Mitochondrial Protein-Coding Gene Expression in the Lizard Sphenomorphus incognitus (Squamata: Scincidae) Responding to Different Temperature Stresses

Animals Pub Date : 2024-06-03 DOI:10.3390/ani14111671
Lemei Zhan, Jingyi He, Siqi Meng, Zhiqiang Guo, Yuxin Chen, Kenneth B. Storey, Jiayong Zhang, Danna Yu
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Abstract

In the context of global warming, the frequency of severe weather occurrences, such as unexpected cold spells and heat waves, will grow, as well as the intensity of these natural disasters. Lizards, as a large group of reptiles, are ectothermic. Their body temperatures are predominantly regulated by their environment and temperature variations directly impact their behavior and physiological activities. Frequent cold periods and heat waves can affect their biochemistry and physiology, and often their ability to maintain their body temperature. Mitochondria, as the center of energy metabolism, are crucial for maintaining body temperature, regulating metabolic rate, and preventing cellular oxidative damage. Here, we used RT-qPCR technology to investigate the expression patterns and their differences for the 13 mitochondrial PCGs in Sphenomorphus incognitus (Squamata:Scincidae), also known as the brown forest skink, under extreme temperature stress at 4 °C, 8 °C, 34 °C, and 38 °C for 24 h, compared to the control group at 25 °C. In southern China, for lizards, 4 °C is close to lethal, and 8 °C induces hibernation, while 34/38 °C is considered hot and environmentally realistic. Results showed that at a low temperature of 4 °C for 24 h, transcript levels of ATP8, ND1, ND4, COI, and ND4L significantly decreased, to values of 0.52 ± 0.08, 0.65 ± 0.04, 0.68 ± 0.10, 0.28 ± 0.02, and 0.35 ± 0.02, respectively, compared with controls. By contrast, transcript levels of COⅢ exhibited a significant increase, with a mean value of 1.86 ± 0.21. However, exposure to 8 °C for 24 h did not lead to an increase in transcript levels. Indeed, transcript levels of ATP6, ATP8, ND1, ND3, and ND4 were significantly downregulated, to 0.48 ± 0.11, 0.68 ± 0.07, 0.41 ± 0.08, 0.54 ± 0.10, and 0.52 ± 0.07, respectively, as compared with controls. Exposure to a hot environment of 34 °C for 24 h led to an increase in transcript levels of COI, COⅡ, COⅢ, ND3, ND5, CYTB, and ATP6, with values that were 3.3 ± 0.24, 2.0 ± 0.2, 2.70 ± 1.06, 1.57 ± 0,08, 1.47 ± 0.13, 1.39 ± 0.56, and 1.86 ± 0.12, respectively, over controls. By contrast, ND4L exhibited a significant decrease (to 0.31 ± 0.01) compared with controls. When exposed to 38 °C, the transcript levels of the 13 PCGs significantly increased, ranging from a 2.04 ± 0.23 increase in ND1 to a 6.30 ± 0.96 rise in ND6. Under two different levels of cold and heat stress, the expression patterns of mitochondrial genes in S. incognitus vary, possibly associated with different strategies employed by this species in response to low and high temperatures, allowing for rapid compensatory adjustments in mitochondrial electron transport chain proteins in response to temperature changes. Furthermore, this underscores once again the significant role of mitochondrial function in determining thermal plasticity in reptiles.
不同温度胁迫下蜥蜴线粒体蛋白编码基因的表达
在全球变暖的背景下,恶劣天气(如突如其来的寒流和热浪)发生的频率和强度都将增加。蜥蜴作为爬行动物中的一大类,属于外温动物。它们的体温主要受环境调节,温度变化直接影响它们的行为和生理活动。频繁的寒冷期和热浪会影响它们的生物化学和生理学,往往也会影响它们维持体温的能力。线粒体作为能量代谢的中心,对维持体温、调节代谢率和防止细胞氧化损伤至关重要。本文采用RT-qPCR技术,研究了褐林鼬在4 °C、8 °C、34 °C和38 °C的极端温度胁迫下24 h内13种线粒体PCGs的表达模式及其与25 °C对照组的差异。在中国南方,对于蜥蜴来说,4 °C接近致命温度,8 °C会导致冬眠,而34/38 °C被认为是高温且符合环境实际情况的温度。结果表明,与对照组相比,在4℃低温条件下24小时,ATP8、ND1、ND4、COI和ND4L的转录水平显著下降,分别为0.52 ± 0.08、0.65 ± 0.04、0.68 ± 0.10、0.28 ± 0.02和0.35 ± 0.02。相比之下,COⅢ的转录物水平有显著增加,平均值为 1.86 ± 0.21。然而,暴露于 8 °C 24 小时并不会导致转录本水平的增加。事实上,与对照组相比,ATP6、ATP8、ND1、ND3 和 ND4 的转录水平明显下调,分别为 0.48 ± 0.11、0.68 ± 0.07、0.41 ± 0.08、0.54 ± 0.10 和 0.52 ± 0.07。与对照组相比,暴露于 34 °C 的高温环境 24 小时后,COI、COⅡ、COⅢ、ND3、ND5、CYTB 和 ATP6 的转录本水平分别为 3.3 ± 0.24、2.0 ± 0.2、2.70 ± 1.06、1.57 ± 0.08、1.47 ± 0.13、1.39 ± 0.56 和 1.86 ± 0.12。相比之下,与对照组相比,ND4L 出现了显著下降(降至 0.31 ± 0.01)。当暴露于 38 °C时,13 种 PCGs 的转录水平显著上升,从 ND1 的 2.04 ± 0.23 到 ND6 的 6.30 ± 0.96 不等。在两种不同程度的冷热胁迫下,S. incognitus 线粒体基因的表达模式各不相同,这可能与该物种在应对低温和高温时采用的不同策略有关,从而使线粒体电子传递链蛋白能够根据温度变化进行快速补偿调整。此外,这也再次强调了线粒体功能在决定爬行动物热可塑性方面的重要作用。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
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