Changes in gene expression associated with acclimation to constant temperatures and fluctuating daily temperatures in an annual killifish<i>Austrofundulus limnaeus</i>

Podrabsky, Jason E.; Somero, George N.

doi:10.1242/jeb.01016

Cited by 392 publications

(351 citation statements)

References 57 publications

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“…Gracey et al 2008); however, the constitutive HSC70 has been designated the main heat-dependant HSP70 family member in the Pacific white shrimp (Litopenaeus vannamei; Wu et al 2008). This latter example may be species specific as there is increasing evidence that although HSC70 may upregulated by acute heat stress, it is often more likely to correlate with longer-term chronic stress such as that described here, in fluctuating temperature regimes (Podrabsky and Somero 2004;Todgham et al 2006) and under environmentally diverse bio-geographical distributions (Fangue et al 2006;Place et al 2008). The great flexibility of the HSP70 gene complex means that if it is to be used as an environmental biomarker, clearly as many family members as possible should be surveyed under a number of different conditions over both acute and chronic timescales.…”

Section: Hsp70 Gene Family Expressionmentioning

confidence: 78%

Triggers of the HSP70 stress response: environmental responses and laboratory manipulation in an Antarctic marine invertebrate (Nacella concinna)

Clark

Peck

2009

Cell Stress and Chaperones

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The Antarctic limpet, Nacella concinna, exhibits the classical heat shock response, with up-regulation of duplicated forms of the inducible heat shock protein 70 (HSP70) gene in response to experimental manipulation of seawater temperatures. However, this response only occurs in the laboratory at temperatures well in excess of any experienced in the field. Subsequent environmental sampling of inter-tidal animals also showed up-regulation of these genes, but at temperature thresholds much lower than those required to elicit a response in the laboratory. It was hypothesised that this was a reflection of the complexity of the stresses encountered in the inter-tidal region. Here, we describe a further series of experiments comprising both laboratory manipulation and environmental sampling of N. concinna. We investigate the expression of HSP70 gene family members (HSP70A, HSP70B, GRP78 and HSC70) in response to a further suite of environmental stressors: seasonal and experimental cold, freshwater, desiccation, chronic heat and periodic emersion. Lowered temperatures (−1.9°C and −1.6°C), generally produced a downregulation of all HSP70 family members, with some upregulation of HSC70 when emerging from the winter period and increasing sea temperatures. There was no significant response to freshwater immersion. In response to acute and chronic heat treatments plus simulated tidal cycles, the data showed a clear pattern. HSP70A showed a strong but very short-term response to heat whilst the duplicated HSP70B also showed heat to be a trigger, but had a more sustained response to complex stresses. GRP78 expression indicates that it was acting as a generalised stress response under the experimental conditions described here. HSC70 was the major chaperone invoked in response to long-term stresses of varying types. These results provide intriguing clues not only to the complexity of HSP70 gene expression in response to environmental change but also insights into the stress response of a non-model species.

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Section: Hsp70 Gene Family Expressionmentioning

confidence: 78%

Triggers of the HSP70 stress response: environmental responses and laboratory manipulation in an Antarctic marine invertebrate (Nacella concinna)

Clark

Peck

2009

Cell Stress and Chaperones

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“…We also detected the strong induction of a number of high-mobility group proteins (HMG1, HMGT1, HMG4, and NHPX) that modulate transcription through the alteration of chromosome conformation, suggesting that chromosomal DNA secondary structure might also be disturbed in the cold. In killifish, the expression of another high-mobility group protein, HMGB1, has also been shown to fluctuate with cycling temperature, providing further evidence that this gene family is involved in temperature responses (18). The identification of genes involved in both RNA processing and chromosomal architecture suggests an important function of cold acclimation is to regulate nucleic acid structures.…”

Section: Resultsmentioning

confidence: 98%

Coping with cold: An integrative, multitissue analysis of the transcriptome of a poikilothermic vertebrate

Gracey

Fraser²,

Li³

et al. 2004

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

403

395

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How do organisms respond adaptively to environmental stress? Although some gene-specific responses have been explored, others remain to be identified, and there is a very poor understanding of the system-wide integration of response, particularly in complex, multitissue animals. Here, we adopt a transcript screening approach to explore the mechanisms underpinning a major, wholebody phenotypic transition in a vertebrate animal that naturally experiences extreme environmental stress. Carp were exposed to increasing levels of cold, and responses across seven tissues were assessed by using a microarray composed of 13,440 cDNA probes. A large set of unique cDNAs (Ϸ3,400) were affected by cold. These cDNAs included an expression signature common to all tissues of 252 up-regulated genes involved in RNA processing, translation initiation, mitochondrial metabolism, proteasomal function, and modification of higher-order structures of lipid membranes and chromosomes. Also identified were large numbers of transcripts with highly tissue-specific patterns of regulation. By unbiased profiling of gene ontologies, we have identified the distinctive functional features of each tissue's response and integrate them into a comprehensive view of the whole-body transition from one strongly adaptive phenotype to another. This approach revealed an expression signature suggestive of atrophy in cooled skeletal muscle. This environmental genomics approach by using a well studied but nongenomic species has identified a range of candidate genes endowing thermotolerance and reveals a previously unrecognized scale and complexity of responses that impacts at the level of cellular and tissue function.fish ͉ microarray ͉ stress

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“…This phenomenon, known as heat hardening (Bowler, 2005), is a very important inducible stress tolerance mechanism in many organisms, both terrestrial and aquatic, inhabiting variable environments (Maness and Hutchinson, 1980;Rutledge et al, 1987;Middlebrook et al, 2008;Bilyk et al, 2012). Previous studies have shown fluctuating thermal environments increase thermal tolerance (Feldmeth et al, 1974;Otto, 1974;Threader and Houston, 1983;Woiwode and Adelman, 1992;Schaefer and Ryan, 2006;Oliver and Palumbi, 2011;Manenti et al, 2014;Kern et al, 2015), with intertidal species exposed to tidal cycle fluctuations being more stress-tolerant than those that are exposed to constant temperatures (Tomanek and Sanford, 2003;Podrabsky and Somero, 2004;Todgham et al, 2006;Giomi et al, 2016). Taken together, these studies suggest that the thermal physiology of intertidal organisms is likely modulated by the natural variability inherent with the ebb and flow of tides.…”

Section: Introductionmentioning

confidence: 99%

The role of stochastic thermal environments in modulating the thermal physiology of an intertidal limpet, Lottia digitalis

Drake

Miller

Todgham

2017

Journal of Experimental Biology

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Much of our understanding of the thermal physiology of intertidal organisms comes from experiments with animals acclimated under constant conditions and exposed to a single heat stress. In nature, however, the thermal environment is more complex. Aerial exposure and the unpredictable nature of thermal stress during low tides may be critical factors in defining the thermal physiology of intertidal organisms. In the fingered limpet, Lottia digitalis, we investigated whether upper temperature tolerance and thermal sensitivity were influenced by the pattern of fluctuation with which thermal stress was applied. Specifically, we examined whether there was a differential response (measured as cardiac performance) to repeated heat stress of a constant and predictable magnitude compared with heat stress applied in a stochastic and unpredictable nature. We also investigated differences in cellular metabolism and damage following immersion for insights into biochemical mechanisms of tolerance. Upper temperature tolerance increased with aerial exposure, but no significant differences were found between predictable treatments of varying magnitudes (13°C versus 24°C versus 32°C). Significant differences in thermal tolerance were found between unpredictable trials with different heating patterns. There were no significant differences among treatments in basal citrate synthase activity, glycogen content, oxidative stress or antioxidants. Our results suggest that aerial exposure and recent thermal history, paired with relief from high low-tide temperatures, are important factors modulating the capacity of limpets to deal with thermal stress.

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Changes in gene expression associated with acclimation to constant temperatures and fluctuating daily temperatures in an annual killifishAustrofundulus limnaeus

Cited by 392 publications

References 57 publications

Triggers of the HSP70 stress response: environmental responses and laboratory manipulation in an Antarctic marine invertebrate (Nacella concinna)

Triggers of the HSP70 stress response: environmental responses and laboratory manipulation in an Antarctic marine invertebrate (Nacella concinna)

Coping with cold: An integrative, multitissue analysis of the transcriptome of a poikilothermic vertebrate

The role of stochastic thermal environments in modulating the thermal physiology of an intertidal limpet, Lottia digitalis

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