Temporal dynamics of gene expression in heat-stressed Caenorhabditis elegans

Jovic, Katharina; Sterken, M.G.; Grilli, Jacopo; Bevers, R.; Rodríguez, Martín González; Riksen, J.A.G.; Allesina, Stefano; Kammenga, J.E.; Snoek, L. Basten

doi:10.1371/journal.pone.0189445

Cited by 63 publications

(75 citation statements)

References 42 publications

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“…2, D, E, and H ). A recent study has shown that prolonged heat stress in C. elegans results in transcriptional up-regulation of core histones and other genes involved in nucleosome assembly ( 44 ). Nonetheless, our results indicate that the higher H4 protein level in hsb-1(−) worms is not due to elevated transcription of H4 genes during development or adulthood (fig.…”

Section: Discussionmentioning

confidence: 99%

HSB-1/HSF-1 pathway modulates histone H4 in mitochondria to control mtDNA transcription and longevity

et al. 2020

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Heat shock factor–1 (HSF-1) is a master regulator of stress responses across taxa. Overexpression of HSF-1 or genetic ablation of its conserved negative regulator, heat shock factor binding protein 1 (HSB-1), results in robust life-span extension in Caenorhabditiselegans. Here, we found that increased HSF-1 activity elevates histone H4 levels in somatic tissues during development, while knockdown of H4 completely suppresses HSF-1–mediated longevity. Moreover, overexpression of H4 is sufficient to extend life span. Ablation of HSB-1 induces an H4-dependent increase in micrococcal nuclease protection of both nuclear chromatin and mitochondrial DNA (mtDNA), which consequently results in reduced transcription of mtDNA-encoded complex IV genes, decreased respiratory capacity, and a mitochondrial unfolded protein response–dependent life-span extension. Collectively, our findings reveal a previously unknown role of HSB-1/HSF-1 signaling in modulation of mitochondrial function via mediating histone H4-dependent regulation of mtDNA gene expression and concomitantly acting as a determinant of organismal longevity.

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Section: Discussionmentioning

confidence: 99%

HSB-1/HSF-1 pathway modulates histone H4 in mitochondria to control mtDNA transcription and longevity

et al. 2020

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“…In C. elegans and C. remanei , plasticity dominates heat‐shock transcriptome responses (Jovic et al, ; Sikkink, Reynolds, Ituarte, Cresko, & Phillips, ). We also found in C. briggsae that >90% of differentially expressed genes changed due to temperature, at least in part, but more often due to chronic cool rather than warm conditions.…”

Section: Discussionmentioning

confidence: 99%

Genome structure predicts modular transcriptome responses to genetic and environmental conditions

et al. 2019

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Understanding the plasticity, robustness and modularity of transcriptome expression to genetic and environmental conditions is crucial to deciphering how organisms adapt in nature. To test how genome architecture influences transcriptome profiles, we quantified expression responses for distinct temperature‐adapted genotypes of the nematode Caenorhabditis briggsae when exposed to chronic temperature stresses throughout development. We found that 56% of the 8,795 differentially expressed genes show genotype‐specific changes in expression in response to temperature (genotype‐by‐environment interactions, GxE). Most genotype‐specific responses occur under heat stress, indicating that cold vs. heat stress responses involve distinct genomic architectures. The 22 co‐expression modules that we identified differ in their enrichment of genes with genetic vs. environmental vs. interaction effects, as well as their genomic spatial distributions, functional attributes and rates of molecular evolution at the sequence level. Genes in modules enriched for simple effects of either genotype or temperature alone tend to evolve especially rapidly, consistent with disproportionate influence of adaptation or weaker constraint on these subsets of loci. Chromosome‐scale heterogeneity in nucleotide polymorphism, however, rather than the scale of individual genes predominates as the source of genetic differences among expression profiles, and natural selection regimes are largely decoupled between coding sequences and noncoding flanking sequences that contain cis‐regulatory elements. These results illustrate how the form of transcriptome modularity and genome structure contribute to predictable profiles of evolutionary change.

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“…We deemed a somite count of 32 ± 1 (corresponding to stage 27 according to Dufaure & Hubert, ; Figure a) appropriate for our purposes since this allowed the warm incubated embryos to develop for at least 12 hr (average 43.7 ± 3.1 hr SE), while requiring the cool incubated embryos to develop for an average of about 2 weeks (16.8 ± 1.1 days). We reasoned that 12 hr is a sufficient amount of time to acclimatize gene expression patterns because (i) the magnitude of temperature change that eggs experience from the warm nesting site to the 24°C incubation treatment is very small (average temperature of nest sites in laboratory conditions, 25°C, While et al., ), and (ii) gene expression has been shown to adjust rather quickly, in the order of 3–4 hr (Jovic et al., ). Based on our predictions, we selected eggs for dissection at regular intervals to ensure that a sufficient number of embryos of the targeted developmental age would be available for sequencing.…”

Section: Methodsmentioning

confidence: 99%

Developmental plasticity in reptiles: Insights from temperature‐dependent gene expression in wall lizard embryos

et al. 2018

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Many features of the development of reptiles are affected by temperature, but very little is known about how incubation temperature affects gene expression. Here, we provide a detailed case study of gene expression profiles in common wall lizard (Podarcis muralis) embryos developing at stressfully low (15°C) versus benign (24°C) temperature. For maximum comparability between the two temperature regimes, we selected a precise developmental stage early in embryogenesis defined by the number of somites. We used a split-clutch design and lizards from four different populations to evaluate the robustness of temperature-responsive gene expression profiles. Embryos incubated at stressfully low incubation temperature expressed on average 20% less total RNA than those incubated at benign temperatures, presumably reflecting lower rates of transcription at cool temperature. After normalizing for differences in total amounts of input RNA, we find that approximately 50% of all transcripts show significant expression differences between the two incubation temperatures. Transcripts with the most extreme changes in expression profiles are associated with transcriptional and translational regulation and chromatin remodeling, suggesting possible epigenetic mechanisms underlying acclimation of early embryos to cool temperature. We discuss our findings in light of current advances in the use of transcriptomic data to study how individuals acclimatize and populations adapt to thermal stress.

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Temporal dynamics of gene expression in heat-stressed Caenorhabditis elegans

Cited by 63 publications

References 42 publications

HSB-1/HSF-1 pathway modulates histone H4 in mitochondria to control mtDNA transcription and longevity

HSB-1/HSF-1 pathway modulates histone H4 in mitochondria to control mtDNA transcription and longevity

Genome structure predicts modular transcriptome responses to genetic and environmental conditions

Developmental plasticity in reptiles: Insights from temperature‐dependent gene expression in wall lizard embryos

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