B. mori CRY1 contributes to photoperiodic time measurement as a photoreceptor. Furthermore, photoperiodic diapause induction during the larval stage was abolished in a cry1/tim double-knockout strain, suggesting that photic information received by CRY1 is relayed to the circadian clock. Overall, this study represents the first evidence of cry1 involvement in insect photoperiodism, specifically in diapause induction.


Subject(s)
Bombyx , Circadian Rhythm , Cryptochromes , Diapause, Insect , Photoperiod , Animals , Cryptochromes/genetics , Cryptochromes/metabolism , Bombyx/genetics , Bombyx/physiology , Bombyx/metabolism , Bombyx/growth & development , Insect Proteins/genetics , Insect Proteins/metabolism , Larva/growth & development , Larva/genetics , Larva/metabolism , Phylogeny , Diapause/genetics , Gene Knockout Techniques , Circadian Clocks/genetics
9.
Nat Commun ; 15(1): 5793, 2024 Jul 10.
Article in English | MEDLINE | ID: mdl-38987256

ABSTRACT

Temperature is a critical environmental cue that controls the development and lifespan of many animal species; however, mechanisms underlying low-temperature adaptation are poorly understood. Here, we describe cold-inducible diapause (CID), another type of diapause induced by low temperatures in Caenorhabditis elegans. A premature stop codon in heat shock factor 1 (hsf-1) triggers entry into CID at 9 °C, whereas wild-type animals enter CID at 4 °C. Furthermore, both wild-type and hsf-1(sy441) mutant animals undergoing CID can survive for weeks, and resume growth at 20 °C. Using epistasis analysis, we demonstrate that neural signalling pathways, namely tyraminergic and neuromedin U signalling, regulate entry into CID of the hsf-1 mutant. Overexpression of anti-ageing genes, such as hsf-1, XBP1/xbp-1, FOXO/daf-16, Nrf2/skn-1, and TFEB/hlh-30, also inhibits CID entry of the hsf-1 mutant. Based on these findings, we hypothesise that regulators of the hsf-1 mutant CID may impact longevity, and successfully isolate 16 long-lived mutants among 49 non-CID mutants via genetic screening. Furthermore, we demonstrate that the nonsense mutation of MED23/sur-2 prevents CID entry of the hsf-1(sy441) mutant and extends lifespan. Thus, CID is a powerful model to investigate neural networks involving cold acclimation and to explore new ageing mechanisms.


Subject(s)
Caenorhabditis elegans Proteins , Caenorhabditis elegans , Cold Temperature , DNA-Binding Proteins , Diapause , Longevity , Transcription Factors , Animals , Caenorhabditis elegans/genetics , Caenorhabditis elegans/physiology , Caenorhabditis elegans Proteins/genetics , Caenorhabditis elegans Proteins/metabolism , Transcription Factors/metabolism , Transcription Factors/genetics , Diapause/genetics , Diapause/physiology , Longevity/genetics , DNA-Binding Proteins/genetics , DNA-Binding Proteins/metabolism , Mutation , Signal Transduction , Forkhead Transcription Factors/metabolism , Forkhead Transcription Factors/genetics , Codon, Nonsense/genetics , Neuropeptides/metabolism , Neuropeptides/genetics , Carrier Proteins , Basic Helix-Loop-Helix Transcription Factors
10.
Mol Ecol ; 33(13): e17425, 2024 Jul.
Article in English | MEDLINE | ID: mdl-38847383

ABSTRACT

Annual rhythms are observed in living organisms with numerous ecological implications. In the zooplanktonic copepod Calanus finmarchicus, such rhythms are crucial regarding its phenology, body lipid accumulation, and global carbon storage. Climate change drives annual biological rhythms out of phase with the prevailing environmental conditions with yet unknown but potentially catastrophic consequences. However, the molecular dynamics underlying phenology are still poorly described. In a rhythmic analysis of C. finmarchicus annual gene expression, results reveal that more than 90% of the transcriptome shows significant annual rhythms, with abrupt and dramatic upheaval between the active and diapause life cycle states. This work explores the implication of the circadian clock in the annual timing, which may control epigenetic mechanisms to profoundly modulate gene expression in response to calendar time. Results also suggest an increased light sensitivity during diapause that would ensure the photoperiodic entrainment of the endogenous annual clock.


Subject(s)
Circadian Clocks , Copepoda , Diapause , Transcriptome , Animals , Copepoda/genetics , Copepoda/physiology , Diapause/genetics , Circadian Clocks/genetics , Photoperiod , Seasons , Climate Change , Zooplankton/genetics , Circadian Rhythm/genetics
11.
Genome Res ; 34(5): 725-739, 2024 06 25.
Article in English | MEDLINE | ID: mdl-38866549

ABSTRACT

Diapause represents a crucial adaptive strategy used by insects to cope with changing environmental conditions. In North China, the Asian corn borer (Ostrinia furnacalis) enters a winter larval diapause stage. Although there is growing evidence implicating epigenetic mechanisms in diapause regulation, it remains unclear whether dynamic genome-wide profiles of epigenetic modifications exist during this process. By investigating multiple histone modifications, we have discovered the essential roles of H3K9me3 and H3K27me3 during diapause of the Asian corn borer. Building upon previous findings in vertebrates highlighting the connection between DNA methylation and repressive histone methylations, we have examined changes in the genome-wide profile of H3K9me3, H3K27me3, and DNA methylation at the nondiapause, prediapause, and diapause stages. Data analysis reveals significant alterations in these three modifications during diapause. Moreover, we observe a correlation between the H3K9me3 and H3K27me3 modification sites during diapause, whereas DNA modifications show little association with either H3K9me3 or H3K27me3. Integrative analysis of epigenome and expression data unveils the relationship between these epigenetic modifications and gene expression levels at corresponding diapause stages. Furthermore, by studying the function of histone modifications on genes known to be important in diapause, especially those involved in the juvenile pathway, we discover that the juvenile hormone pathway lies downstream from H3K9me3 and H3K27me3 histone modifications. Finally, the analysis of gene loci with modified modifications unreported in diapause uncovers novel pathways potentially crucial in diapause regulation. This study provides a valuable resource for future investigations aiming to elucidate the underlying mechanisms of diapause.


Subject(s)
DNA Methylation , Epigenesis, Genetic , Histones , Moths , Animals , Histones/metabolism , Moths/genetics , Moths/metabolism , Larva/genetics , Larva/metabolism , Diapause, Insect/genetics , Genome, Insect , Diapause/genetics , Histone Code , Insect Proteins/genetics , Insect Proteins/metabolism
12.
Cell ; 187(13): 3338-3356.e30, 2024 Jun 20.
Article in English | MEDLINE | ID: mdl-38810644

ABSTRACT

Suspended animation states allow organisms to survive extreme environments. The African turquoise killifish has evolved diapause as a form of suspended development to survive a complete drought. However, the mechanisms underlying the evolution of extreme survival states are unknown. To understand diapause evolution, we performed integrative multi-omics (gene expression, chromatin accessibility, and lipidomics) in the embryos of multiple killifish species. We find that diapause evolved by a recent remodeling of regulatory elements at very ancient gene duplicates (paralogs) present in all vertebrates. CRISPR-Cas9-based perturbations identify the transcription factors REST/NRSF and FOXOs as critical for the diapause gene expression program, including genes involved in lipid metabolism. Indeed, diapause shows a distinct lipid profile, with an increase in triglycerides with very-long-chain fatty acids. Our work suggests a mechanism for the evolution of complex adaptations and offers strategies to promote long-term survival by activating suspended animation programs in other species.


Subject(s)
Diapause , Animals , Biological Evolution , Diapause/genetics , Embryo, Nonmammalian/metabolism , Fundulidae/genetics , Fundulidae/metabolism , Gene Expression Regulation, Developmental , Killifishes/genetics , Killifishes/metabolism , Lipid Metabolism/genetics , Fish Proteins/genetics , Male , Female
13.
Article in English | MEDLINE | ID: mdl-38810773

ABSTRACT

Spotted stem borer, Chilo partellus, undergoes larval diapause (hibernation and aestivation), and depends on the food reserve accumulated during feeding stage for its survival. Lipids are the primary source of energy during diapause, and essential for different cellular, biochemical and physiological functions. However, there is no information on lipid and lipophilic compound contents during different stages of hibernation, aestivation and nondiapause in C. partellus. Thus, we compared the concentration and composition of lipids in pre-diapause, diapause and post-diapause stages of hibernation and aestivation with nondiapause stages of C. partellus. The studies revealed significant differences in total lipids and various lipophilic compounds during different stages of diapause as compared to nondiapause C. partellus. The total lipids were significantly lower during diapause stage of aestivation and hibernation as compared to nondiapause larvae. Further, the linoleic acid, Methyl 3-methoxytetradecanoate, and l-(+)-Ascorbic acid 2,6-dihexadecanoate were significantly lower, and oleic and palmitoleic acids greater during pre-diapause and diapause stages of hibernation and aestivation as compared to nondiapause larvae. The cholesterol content was significantly greater during pre-diapause stage of hibernation, and diapause and post-diapause stages of aestivation as compared to nondiapause stages. The unsaturation ratio was significantly higher in the pre-diapause and diapause stages and lower in post-diapause stage of aestivation than the hibernation and nondiapause states. This study provides insights on differential lipid profiles during different phases of diapause, which could be useful for further understanding biochemical and physiological cross-talk, and develop target-specific technologies for the management of C. partellus.


Subject(s)
Diapause, Insect , Larva , Moths , Animals , Diapause, Insect/physiology , Moths/physiology , Moths/growth & development , Larva/physiology , Larva/growth & development , Lipids/chemistry , Hibernation/physiology , Lipid Metabolism/physiology , Linoleic Acid/metabolism , Diapause/physiology
14.
ISME J ; 18(1)2024 Jan 08.
Article in English | MEDLINE | ID: mdl-38767866

ABSTRACT

Host-microbe interactions underlie the development and fitness of many macroorganisms, including bees. Whereas many social bees benefit from vertically transmitted gut bacteria, current data suggests that solitary bees, which comprise the vast majority of species diversity within bees, lack a highly specialized gut microbiome. Here, we examine the composition and abundance of bacteria and fungi throughout the complete life cycle of the ground-nesting solitary bee Anthophora bomboides standfordiana. In contrast to expectations, immature bee stages maintain a distinct core microbiome consisting of Actinobacterial genera (Streptomyces, Nocardiodes) and the fungus Moniliella spathulata. Dormant (diapausing) larval bees hosted the most abundant and distinctive bacteria and fungi, attaining 33 and 52 times their initial copy number, respectively. We tested two adaptive hypotheses regarding microbial functions for diapausing bees. First, using isolated bacteria and fungi, we found that Streptomyces from brood cells inhibited the growth of multiple pathogenic filamentous fungi, suggesting a role in pathogen protection during overwintering, when bees face high pathogen pressure. Second, sugar alcohol composition changed in tandem with major changes in fungal abundance, suggesting links with bee cold tolerance or overwintering biology. We find that A. bomboides hosts a conserved core microbiome that may provide key fitness advantages through larval development and diapause, which raises the question of how this microbiome is maintained and faithfully transmitted between generations. Our results suggest that focus on microbiomes of mature or active insect developmental stages may overlook stage-specific symbionts and microbial fitness contributions during host dormancy.


Subject(s)
Bacteria , Fungi , Symbiosis , Animals , Bees/microbiology , Bacteria/classification , Bacteria/isolation & purification , Bacteria/genetics , Bacteria/growth & development , Fungi/physiology , Fungi/classification , Fungi/genetics , Fungi/isolation & purification , Fungi/growth & development , Larva/microbiology , Gastrointestinal Microbiome , Seasons , Host Microbial Interactions , Diapause/physiology
15.
Sci Rep ; 14(1): 11208, 2024 05 16.
Article in English | MEDLINE | ID: mdl-38755232

ABSTRACT

The mechanisms that underlie senescence are not well understood in insects. Telomeres are conserved repetitive sequences at chromosome ends that protect DNA during replication. In many vertebrates, telomeres shorten during cell division and in response to stress and are often used as a cellular marker of senescence. However, little is known about telomere dynamics across the lifespan in invertebrates. We measured telomere length in larvae, prepupae, pupae, and adults of two species of solitary bees, Osmia lignaria and Megachile rotundata. Contrary to our predictions, telomere length was longer in later developmental stages in both O. lignaria and M. rotundata. Longer telomeres occurred after emergence from diapause, which is a physiological state with increased tolerance to stress. In O. lignaria, telomeres were longer in adults when they emerged following diapause. In M. rotundata, telomeres were longer in the pupal stage and subsequent adult stage, which occurs after prepupal diapause. In both species, telomere length did not change during the 8 months of diapause. Telomere length did not differ by mass similarly across species or sex. We also did not see a difference in telomere length after adult O. lignaria were exposed to a nutritional stress, nor did length change during their adult lifespan. Taken together, these results suggest that telomere dynamics in solitary bees differ from what is commonly reported in vertebrates and suggest that insect diapause may influence telomere dynamics.


Subject(s)
Telomere , Animals , Bees/genetics , Bees/physiology , Telomere/genetics , Telomere/metabolism , Pupa/growth & development , Pupa/genetics , Female , Male , Telomere Homeostasis , Larva/genetics , Larva/growth & development , Larva/physiology , Diapause/genetics
16.
Sci Rep ; 14(1): 12192, 2024 05 28.
Article in English | MEDLINE | ID: mdl-38806592

ABSTRACT

Winter diapause consists of cessation of development that allows individuals to survive unfavourable conditions. Winter diapause may bear various costs and questions have been raised about the evolutionary mechanisms maintaining facultative diapause. Here, we explored to what extent a facultative winter diapause affects life-history traits and the transcriptome in the damselfly Ischnura elegans, and whether these effects were latitude-specific. We collected adult females at central and high latitudes and raised their larvae in growth chambers. Larvae were split into a non-diapausing and post-winter (diapausing) cohort, were phenotyped and collected for a gene expression analysis. At the phenotypic level, we found no difference in survival between the two cohorts, and the post-winter cohort was larger and heavier than the non-winter cohort. These effects were mostly independent of the latitude of origin. At the transcriptomic level, wintering affected gene expression with a small fraction of genes significantly overlapping across latitudes, especially those related to morphogenesis. In conclusion, we found clear effects of diapause on the phenotype but little evidence for latitudinal-specific effects of diapause. Our results showed a shared transcriptomic basis underpinning diapause demonstrated, here, at the intraspecific level and supported the idea of evolutionary convergence of the response to diapause across organisms.


Subject(s)
Odonata , Seasons , Transcriptome , Animals , Odonata/genetics , Female , Larva/genetics , Phenotype , Diapause, Insect/genetics , Diapause/genetics , Genetic Fitness
17.
Reprod Domest Anim ; 59(5): e14576, 2024 May.
Article in English | MEDLINE | ID: mdl-38712681

ABSTRACT

The possibility of embryo cryopreservation is important for applying the genome resource banking (GRB) concept to those mammalian species that exhibit embryonal diapause in their early development. Odc1 encodes ODC1, which is a key enzyme in polyamine synthesis. RhoA is an essential part of Rho/ROCK system. Both Odc1 and RhoA play an important role in preimplantation embryo development. Studying these systems in mammalian species with obligate or experimentally designed embryonic diapause may provide insight into the molecular machinery underlying embryo dormancy and re-activation. The effect of cryopreservation procedures on the expression of the Odc1 and RhoA in diapausing embryos has not been properly studied yet. The purpose of this work is to address the possibility of cryopreservation diapausing embryos and to estimate the expression of the Odc1 and RhoA genes in diapausing and non-diapausing embryos before and after freeze-thaw procedures using ovariectomized progesterone treated mice as a model. Both diapausing and non-diapausing in vivo-derived embryos continued their development in vitro after freezing-thawing as evidenced by blastocoel re-expansion. Although cryopreservation dramatically decreased the expression of the Odc1 and RhoA genes in non-diapausing embryos, no such effects have been observed in diapausing embryos where these genes were already at the low level before freeze-thaw procedures. Future studies may attempt to facilitate the re-activation of diapausing embryos, for example frozen-thawed ones, specifically targeting Odc1 or Rho/ROCK system.


Subject(s)
Blastocyst , Cryopreservation , rhoA GTP-Binding Protein , Animals , Female , Mice , Blastocyst/metabolism , Diapause , Embryo Culture Techniques , Embryonic Development , Gene Expression Regulation, Developmental , rhoA GTP-Binding Protein/genetics , rhoA GTP-Binding Protein/metabolism
18.
Curr Opin Genet Dev ; 86: 102192, 2024 Jun.
Article in English | MEDLINE | ID: mdl-38604005

ABSTRACT

Embryonic diapause in mammals is a period of developmental pause of the embryo at the blastocyst stage. During diapause, the blastocyst has minimal cell proliferation, metabolic activity and gene expression. At reactivation, blastocyst development resumes, characterised by increases in cell number, biosynthesis and metabolism. Until recently, it has been unknown how diapause is maintained without any loss of blastocyst viability. This review focuses on recent progress in the identification of molecular pathways occurring in the blastocyst that can both cause and maintain the diapause state. A switch to lipid metabolism now appears essential to maintaining the diapause state and is induced by forkhead box protein O1. The forkhead box protein O transcription family is important for diapause in insects, nematodes and fish, but this is the first time a conclusive role has been established in mammals. Multiple epigenetic modifications are also essential to inducing and maintaining the diapause state, including both DNA and RNA methylation mechanisms. Finally, it now appears that diapause embryos, dormant stem cells and chemotherapeutic-resistant cancer cells may all share a universal system of quiescence.


Subject(s)
Blastocyst , Diapause , Embryonic Development , Animals , Blastocyst/metabolism , Blastocyst/cytology , Diapause/genetics , Embryonic Development/genetics , Epigenesis, Genetic , Gene Expression Regulation, Developmental/genetics , Humans , Lipid Metabolism/genetics , Forkhead Transcription Factors/genetics , Forkhead Transcription Factors/metabolism
19.
Development ; 151(7)2024 Apr 01.
Article in English | MEDLINE | ID: mdl-38603796

ABSTRACT

Embryonic diapause is a special reproductive phenomenon in mammals that helps embryos to survive various harsh stresses. However, the mechanisms of embryonic diapause induced by the maternal environment is still unclear. Here, we uncovered that nutrient deficiency in uterine fluid was essential for the induction of mouse embryonic diapause, shown by a decreased concentration of arginine, leucine, isoleucine, lysine, glucose and lactate in the uterine fluid of mice suffering from maternal starvation or ovariectomy. Moreover, mouse blastocysts cultured in a medium with reduced levels of these six components could mimic diapaused blastocysts. Our mechanistic study indicated that amino acid starvation-dependent Gator1 activation and carbohydrate starvation-dependent Tsc2 activation inhibited mTORC1, leading to induction of embryonic diapause. Our study elucidates the essential environmental factors in diapause induction.


Subject(s)
Diapause , Nutrients , Animals , Female , Mice , Blastocyst/metabolism , Diapause/physiology , Embryonic Development/physiology
20.
Sci Rep ; 14(1): 8137, 2024 04 07.
Article in English | MEDLINE | ID: mdl-38584175

ABSTRACT

The design and implementation of Philaenus spumarius control strategies can take advantage of properly calibrated models describing and predicting the phenology of vector populations in agroecosystems. We developed a temperature-driven physiological-based model based on the system of Kolmogorov partial differential equations to predict the phenological dynamics of P. spumarius. The model considers the initial physiological age distribution of eggs, the diapause termination process, and the development rate functions of post-diapausing eggs and nymphal stages, estimated from data collected in laboratory experiments and field surveys in Italy. The temperature threshold and cumulative degree days for egg diapause termination were estimated as 6.5 °C and 120 DD, respectively. Preimaginal development rate functions exhibited lower thresholds ranging between 2.1 and 5.0 °C, optimal temperatures between 26.6 and 28.3 °C, and upper threshold between 33.0 and 35 °C. The model correctly simulates the emergence of the 3rd, 4th, and 5th nymphal instars, key stages to target monitoring actions and control measures against P. spumarius. Precision in simulating the phenology of the 1st and 2nd nymphal stages was less satisfactory. The model is a useful rational decision tool to support scheduling monitoring and control actions against the late and most important nymphal stages of P. spumarius.


Subject(s)
Diapause , Hemiptera , Animals , Temperature , Hemiptera/physiology , Italy , Nymph
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