蝙蝠核心生物钟基因Per1昼夜表达节律与适应性进化研究

王慧; 许宁宁; 李昕彤; 冯江

doi:10.16829/j.slxb.150882

兽类学报 >

2024 , Vol. 44 >Issue 3: 259 - 267

DOI: https://doi.org/10.16829/j.slxb.150882

研究论文

蝙蝠核心生物钟基因Per1昼夜表达节律与适应性进化研究

王慧 ,
许宁宁 ,
李昕彤 ,
冯江

展开

1 吉林农业大学生命科学学院, 长春 130118;
2 东北师范大学, 吉林省动物资源保护与利用重点实验室, 长春 130117

王慧(1989-)，女，博士，副教授，主要从事动物分子生态学研究.

收稿日期: 2023-12-05

修回日期: 2024-03-12

网络出版日期: 2024-05-31

基金资助

国家自然科学基金 (32371561)；2022年国家级全国大学生创新创业项目

收起

The circadian expression rhythms and adaptive evolution of the core circadian clock gene Per1 in bats

WANG Hui ,
XU Ningning ,
LI Xintong ,
FENG Jiang

Expand

1 College of Life Science, Jilin Agricultural University, Changchun 130118, China;
2 Jilin Provincial Key Laboratory of Animal Resource Conservation and Utilization, Northeast Normal University, Changchun 130117, China

Received date: 2023-12-05

Revised date: 2024-03-12

Online published: 2024-05-31

Fold

摘要

长期以来，生物钟相关研究一直是生命科学领域的热点话题。以往研究表明核心生物钟基因 Per1 广泛参与哺乳动物昼夜节律调控。然而，Per1 基因在具有不同昼夜节律活动模式的哺乳动物中是否发生了遗传位点改变，以及这些改变是否促进了哺乳动物昼夜活动模式的形成和稳定仍有待研究。本研究通过荧光定量 PCR、基因克隆测序与分子进化分析方法，对核心生物钟基因 Per1 开展了深入的分子进化分析，明确了 Per1 基因在夜行性蝙蝠脑区的昼夜振荡规律，由休息状态到睡眠状态对应着 Per1 基因表达量的由高到低，睡眠状态的表达量最低，而由觉醒状态到活动状态对应着 Per1 基因表达量的持续升高，与 Per1 基因维持中枢生物钟调控功能高度相关；检测到 Per1 基因序列上的 15 个潜在受正选择位点与 2 个显著受正选择位点，其中在夜行性动物中检测到的显著受正选择的 1118A 氨基酸位点恰好位于该基因编码蛋白的功能域上；通过滑窗分析结果显示，Per1 基因在夜行性哺乳动物中的进化速率均普遍高于其在日行性哺乳动物中的进化速率，可能促进了哺乳动物夜行性活动模式的形成和稳定。本研究为深入理解哺乳动物自身稳态维持与适应环境周期性变化的关键分子基础提供新的认知，为生物钟相关研究提供思路和参考。

关键词： 生物钟; 夜行性哺乳动物; Per1基因; 昼夜节律; 适应性进化

本文引用格式

王慧 , 许宁宁 , 李昕彤 , 冯江 . 蝙蝠核心生物钟基因Per1昼夜表达节律与适应性进化研究[J]. 兽类学报, 2024 , 44(3) : 259 -267 . DOI: 10.16829/j.slxb.150882

Abstract

For a long time, research on circadian clock has been a hot topic in the field of life science. Previous studies have shown that the core clock gene Per1 is widely involved in the regulation of mammalian circadian rhythms. However, limited understanding of the adaptive sites evolved in the sequence of Per1 gene. And whether these adaptive alterations may promote the formation and stabilization of mammalian diurnal activity patterns remains to be investigated. In this study, we conducted in-depth molecular evolution analyses of the core clock gene Per1 through the real-time quantitative PCR, gene cloning sequencing and molecular evolution analysis. We have identified the circadian oscillation patterns of Per1 gene expressed in the brain of bats, from rest state to sleep state corresponding with the expression level of Per1 gene changed from high to low, and the sleep state showing the lowest expression level, while from wake state to active state, its expression level increased continuously, which was highly correlated with the maintenance of the central biological clock regulation function of Per1 gene. There were 15 potential and 2 significant positively selected sites were detected on the Per1 gene sequence, and one of the significant positively selected sites, 1118A amino acid site detected in nocturnal animals was found to be located on the functional domain of the gene encoded protein sequence. We also found that the evolution rate of Per1 gene in nocturnal mammals was generally higher than that in diurnal mammals, indicating that the core clock gene Per1 experienced strong selective pressures during the evolution of nocturnal mammals, further promoted the formation and stabilization of nocturnal activity patterns in mammals. This study provides a new understanding of the key molecular basis of mammalian homeostasis maintenance and adaptation to the periodically changing environmental conditions, and provides ideas and references for circadian clock related studies.

Key words： Circadian clock; Nocturnal mammals; Per1 gene; Circadian rhythms; Adaptive evolution

参考文献

Álvarez-Carretero S, Kapli P, Yang Z. 2023. Beginner’s guide on the use of PAML to detect positive selection. Molecular Biology and Evolution, 40: msad041.
Asai M, Yoshinobu Y, Kaneko S, Mori A, Nikaido T, Moriya T, Akiyama M, Shibata S. 2001. Circadian profile of Per gene mRNA expression in the suprachiasmatic nucleus, paraventricular nucleus, and pineal body of aged rats. Journal of Neuroscience Research, 66: 1133-1139.
Bae K, Jin X, Maywood E S, Hastings M H, Reppert S M, Weaver D R. 2001. Differential functions of mPer1, mPer2, and mPer3 in the SCN circadian clock. Neuron, 30: 525-536.
Bogdanowicz W, Kasper S, Owen R D. 1998. Phylogeny of plecotine bats: reevaluation of morphological and chromosomal data. Journal of Mammalogy, 79: 78-90.
Brunswick C A, Baldwin D J, Bodinayake K K, McKenna A R, Lo C Y, Bellfy L, Urban M W, Stuart E M, Murakami S, Smies C W. 2023. The clock gene Per1 is necessary in the retrosplenial cortex-but not in the suprachiasmatic nucleus for incidental learning in young and aging male mice. Neurobiology of Aging, 126: 77-90.
Cano P, Poliandri A H B, Jimnez V. 2007. Cadmium-induced changes in Per 1 and Per 2 gene expression in rat hypothalamus and anterior pituitary: effect of melatonin. Toxicology Letters, 172:131-136.
Dardente H, Dardente H, Cermakian N. 2007. Molecular circadian rhythms in central and peripheral clocks in mammals. Chronobiology International, 24: 195-213.
Darriba D, Taboada G L, Doallo R, Posada D. 2012. jModelTest 2:more models, new heuristics and high-performance computing. Nature Methods, 9: 772.
Duffield G E, Best J D, Meurers B H, Bittner A, Loros J J, Dunlap J C. 2002. Circadian programs of transcriptional activation, signaling, and protein turnover revealed by microarray analysis of mammalian cells. Current Biology, 12: 551-557.
Fernandes J M, Ruangsri J, Kiron V. 2010. Atlantic cod piscidin and its diversification through positive selection. PLoS ONE, 5:e9501.
Fletcher W, Yang Z. 2010. The effect of insertions, deletions, and alignment errors on the branch-site test of positive selection. Molecular Biology and Evolution, 27: 2257-2267.
Ge W H, Sun Q, Yang Y X, Ding Z, Liu J H, Zhang J F. 2023. Circadian PER1 controls daily fat absorption with the regulation of PER1-PKA on phosphorylation of bile acid synthetase. Journal of Lipid Research, 64: 1-14.
Guan D, Lazar M A. 2021. Interconnections between circadian clocks and metabolism. The Journal of Clinical Investigation, 131:1-15.
Hall T, Biosciences I, Carlsbad C. 2011. BioEdit: an important software for molecular biology. GERF Bull Biosci, 2: 60-61.
Hao H, Allen D L, Hardin P E. 1997. A circadian enhancer mediates PER-dependent mRNA cycling in Drosophila melanogaster. Molecular and Cellular Biology, 17: 3687-3693.
Jankunis E S, Whishaw I Q. 2013. Sucrose Bobs and Quinine Gapes:horse (Equus caballus) responses to taste support phylogenetic similarity in taste reactivity. Behavioural Brain Research, 256:284-290.
Jones J R, McMahon D G. 2016. The core clock gene Per1 phases molecular and electrical circadian rhythms in SCN neurons. PeerJ, 4: e2297.
Kunz T H, Fenton M B. 2005. Bat Ecology. Chicago: University of Chicago Press.
King D P, Takahashi J S. 2000. Molecular genetics of circadian rhythms in mammals. Annual Review of Neuroscience, 23:713-742.
Lalitha S. 2000. Primer premier 5. Biotech Software & Internet Report: The Computer Software Journal for Scient, 1: 270-272.
Lin B Z, Sasazaki S, Mannen H. 2010. Genetic diversity and structure in Bos taurus and Bos indicus populations analyzed by SNP markers. Animal Science Journal, 81: 281-289.
Luo P H. 2020. Circadian activity and expression pattern of circadian genes of the tree shrew. Ph. D thesis. Hefei: Unversity of Science and Technology of China. (in Chinese)
McCrea D A, Rybak I A. 2008. Organization of mammalian locomotor rhythm and pattern generation. Brain Research Reviews, 57:134-146.
Michaux J, Reyes A, Catzeflis F. 2001. Evolutionary history of the most speciose mammals: molecular phylogeny of muroid rodents. Molecular Biology and Evolution, 18: 2017-2031.
Mizuno T, Higo S, Kamei N, Mori K, Sakamoto A, Ozawa H. 2022. Effects of general anesthesia on behavioral circadian rhythms and clock-gene expression in the suprachiasmatic nucleus in rats. Histochemistry and Cell Biology, 158: 149-158.
Mure L S, Le H D, Benegiamo G, Chang M W, Rios L, Jillani N, Ngotho M, Kariuki T, Dkhissi-Benyahya O, Cooper H M. 2018. Diurnal transcriptome atlas of a primate across major neural and peripheral tissues. Science, 359: eaao0318.
Nishide S, Hashimoto K, Nishio T, Honma K, Honma S. 2014. Organ-specific development characterizes circadian clock gene Per2 expression in rats. American Journal of PhysiologyRegulatory, Integrative and Comparative Physiology, 306: R67-R74.
Osborne C, Cryan P M, O’Shea T J, Oko L M, Ndaluka C, Calisher C H, Berglund A D, Klavetter M L, Bowen R A, Holmes K V. 2011. Alphacoronaviruses in New World bats: prevalence, persistence, phylogeny, and potential for interaction with humans. PLoS ONE, 6: e19156.
Pride D. 2000. SWAAP: a tool for analyzing substitutions and similarity in multiple alignments. Version 1. 0. 2.
Rychlik W. 2007. OLIGO 7 primer analysis software. PCR Primer Design, 35-59.
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version 6. 0. Molecular Biology and Evolution, 30: 2725-2729.
Vitaterna M H, Takahashi J S, Turek F W. 2001. Overview of circadian rhythms. Alcohol Research & Health, 25: 85.
Xin H R, Huang R F, Zhou M Y, Chen J H, Zhang J X, Zhou T T, Ji S S, Liu X, Tian H, Lam S M, Bao X Y, ,Li L H, Tong S F, Deng F, Shui G H, Zhang Z H, Wong C C L, Li M D. 2023. Daytimerestricted feeding enhances running endurance without prior exercise in mice. Nature Metabolism, 5 (7): 1236-1251.
Yang Z. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution, 24: 1586-1591.
Yang Z, Wong W S, Nielsen R. 2005. Bayes empirical Bayes inference of amino acid sites under positive selection. Molecular Biology and Evolution, 22: 1107-1118.
罗鹏昊. 2020. 树鼩节律活动及节律基因表达调控的研究. 合肥:中国科学技术大学博士学位论文.

Options

文章导航

模态框（Modal）标题

摘要

本文引用格式

Abstract

参考文献