Transcriptional regulation of <i>heat shock protein 70</i> genes by class I histone deacetylases in the red flour beetle, <scp><i>Tribolium castaneum</i></scp>

Chen, M; N, Zhang; Jiang, Heng; Meng, Xiangkun; Qiang, Karen; Wang, J

doi:10.1111/imb.12627

Cited by 7 publications

(4 citation statements)

References 41 publications

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“…HSPs identified as differentially expressed in this study support past results for beetle species and other insects more broadly. A major trend in our results concerned the upregulation of HSP70 genes at high temperatures, particularly Hsp68 ; HSP70s are highly expressed in response to heat shock in other beetle species, including cave-adapted subterranean taxa 28 , 49 , 50 , and work in concert with sHSPs and HSP90s 51 – 54 . In addition to the heat shock proteins, we also observed the upregulation of the heat shock cognates Hsc70-3 and Hsc70-4 and putative cochaperones Samui , DnaJ , AHSA1 , and Unc45a at 35 °C relative to the 25 °C treatment.…”

Section: Discussionmentioning

confidence: 71%

Differential transcriptomic responses to heat stress in surface and subterranean diving beetles

Beasley‐Hall

Bertozzi

Bradford

et al. 2022

Sci Rep

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Subterranean habitats are generally very stable environments, and as such evolutionary transitions of organisms from surface to subterranean lifestyles may cause considerable shifts in physiology, particularly with respect to thermal tolerance. In this study we compared responses to heat shock at the molecular level in a geographically widespread, surface-dwelling water beetle to a congeneric subterranean species restricted to a single aquifer (Dytiscidae: Hydroporinae). The obligate subterranean beetle Paroster macrosturtensis is known to have a lower thermal tolerance compared to surface lineages (CTmax 38 °C cf. 42–46 °C), but the genetic basis of this physiological difference has not been characterized. We experimentally manipulated the thermal environment of 24 individuals to demonstrate that both species can mount a heat shock response at high temperatures (35 °C), as determined by comparative transcriptomics. However, genes involved in these responses differ between species and a far greater number were differentially expressed in the surface taxon, suggesting it can mount a more robust heat shock response; these data may underpin its higher thermal tolerance compared to subterranean relatives. In contrast, the subterranean species examined not only differentially expressed fewer genes in response to increasing temperatures, but also in the presence of the experimental setup employed here alone. Our results suggest P. macrosturtensis may be comparatively poorly equipped to respond to both thermally induced stress and environmental disturbances more broadly. The molecular findings presented here have conservation implications for P. macrosturtensis and contribute to a growing narrative concerning weakened thermal tolerances in obligate subterranean organisms at the molecular level.

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Section: Discussionmentioning

confidence: 71%

Differential transcriptomic responses to heat stress in surface and subterranean diving beetles

Beasley‐Hall

Bertozzi

Bradford

et al. 2022

Sci Rep

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“…HSPs identified as differentially expressed in this study support past results from beetle species and other insects more broadly. A major trend from our results concerned the upregulation of HSP70 genes, particularly Hsp68 ; HSP70s are highly expressed in response to heat shock in the Colorado potato beetle (Yocum, 2001), red flour beetle (Chen et al, 2020), and the cave beetle Neobathyscia (Bernabò et al, 2011). These genes are upregulated in concert with sHSPs and HSP90 genes in the rice weevil (Yuan et al, 2014) and Japanese sawyer beetle (Cai et al, 2017) under the same conditions.…”

Section: Discussionmentioning

confidence: 77%

“…HSPs identified as differentially expressed in this study support past results for beetle species and other insects more broadly. A major trend in our results concerned the upregulation of HSP70 genes at high temperatures, particularly Hsp68; HSP70s are highly expressed in response to heat shock in other beetle species, including cave-adapted subterranean taxa (28,49,50), and work in concert with sHSPs and HSP90s (51)(52)(53)(54). In addition to the heat shock proteins, we also observed the upregulation of the heat shock cognates Hsc70-2, Hsc70-3, and Hsc70-4 and cochaperones Tsc2, Samui, DnaJ, AHSA1, Unc45a in at 35ºC relative to the 25ºC treatment.…”

Section: Heat Shock-induced Gene Expression In Parostermentioning

confidence: 76%

Differential transcriptomic responses to heat stress in surface and subterranean diving beetles

Beasley‐Hall

Bertozzi

Bradford

et al. 2021

Preprint

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Subterranean habitats are environmentally stable with respect to temperature, humidity, and the absence of light. The transition to a subterranean lifestyle might therefore be expected to cause considerable shifts in an organism’s physiology; here, we investigate how subterranean colonisation affects thermal tolerance. Subterranean organisms might be at an increased risk of decline in the face of global temperature rises, but robust data on the fauna is lacking, particularly at the molecular level. In this study we compare the heat shock response of two species of diving beetle in the genus Paroster: one surface-dwelling (P. nigroadumbratus), the other restricted to a single aquifer (P. macrosturtensis). P. macrosturtensis has been previously established as having a lower thermal tolerance compared to surface-dwelling relatives, but the genomic basis of this difference is unknown. By sequencing transcriptomes of experimentally heat-shocked individuals and performing differential expression analysis, we demonstrate both species can mount a heat shock response at high temperatures (35C), in agreement with past survival experiments. However, the genes involved in these responses differ between species, and far greater genes are differentially expressed in the surface species, which may explain its more robust response to heat stress. In contrast, the subterranean species significantly upregulated the heat shock protein gene Hsp68 in the experimental setup under conditions it would likely encounter in nature (25C), suggesting it may be more sensitive to ambient stressors, e.g. handling. The results presented here contribute to an emerging narrative concerning weakened thermal tolerances in obligate subterranean organisms at the molecular level.

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“…HSP70 is one of the critical predictors of insect tolerance to heat stress. Previous studies showed that higher induced levels of HSP corresponded to stronger heat tolerance in arthropods (Chang et al ., 2018; Chen et al ., 2020). MaltHSP70s accumulated by over a thousand-fold after heat shock, which implied that MaltHSP70s were more sensitive than HSP70s in other insects (Li et al ., 2009; Udaka et al ., 2010; Wang et al ., 2015; Quan et al ., 2018).…”

Section: Discussionmentioning

confidence: 99%

Characterization, expression profiling, and thermal tolerance analysis of heat shock protein 70 in pine sawyer beetle, Monochamus alternatus hope (Coleoptera: Cerambycidae)

Qiao

Liu

et al. 2020

Bull. Entomol. Res.

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Monochamus alternatus Hope (Coleoptera: Cerambycidae) warrants attention as a dominant transmission vector of the pinewood nematode, and it exhibits tolerance to high temperature. Heat shock protein 70 (HSP70) family members, including inducible HSP70 and heat shock cognate protein 70 (HSC70), are major contributors to the molecular chaperone networks of insects under heat stress. In this regard, we specifically cloned and characterized three MaltHSP70s and three MaltHSC70s. Bioinformatics analysis on the deduced amino acid sequences showed these genes, having close genetic relationships with HSP70s of Coleopteran species, collectively shared conserved signature structures and ATPase domains. Subcellular localization prediction revealed the HSP70s of M. alternatus were located not only in the cytoplasm and endoplasmic reticulum but also in the nucleus and mitochondria. The transcript levels of MaltHSP70s and MaltHSC70s in each state were significantly upregulated by exposure to 35–50°C for early 3 h, while MaltHSP70s reached a peak after exposure to 45°C for 2–3 h in contrast to less-upregulated MaltHSC70s. In terms of MaltHSP70s, the expression threshold in females was lower than that in males. Also, both fat bodies and Malpighian tubules were the tissues most sensitive to heat stress in M. alternatus larvae. Lastly, the ATPase activity of recombinant MaltHSP70-2 in vitro remained stable at 25–40°C, and this recombinant availably enhanced the thermotolerance of Escherichia coli. Overall, our findings unraveled HSP70s might be the intrinsic mediators of the strong heat tolerance of M. alternatus due to their stabilized structure and bioactivity.

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Transcriptional regulation of heat shock protein 70 genes by class I histone deacetylases in the red flour beetle, Tribolium castaneum

Cited by 7 publications

References 41 publications

Differential transcriptomic responses to heat stress in surface and subterranean diving beetles

Differential transcriptomic responses to heat stress in surface and subterranean diving beetles

Differential transcriptomic responses to heat stress in surface and subterranean diving beetles

Characterization, expression profiling, and thermal tolerance analysis of heat shock protein 70 in pine sawyer beetle, Monochamus alternatus hope (Coleoptera: Cerambycidae)

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