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High incubation temperatures enhance mitochondrial energy metabolism in reptile embryos.

Sun BJ, Li T, Gao J, Ma L, Du WG - Sci Rep (2015)

Bottom Line: We measured mitochondrial respiration and metabolic enzyme activities of turtle embryos (Pelodiscus sinensis) incubated at different temperatures to identify the metabolic basis of the rapid development occurring at high temperatures in reptile embryos.Developmental rate increased with increasing incubation temperatures in the embryos of P. sinensis.Our study highlights the importance of biochemical investigations in understanding the proximate mechanisms by which temperature affects embryonic development.

View Article: PubMed Central - PubMed

Affiliation: Key Laboratory of Animal Ecology and Conservational Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, People's Republic of China.

ABSTRACT
Developmental rate increases exponentially with increasing temperature in ectothermic animals, but the biochemical basis underlying this thermal dependence is largely unexplored. We measured mitochondrial respiration and metabolic enzyme activities of turtle embryos (Pelodiscus sinensis) incubated at different temperatures to identify the metabolic basis of the rapid development occurring at high temperatures in reptile embryos. Developmental rate increased with increasing incubation temperatures in the embryos of P. sinensis. Correspondingly, in addition to the thermal dependence of mitochondrial respiration and metabolic enzyme activities, high-temperature incubation further enhanced mitochondrial respiration and COX activities in the embryos. This suggests that embryos may adjust mitochondrial respiration and metabolic enzyme activities in response to developmental temperature to achieve high developmental rates at high temperatures. Our study highlights the importance of biochemical investigations in understanding the proximate mechanisms by which temperature affects embryonic development.

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Related in: MedlinePlus

Developmental rates (a) and instantaneous developmental rates (wet mass) (b) of embryos incubated under different temperatures.Developmental rate (DR) at each temperature (T) was calculated by dividing the incubation duration by the shortest incubation duration recorded in the laboratory, and taking the inverse of this value. Data were obtained from Du and Ji, 2003 (a)35 and from Yang et al., 2002 (b)36.
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f1: Developmental rates (a) and instantaneous developmental rates (wet mass) (b) of embryos incubated under different temperatures.Developmental rate (DR) at each temperature (T) was calculated by dividing the incubation duration by the shortest incubation duration recorded in the laboratory, and taking the inverse of this value. Data were obtained from Du and Ji, 2003 (a)35 and from Yang et al., 2002 (b)36.

Mentions: The development of reptilian embryos involves two distinct but related processes: differentiation and growth11. The developmental rate of embryos is enhanced with increasing temperature, and this temperature effect is universally observed in almost all studied species of ectothermic animals such as insects, fish, and reptiles312. As in other ectothermic animals, developmental rate increases exponentially with temperature in reptile embryos13. For example, developmental rate is enhanced with increasing temperature in the embryos of the Chinese softshell turtle Pelodiscus sinensis, a species with a widespread distribution across China and Southeast Asia (Fig. 1a). In addition, the instantaneous developmental rate (i.e., the slope of the developmental curve) increases with temperature, and the among-temperature difference in instantaneous developmental rate becomes larger as embryonic development proceeds over most of the incubation period (70%) in this species (Fig. 1b). How might turtle embryos develop more rapidly at high temperatures? The developmental rate depends on the metabolic rate, that is, the rates of energy utilization, transformation, and allocation1415, which are in turn related to the function of mitochondria16.To enhance its developmental rate, an embryo may increase energy metabolism with increasing temperature. In addition to this same general rule of biochemical reactions underpinning all life activities, we envisage another potential pathway that an embryo might use to enhance its developmental rate. That is, the mitochondrial energy metabolism of embryos at high temperatures could be further enhanced through developmental plasticity or thermal acclimation, because both developmental plasticity1718 and thermal acclimation9 may modify physiological and biochemical responses to temperature. In this study, we incubated P. sinensis eggs under 24, 28 and 32°C respectively and measured mitochondrial respiration, activities of aerobic metabolic enzyme (COX) and anaerobic metabolic enzyme (LDH) of P. sinensis embryos at different test temperatures of 24, 28 and 32°C. By determining the effects of incubation and test temperatures on mitochondrial traits and metabolic enzyme activities, we aimed to identify how turtle embryos enhance developmental rate at high temperatures, and thereby test for the proposed hypothesis.


High incubation temperatures enhance mitochondrial energy metabolism in reptile embryos.

Sun BJ, Li T, Gao J, Ma L, Du WG - Sci Rep (2015)

Developmental rates (a) and instantaneous developmental rates (wet mass) (b) of embryos incubated under different temperatures.Developmental rate (DR) at each temperature (T) was calculated by dividing the incubation duration by the shortest incubation duration recorded in the laboratory, and taking the inverse of this value. Data were obtained from Du and Ji, 2003 (a)35 and from Yang et al., 2002 (b)36.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4352865&req=5

f1: Developmental rates (a) and instantaneous developmental rates (wet mass) (b) of embryos incubated under different temperatures.Developmental rate (DR) at each temperature (T) was calculated by dividing the incubation duration by the shortest incubation duration recorded in the laboratory, and taking the inverse of this value. Data were obtained from Du and Ji, 2003 (a)35 and from Yang et al., 2002 (b)36.
Mentions: The development of reptilian embryos involves two distinct but related processes: differentiation and growth11. The developmental rate of embryos is enhanced with increasing temperature, and this temperature effect is universally observed in almost all studied species of ectothermic animals such as insects, fish, and reptiles312. As in other ectothermic animals, developmental rate increases exponentially with temperature in reptile embryos13. For example, developmental rate is enhanced with increasing temperature in the embryos of the Chinese softshell turtle Pelodiscus sinensis, a species with a widespread distribution across China and Southeast Asia (Fig. 1a). In addition, the instantaneous developmental rate (i.e., the slope of the developmental curve) increases with temperature, and the among-temperature difference in instantaneous developmental rate becomes larger as embryonic development proceeds over most of the incubation period (70%) in this species (Fig. 1b). How might turtle embryos develop more rapidly at high temperatures? The developmental rate depends on the metabolic rate, that is, the rates of energy utilization, transformation, and allocation1415, which are in turn related to the function of mitochondria16.To enhance its developmental rate, an embryo may increase energy metabolism with increasing temperature. In addition to this same general rule of biochemical reactions underpinning all life activities, we envisage another potential pathway that an embryo might use to enhance its developmental rate. That is, the mitochondrial energy metabolism of embryos at high temperatures could be further enhanced through developmental plasticity or thermal acclimation, because both developmental plasticity1718 and thermal acclimation9 may modify physiological and biochemical responses to temperature. In this study, we incubated P. sinensis eggs under 24, 28 and 32°C respectively and measured mitochondrial respiration, activities of aerobic metabolic enzyme (COX) and anaerobic metabolic enzyme (LDH) of P. sinensis embryos at different test temperatures of 24, 28 and 32°C. By determining the effects of incubation and test temperatures on mitochondrial traits and metabolic enzyme activities, we aimed to identify how turtle embryos enhance developmental rate at high temperatures, and thereby test for the proposed hypothesis.

Bottom Line: We measured mitochondrial respiration and metabolic enzyme activities of turtle embryos (Pelodiscus sinensis) incubated at different temperatures to identify the metabolic basis of the rapid development occurring at high temperatures in reptile embryos.Developmental rate increased with increasing incubation temperatures in the embryos of P. sinensis.Our study highlights the importance of biochemical investigations in understanding the proximate mechanisms by which temperature affects embryonic development.

View Article: PubMed Central - PubMed

Affiliation: Key Laboratory of Animal Ecology and Conservational Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, People's Republic of China.

ABSTRACT
Developmental rate increases exponentially with increasing temperature in ectothermic animals, but the biochemical basis underlying this thermal dependence is largely unexplored. We measured mitochondrial respiration and metabolic enzyme activities of turtle embryos (Pelodiscus sinensis) incubated at different temperatures to identify the metabolic basis of the rapid development occurring at high temperatures in reptile embryos. Developmental rate increased with increasing incubation temperatures in the embryos of P. sinensis. Correspondingly, in addition to the thermal dependence of mitochondrial respiration and metabolic enzyme activities, high-temperature incubation further enhanced mitochondrial respiration and COX activities in the embryos. This suggests that embryos may adjust mitochondrial respiration and metabolic enzyme activities in response to developmental temperature to achieve high developmental rates at high temperatures. Our study highlights the importance of biochemical investigations in understanding the proximate mechanisms by which temperature affects embryonic development.

Show MeSH
Related in: MedlinePlus