Embryonic temperature affects muscle fibre recruitment in adult zebrafish: genome-wide changes in gene and microRNA expression associated with the transition from hyperplastic to hypertrophic growth phenotypes

Johnston, Ian A.; Lee, Hung-Tai; Macqueen, Daniel J.; Paranthaman, Karthikeyani; Kawashima, Cintia Goulart; Anwar, Attia; Kinghorn, James R.; Dalmay, Tamás

doi:10.1242/jeb.029918

Cited by 157 publications

(130 citation statements)

References 75 publications

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“…However, it remains unclear whether the changes in DNA methylation variation were specific to myog alone because methylation changes at other loci were not investigated. Johnston et al (2009) provided evidence that in addition to DNA methylation, microRNA expression at different embryonic temperatures can also be associated with the transition from hyperplastic to hypertrophic muscle growth phenotype in adult zebrafish (Danio rerio). Effects of microRNA on thermal plasticity are not only confined to simple developmental transitions, but have also been shown to be involved in complex neuronal network remodelling.…”

Section: Within-generational Epigenetic Effectsmentioning

confidence: 99%

Epigenetics in natural animal populations

Barrett

2017

J of Evolutionary Biology

130

127

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Phenotypic plasticity is an important mechanism for populations to buffer themselves from environmental change. While it has long been appreciated that natural populations possess genetic variation in the extent of plasticity, a surge of recent evidence suggests that epigenetic variation could also play an important role in shaping phenotypic responses. Compared with genetic variation, epigenetic variation is more likely to have higher spontaneous rates of mutation and a more sensitive reaction to environmental inputs. In our review, we first provide an overview of recent studies on epigenetically encoded thermal plasticity in animals to illustrate environmentally-mediated epigenetic effects within and across generations. Second, we discuss the role of epigenetic effects during adaptation by exploring population epigenetics in natural animal populations. Finally, we evaluate the evolutionary potential of epigenetic variation depending on its autonomy from genetic variation and its transgenerational stability. Although many of the causal links between epigenetic variation and phenotypic plasticity remain elusive, new data has explored the role of epigenetic variation in facilitating evolution in natural populations. This recent progress in ecological epigenetics will be helpful for generating predictive models of the capacity of organisms to adapt to changing climates.

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Section: Within-generational Epigenetic Effectsmentioning

confidence: 99%

Epigenetics in natural animal populations

Barrett

2017

J of Evolutionary Biology

130

127

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“…The influence of developmental temperature on the muscle ontogeny of the fish which has long been established (Johnston 1981(Johnston , 1993(Johnston , 2006Johnston et al 2009;Koumoundouros et al 2009) appears to have a substantial effect on swimming performance. Different temperatures lead to variation in body muscle mass (in terms of size and number of muscle fibres) that directly affect swimming ability.…”

Section: Discussionmentioning

confidence: 99%

“…Koumoundouros et al (2009), showed that in the case of European sea bass, the best swimmers had relatively higher red muscle to white muscle ratio and more red muscle fibres than the others. In the case of zebrafish, Johnston et al (2009) showed that the optimal embryonic temperature for fast muscle fibre recruitment (hyperplasia) is 26°C, as in that temperature there were 18.8% more fast fibers than at 22°C and 13.7% more fibers than at 31°C. After this phase, myotube formation stops and a new phase begins (hypertrophy) that consists of nuclear accretion and increase in fibre length and diameter (Johnston et al 2004).…”

Section: Discussionmentioning

confidence: 99%

Effect of developmental temperature on swimming performance of zebrafish (Danio rerio) juveniles

2010

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It is widely known that water temperature affects the swimming capacity of fish. But the effect of the rearing temperature on the swimming ability of the fish at later stages, has not had similar attention. In this study, four populations of zebrafish, were reared in different water temperatures (22, 25, 28 and 31°C) and after being acclimatized in a common temperature (26.5°C) for over a month, they were subjected to swimming trials in order to evaluate the maximum relative critical velocity (RU crit ) in each case. Fish that were reared in 22°C showed statistically significant lower performance than the ones reared in 31°C (7.72 ±0.17 vs. 8.79±0.28, means ± S.E.). Possible explanations for the observed differentiation could be the effect of early life temperature on fish muscle ontogeny or on body shape.

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“…The Journal of Experimental Biology (2014) doi:10.1242/jeb.094037 size of both red fibres (Scott and Johnston, 2012) and fast glycolytic (white) fibres (Johnston et al, 2009) in zebrafish: fibres tend to be larger but fewer in number in fish raised at 22°C or 31-32°C as embryos compared with fish raised at 26-27°C. The observation that muscle COX and PK activities are higher in concert with an increase in muscle fibre size (but not total area) in the 22°C and 32°C T E groups provides correlative evidence that there may be metabolic consequences for the often observed effect of T E on muscle cellularity (Vieira and Johnston, 1992;Rowlerson and Veggetti, 2001;Stoiber et al, 2002;McClelland and Scott, 2013).…”

Section: Research Articlementioning

confidence: 99%

Temperature during embryonic development has persistent effects on metabolic enzymes in the muscle of zebrafish

Schnurr

Scott

2013

Journal of Experimental Biology

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Global warming is intensifying interest in the physiological consequences of temperature change in ectotherms, but we still have a relatively poor understanding of the effects of temperature on early life stages. This study determined how embryonic temperature (T E ) affects development and the activity of metabolic enzymes in the swimming muscle of zebrafish. Embryos developed successfully to hatching (survival ≥88%) from 22 to 32°C, but suffered sharp increases in mortality outside of this range. Embryos that were incubated until hatching at a control T E (27°C) or near the extremes for successful development (22 or 32°C) were next raised to adulthood under control conditions at 27°C. Growth trajectories after hatching were altered in the 22°C and 32°C T E groups compared with 27°C T E controls, but growth slowed after 3 months of age in all groups. Maximal enzyme activities of cytochrome c oxidase (COX), citrate synthase (CS), hydroxyacyl-coA dehydrogenase (HOAD), pyruvate kinase (PK) and lactate dehydrogenase (LDH) were measured across a range of assay temperatures (22, 27, 32 and 36°C) in adults from each T E group that were acclimated to 27 or 32°C. Substrate affinities (K m ) were also determined for COX and LDH. In adult fish acclimated to 27°C, COX and PK activities were higher in 22°C and 32°C T E groups than in 27°C T E controls, and the temperature optimum for COX activity was higher in the 32°C T E group than in the 22°C T E group. Warm acclimation reduced COX, CS and/or PK activities in the 22 and 32°C T E groups, possibly to compensate for thermal effects on molecular activity. This response did not occur in the 27°C T E controls, which instead increased LDH and HOAD activities. Warm acclimation also increased thermal sensitivity (Q 10 ) of HOAD to cool temperatures across all T E groups. We conclude that the temperature experienced during early development can have a persistent impact on energy metabolism pathways and acclimation capacity in later life.

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Embryonic temperature affects muscle fibre recruitment in adult zebrafish: genome-wide changes in gene and microRNA expression associated with the transition from hyperplastic to hypertrophic growth phenotypes

Cited by 157 publications

References 75 publications

Epigenetics in natural animal populations

Epigenetics in natural animal populations

Effect of developmental temperature on swimming performance of zebrafish (Danio rerio) juveniles

Temperature during embryonic development has persistent effects on metabolic enzymes in the muscle of zebrafish

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