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. 2017 Aug 1;72(8):1033-1037.
doi: 10.1093/gerona/glx017.

Environmental Canalization of Life Span and Gene Expression in Caenorhabditis Elegans

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Free PMC article

Environmental Canalization of Life Span and Gene Expression in Caenorhabditis Elegans

Alexander Mendenhall et al. J Gerontol A Biol Sci Med Sci. .
Free PMC article

Abstract

Animals, particularly poikilotherms, exhibit distinct physiologies at different environmental temperatures. Here, we hypothesized that temperature-based differences in physiology could affect the amount of variation in complex quantitative traits. Specifically, we examined, in Caenorhabditis elegans, how different temperatures (15°C, 20°C, and 25°C) affected the amount of interindividual variation in life span and also expression of three reporter genes-transcriptional reporters for vit-2, gpd-2, and hsp-16.2 (a life-span biomarker). We found the expected inverse relationship between temperature and average life span. Surprisingly, we found that at the highest temperature, there were fewer differences between individuals in life span and less interindividual variation in expression of all three reporters. We suggest that growth at 25°C might canalize (reduce interindividual differences in) life span and expression of some genes by eliciting a small constitutive heat shock response. Growth at 25°C requires wild-type hsf-1, which encodes the main heat shock response transcriptional activator. We speculate that increased chaperone activity at 25°C may reduce interindividual variation in gene expression by increasing protein folding efficiency. We hypothesize that reduced variation in gene expression may ultimately cause reduced variation in life span.

Keywords: Aging; Biomarker; Nongenetic; Proteostasis; Variation.

Figures

Figure 1.
Figure 1.
Interindividual variation in gene expression and life span as a function of temperature. This figure shows that the amount of interindividual variation in three kinds of reporter gene expression, including a life-span biomarker, decreases at 25°C (B); interestingly, the amount of interindividual variation in life span also decreased at 25°C (D). Top graphs (A, B) depict mean ± SEM; bottom graphs (C, D) depict 95% confidence intervals (CI). To determine statistical significance, two-way analysis of variance (ANOVA) followed by the Holm–Sidak test for multiple comparisons was used for comparing the effects of temperature and strain on mean or CV, unless otherwise stated. CV is the coefficient of variation (SD/mean); CV is displayed as a whole-number percentage. Five independent trials consisting of approximately 500 individuals of each strain (one per reporter) at each temperature were used to generate the graphs of reporter gene expression. Fluorescence levels for animals expressing Pgpd-2::gfp are divided by 10 for plotting purposes; actual values are shown in Supplementary Table S1. (A) All reporters were significantly different in expression level from one another within each temperature. All p values from two-way ANOVA followed by Holm–Sidak testing for effects of strain and temperature on mean expression are shown in Supplementary File F1. Measured Pgpd-2::gfp expression was significantly different between 16°C and 20°C (p = .001) and 16°C and 25°C (p = .0003). Pvit-2::gfp was significantly different between 16°C and 20°C (p = .007). No significant differences were detected in induced Phsp-16.2::gfp expression between any temperatures; constitutive Phsp-16.2::gfp expression at 25°C was significantly different from all other gene expression levels at 25°C (p = .02, one-way repeated measures ANOVA, Student–Newman–Keuls test). Temperature had a significant effect on mean expression between 16°C and 20°C and between 16°C and 25°C, when the entire profile of reporters is considered (p = .00009 for 16°C vs 25°C and 16°C vs 20°C). Also, see Table 1. (B) Pvit-2::gfp CV was significantly greater than Phsp-16.2::gfp CV at 16°C (p = .011). Pgpd-2::gfp CV significantly changed between 20°C and 25°C (p = .0003). Pvit-2::gfp CV significantly changed between 16°C and 25°C (p = .008). CV measured for 25°C Phsp-16.2::gfp expression was significantly higher than for the 35°C -induced expression of Phsp-16.2::gfp (p = .02, paired t test). Temperature has a significant effect on CV of the analyzed reporters between 16°C and 25°C (p = .00028) and between 20°C and 25°C (p = .019); increasing temperature decreased worm-to-worm variation in gene expression. Explicit p values for every comparison from the two-way ANOVA followed by Holm–Sidak testing for effects of temperature and strain on CV are detailed in Supplementary File F2. Also, see Table 1. (C) Mean life span significantly decreased with increasing temperature; 95% CI shown. Fifty independent life-span experiments at various temperatures comprised the Life span × Temperature data set. Also, see Table 2. (D) Interindividual variation in life span significantly decreased at 25°C; 95% CI shown. Also, see Table 2. Raw data for life spans and individual life-span trial CVs is available in Supplementary File F3.

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