دورية أكاديمية
Variation in mitochondrial DNA affects locomotor activity and sleep in Drosophila melanogaster.
العنوان: | Variation in mitochondrial DNA affects locomotor activity and sleep in Drosophila melanogaster. |
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المؤلفون: | Anderson L; Institute of Ecology and Evolution, School of Biological Sciences, University of Edinburgh, Edinburgh, UK., Camus MF; Research Department of Genetics, Evolution and Environment, University College London, Gower Street, London, WC1E 6BT, UK., Monteith KM; Institute of Ecology and Evolution, School of Biological Sciences, University of Edinburgh, Edinburgh, UK., Salminen TS; Faculty of Medicine and Health Technology, Tampere University, Tampere, Finland., Vale PF; Institute of Ecology and Evolution, School of Biological Sciences, University of Edinburgh, Edinburgh, UK. pedro.vale@ed.ac.uk. |
المصدر: | Heredity [Heredity (Edinb)] 2022 Oct; Vol. 129 (4), pp. 225-232. Date of Electronic Publication: 2022 Jun 28. |
نوع المنشور: | Journal Article; Research Support, Non-U.S. Gov't |
اللغة: | English |
بيانات الدورية: | Publisher: Nature Publishing Group Country of Publication: England NLM ID: 0373007 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1365-2540 (Electronic) Linking ISSN: 0018067X NLM ISO Abbreviation: Heredity (Edinb) Subsets: MEDLINE |
أسماء مطبوعة: | Publication: <2003->: London : Nature Publishing Group Original Publication: London, Oliver and Boyd. |
مواضيع طبية MeSH: | DNA, Mitochondrial*/genetics , Drosophila melanogaster*/genetics, Adenosine Triphosphate/metabolism ; Animals ; Drosophila/genetics ; Female ; Locomotion/genetics ; Male ; Mitochondria/genetics ; Sleep/genetics |
مستخلص: | Mitochondria are organelles that produce cellular energy in the form of ATP through oxidative phosphorylation, and this primary function is conserved among many taxa. Locomotion is a trait that is highly reliant on metabolic function and expected to be greatly affected by disruptions to mitochondrial performance. To this end, we aimed to examine how activity and sleep vary between Drosophila melanogaster strains with different geographic origins, how these patterns are affected by mitochondrial DNA (mtDNA) variation, and how breaking up co-evolved mito-nuclear gene combinations affect the studied activity traits. Our results demonstrate that Drosophila strains from different locations differ in sleep and activity, and that females are generally more active than males. By comparing activity and sleep of mtDNA variants introgressed onto a common nuclear background in cytoplasmic hybrid (cybrid) strains, we were able to quantify the among-line variance attributable to mitochondrial DNA, and we establish that mtDNA variation affects both activity and sleep, in a sex-specific manner. Altogether our study highlights the important role that mitochondrial genome variation plays on organismal physiology and behaviour. (© 2022. The Author(s).) |
References: | Anderson S, Bankier AT, Barrell BG, de Bruijn MH, Coulson AR, Drouin J et al. (1981) Sequence and organization of the human mitochondrial genome. Nature 290(5806):457–465. (PMID: 721953410.1038/290457a0) Andretic R, Shaw PJ (2005) Essentials of sleep recordings in Drosophila: moving beyond sleep time. Methods Enzymol 393:759–772. (PMID: 1581732310.1016/S0076-6879(05)93040-1) Andreu AL, Hanna MG, Reichmann H, Bruno C, Penn AS, Tanji K et al. (1999) Exercise intolerance due to mutations in the cytochrome b gene of mitochondrial DNA. N Engl J Med 341(14):1037–1044. (PMID: 1050259310.1056/NEJM199909303411404) Bar S, Prasad M, Datta R (2018) Neuromuscular degeneration and locomotor deficit in a Drosophila model of mucopolysaccharidosis VII is attenuated by treatment with resveratrol. Dis Models Mech 11(11):dmm036954. (PMID: 10.1242/dmm.036954) Bates D, Maechler M, Bolkler B (2012) lme4: Linear mixed-effects models using S4 classes. R package version 0999999-0. https://cran.r-project.org/web/packages/lme4/index.html. Brunetti V, Della Marca G, Servidei S, Primiano G (2021) Sleep disorders in mitochondrial diseases. Curr Neurol Neurosci Rep. 21(7):30. (PMID: 33948737809674310.1007/s11910-021-01121-2) Buchanan JL, Meiklejohn CD, Montooth KL (2018) Mitochondrial dysfunction and infection generate immunity-fecundity tradeoffs in Drosophila. Integr Comp Biol 58(3):591–603. (PMID: 29945242614541510.1093/icb/icy078) Bushey D, Huber R, Tononi G, Cirelli C (2007) Drosophila Hyperkinetic mutants have reduced sleep and impaired memory. J Neurosci 27(20):5384–5393. (PMID: 17507560667233810.1523/JNEUROSCI.0108-07.2007) Bushey D, Hughes KA, Tononi G, Cirelli C (2010) Sleep, aging, and lifespan in Drosophila. BMC Neurosci 11:56. (PMID: 20429945287126810.1186/1471-2202-11-56) Camus MF, Clancy DJ, Dowling DK (2012) Mitochondria, maternal inheritance, and male aging. Curr Biol 22(18):1717–1721. (PMID: 2286331310.1016/j.cub.2012.07.018) Camus MF, Dowling DK (2018) Mitochondrial genetic effects on reproductive success: signatures of positive intrasexual, but negative intersexual pleiotropy. Proc Biol Sci 285:1879. Camus MF, O’Leary M, Reuter M, Lane N (2020) Impact of mito-nuclear interactions on life-history responses to diet. Philos Trans R Soc Lond B Biol Sci 375(1790):20190416. (PMID: 3178703710.1098/rstb.2019.0416) Camus MF, Wolf JB, Morrow EH, Dowling DK (2015) Single nucleotides in the mtDNA sequence modify mitochondrial molecular function and are associated with sex-specific effects on fertility and aging. Curr Biol 25(20):2717–2722. (PMID: 2645530910.1016/j.cub.2015.09.012) Camus MF, Wolff JN, Sgrò CM, Dowling DK (2017) Experimental Support That Natural Selection Has Shaped the Latitudinal Distribution of Mitochondrial Haplotypes in Australian Drosophila melanogaster. Mol Biol Evol 34:2600–2612. (PMID: 2863721710.1093/molbev/msx184) Carnegie L, Reuter M, Fowler K, Lane N, Camus MF (2021) Mother’s curse is pervasive across a large mito-nuclear Drosophila panel. Evol Lett 5(3):230–239. (PMID: 34136271819044610.1002/evl3.221) Chandel NS (2015) Evolution of mitochondria as signaling organelles. Cell Metab 22:204–206. (PMID: 2607349410.1016/j.cmet.2015.05.013) Chiu JC, Low KH, Pike DH, Yildirim E, Edery I (2010) Assaying locomotor activity to study circadian rhythms and sleep parameters in Drosophila. JoVE (Journal of Visualized Experiments), (43):e2157. Cirelli C, Bushey D, Hill S, Huber R, Kreber R, Ganetzky B et al. (2005) Reduced sleep in Drosophila Shaker mutants. Nature 434(7037):1087–1092. (PMID: 1585856410.1038/nature03486) Clancy DJ (2008) Variation in mitochondrial genotype has substantial lifespan effects which may be modulated by nuclear background. Aging Cell 7(6):795–804. (PMID: 1872770410.1111/j.1474-9726.2008.00428.x) Clancy DJ, Hime GR, Shirras AD (2011) Cytoplasmic male sterility in Drosophila melanogaster associated with a mitochondrial CYTB variant. Heredity 107(4):374–376. (PMID: 21407254318249510.1038/hdy.2011.12) Crocker A, Sehgal A (2010) Genetic analysis of sleep. Genes Dev 24(12):1220–1235. (PMID: 20551171288565810.1101/gad.1913110) DiMauro S, Schon EA (2003) Mitochondrial respiratory-chain diseases. N Engl J Med 348(26):2656–2668. (PMID: 1282664110.1056/NEJMra022567) Dowling DK, Adrian RE (2019) Challenges and prospects for testing the mother’s curse hypothesis. Integr Comp Biol 59(4):875–889. (PMID: 3122559110.1093/icb/icz110) Filler K, Lyon D, Bennett J, McCain N, Elswick R, Lukkahatai N et al. (2014) Association of mitochondrial dysfunction and fatigue: a review of the literature. BBA Clin 1:12–23. (PMID: 25147756413652910.1016/j.bbacli.2014.04.001) Fogle KJ, Mobini CL, Paseos AS, Palladino MJ (2019) Sleep and circadian defects in a Drosophila model of mitochondrial encephalomyopathy. Neurobiol Sleep Circadian Rhythms 6:44–52. (PMID: 30868108641107310.1016/j.nbscr.2019.01.003) Fox J, Weisberg S (2011). An R companion to applied regression, Second Edition. Frank SA (2012) Evolution: mitochondrial burden on male health. Curr Biol 22(18):R797–799. (PMID: 2301799210.1016/j.cub.2012.07.066) Ganguly-Fitzgerald I, Donlea J, Shaw PJ (2006) Waking experience affects sleep need in Drosophila. Science 313(5794):1775–1781. (PMID: 1699054610.1126/science.1130408) Gemmell NJ, Metcalf VJ, Allendorf FW (2004) Mother’s curse: the effect of mtDNA on individual fitness and population viability. Trends Ecol Evol 19(5):238–244. (PMID: 1670126210.1016/j.tree.2004.02.002) Ghaoui R, Sue CM (2018) Movement disorders in mitochondrial disease. J Neurol 265(5):1230–1240. (PMID: 2930700810.1007/s00415-017-8722-6) Ghimire S, Kim MS (2015) Enhanced locomotor activity is required to exert dietary restriction-dependent increase of stress resistance in Drosophila. Oxid Med Cell Longev 2015:813801–813801. (PMID: 26060531442780010.1155/2015/813801) Gray MW, Burger G, Cedergren R, Golding GB, Lemieux C, Sankoff D et al. (1999a) A genomics approach to mitochondrial evolution. Biol Bull 196(3):400–403. (PMID: 2829648710.2307/1542980) Gray MW, Burger G, Lang BF (1999b) Mitochondrial evolution. Science 283(5407):1476–1481. (PMID: 1006616110.1126/science.283.5407.1476) Gupta V, Stewart CO, Rund SSC, Monteith K, Vale PF (2017) Costs and benefits of sublethal Drosophila C virus infection. J Evol Biol 30:1325–1335. (PMID: 2842517410.1111/jeb.13096) Harbison ST, McCoy LJ, Mackay TF (2013) Genome-wide association study of sleep in Drosophila melanogaster. BMC Genom 14:281. (PMID: 10.1186/1471-2164-14-281) Hendricks JC, Finn SM, Panckeri KA, Chavkin J, Williams JA, Sehgal A et al. (2000) Rest in Drosophila is a sleep-like state. Neuron 25(1):129–138. (PMID: 1070797810.1016/S0896-6273(00)80877-6) Hyde JF, Jerussi TP (1983) Sexual dimorphism in rats with respect to locomotor activity and circling behavior. Pharmacol Biochem Behav 18:725–729. (PMID: 685664710.1016/0091-3057(83)90014-X) Hill GE, Havird JC, Sloan DB, Burton RS, Greening C, Dowling DK (2019) Assessing the fitness consequences of mito-nuclear interactions in natural populations. Biol Rev Camb Philos Soc 94(3):1089–1104. (PMID: 3058872610.1111/brv.12493) Hoekstra LA, Siddiq MA, Montooth KL (2013) Pleiotropic effects of a mitochondrial–nuclear incompatibility depend upon the accelerating effect of temperature in Drosophila. Genetics 195(3):1129–1139. (PMID: 24026098381384210.1534/genetics.113.154914) Holmbeck MA, Donner JR, Villa-Cuesta E, Rand DM (2015) A Drosophila model for mito-nuclear diseases generated by an incompatible interaction between tRNA and tRNA synthetase. Dis Model Mech 8(8):843–854. (PMID: 260353884527286) Isaac RE, Li C, Leedale AE, Shirras AD (2010) Drosophila male sex peptide inhibits siesta sleep and promotes locomotor activity in the post-mated female. Proc Biol Sci 277(1678):65–70. (PMID: 19793753) Lang BF, Gray MW, Burger G (1999) Mitochondrial genome evolution and the origin of eukaryotes. Annu Rev Genet 33:351–397. (PMID: 1069041210.1146/annurev.genet.33.1.351) Lemon J (2016) Plotrix: a package in the red light district of R. R-N. 6(4):8–12. Lewis E (1960) A new standard food medium. Drosoph Inform Serv 34(117):1–55. Long TA, Rice WR (2007) Adult locomotory activity mediates intralocus sexual conflict in a laboratory-adapted population of Drosophila melanogaster. Proc Biol Sci 274(1629):3105–3112. (PMID: 179252792293944) Meiklejohn CD, Holmbeck MA, Siddiq MA, Abt DN, Rand DM, Montooth KL (2013) An Incompatibility between a Mitochondrial tRNA and Its Nuclear-Encoded tRNA Synthetase Compromises Development and Fitness in Drosophila. PLoS Genet 9:e1003238. (PMID: 23382693356110210.1371/journal.pgen.1003238) Mossman JA, Ge JY, Navarro F, Rand DM (2019) Mitochondrial DNA fitness depends on nuclear genetic background in Drosophila. G3 9(4):1175–1188. (PMID: 30745378646941710.1534/g3.119.400067) Nagarajan-Radha V, Aitkenhead I, Clancy DJ, Chown SL, Dowling DK (2020) Sex-specific effects of mitochondrial haplotype on metabolic rate in Drosophila melanogaster support predictions of the Mother’s Curse hypothesis. Philos Trans R Soc Lond B Biol Sci 375(1790):20190178. (PMID: 3178703810.1098/rstb.2019.0178) Nitz DA, van Swinderen B, Tononi G, Greenspan RJ (2002) Electrophysiological correlates of rest and activity in Drosophila melanogaster. Curr Biol 12(22):1934–1940. (PMID: 1244538710.1016/S0960-9822(02)01300-3) Pichaud N, Berube R, Cote G, Belzile C, Dufresne F, Morrow G et al. (2019) Age-dependent dysfunction of mitochondrial and ROS metabolism induced by mito-nuclear mismatch. Front Genet 10:130. (PMID: 30842791639184910.3389/fgene.2019.00130) Potdar S, Sheeba V (2013) Lessons from sleeping flies: insights from Drosophila melanogaster on the neuronal circuitry and importance of sleep. J Neurogenet 27(1-2):23–42. (PMID: 2370141310.3109/01677063.2013.791692) Ramezani RJ, Stacpoole PW (2014) Sleep disorders associated with primary mitochondrial diseases. J Clin Sleep Med 10(11):1233–1239. (PMID: 25325607422472610.5664/jcsm.4212) Rand DM, Fry A, Sheldahl L (2006) Nuclear-mitochondrial epistasis and drosophila aging: introgression of Drosophila simulans mtDNA modifies longevity in D. melanogaster nuclear backgrounds. Genetics 172(1):329–341. (PMID: 16219776145616110.1534/genetics.105.046698) Rand DM, Haney RA, Fry AJ (2004) Cytonuclear coevolution: the genomics of cooperation. Trends Ecol Evol 19(12):645–653. (PMID: 1670132710.1016/j.tree.2004.10.003) Rechtschaffen A, Bergmann BM, Everson CA, Kushida CA, Gilliland MA (1989) Sleep deprivation in the rat: X. Integration and discussion of the findings. Sleep 12(1):68–87. (PMID: 264853310.1093/sleep/25.1.68) Robin ED, Wong R (1988) Mitochondrial DNA molecules and virtual number of mitochondria per cell in mammalian cells. J Cell Physiol 136(3):507–513. (PMID: 317064610.1002/jcp.1041360316) Rodrigues NR, Macedo GE, Martins IK, Gomes KK, de Carvalho NR, Posser T et al. (2018) Short-term sleep deprivation with exposure to nocturnal light alters mitochondrial bioenergetics in Drosophila. Free Radic Biol Med 120:395–406. (PMID: 2965586710.1016/j.freeradbiomed.2018.04.549) Ruiz-Pesini E, Lapena AC, Diez-Sanchez C, Perez-Martos A, Montoya J, Alvarez E et al. (2000) Human mtDNA haplogroups associated with high or reduced spermatozoa motility. Am J Hum Genet 67(3):682–696. (PMID: 10936107128752810.1086/303040) Sackton TB, Haney RA, Rand DM (2003) Cytonuclear coadaptation in Drosophila: disruption of cytochrome c oxidase activity in backcross genotypes. Evolution 57(10):2315–2325. (PMID: 1462891910.1111/j.0014-3820.2003.tb00243.x) Salminen TS, Cannino G, Oliveira MT, Lillsunde P, Jacobs HT, Kaguni LS (2019) Lethal interaction of nuclear and mitochondrial genotypes in Drosophila melanogaster. G3 9(7):2225–2234. (PMID: 31076384664388210.1534/g3.119.400315) Salminen TS, Oliveira MT, Cannino G, Lillsunde P, Jacobs HT, Kaguni LS (2017) Mitochondrial genotype modulates mtDNA copy number and organismal phenotype in Drosophila. Mitochondrion 34:75–83. (PMID: 2821456010.1016/j.mito.2017.02.001) Salminen TS, Vale PF (2020) Drosophila as a model system to investigate the effects of mitochondrial variation on innate immunity. Front Immunol 11:521. (PMID: 32269576710926310.3389/fimmu.2020.00521) Schon EA, DiMauro S, Hirano M (2012) Human mitochondrial DNA: roles of inherited and somatic mutations. Nat Rev Genet 13(12):878–890. (PMID: 23154810395976210.1038/nrg3275) Shaw PJ, Cirelli C, Greenspan RJ, Tononi G (2000) Correlates of sleep and waking in Drosophila melanogaster. Science 287(5459):1834–1837. (PMID: 1071031310.1126/science.287.5459.1834) Shaw PJ, Tononi G, Greenspan RJ, Robinson DF (2002) Stress response genes protect against lethal effects of sleep deprivation in Drosophila. Nature 417(6886):287–291. (PMID: 1201560310.1038/417287a) Smeitink J, van den Heuvel L, DiMauro S (2001) The genetics and pathology of oxidative phosphorylation. Nat Rev Genet 2(5):342–352. (PMID: 1133190010.1038/35072063) Sujkowski A, Spierer AN, Rajagopalan T, Bazzell B, Safdar M, Imsirovic D et al. (2019) Mito-nuclear interactions modify Drosophila exercise performance. Mitochondrion 47:188–205. (PMID: 3040859310.1016/j.mito.2018.11.005) Team RC (2019). R: a language and environment for statistical computing. R Foundation for Statistical Computing. Trivedi MS, Holger D, Bui AT, Craddock TJA, Tartar JL (2017) Short-term sleep deprivation leads to decreased systemic redox metabolites and altered epigenetic status. PLoS One 12(7):e0181978. (PMID: 28738082552432010.1371/journal.pone.0181978) Vale PF (2021) Data and code for Mitonuclear interactions affect locomotor activity and sleep in Drosophila melanogaster [Data set]. Zenodo https://doi.org/10.5281/zenodo.5573904. Vale PF, Jardine MD (2015) Sex-specific behavioural symptoms of viral gut infection and Wolbachia in Drosophila melanogaster. J Insect Physiol 82:28–32. (PMID: 2630152110.1016/j.jinsphys.2015.08.005) Vale PF, Siva-Jothy JA, Morrill A, Forbes MR (2018). The influence of parasites on insect behavior. In: Insect behavior: from mechanisms to ecological and evolutionary consequences, Oxford University Press. Vega-Naredo I, Loureiro R, Mesquita KA, Barbosa IA, Tavares LC, Branco AF et al. (2014) Mitochondrial metabolism directs stemness and differentiation in P19 embryonal carcinoma stem cells. Cell Death Differ 21(10):1560–1574. (PMID: 24832466415868210.1038/cdd.2014.66) Videlier M, Rundle HD, Careau V (2019) Sex-specific among-individual covariation in locomotor activity and resting metabolic rate in Drosophila melanogaster. Am Nat 194(6):E164–E176. (PMID: 3173810110.1086/705678) Vincent CM, Dionne MS (2021) Disparate regulation of IMD signaling drives sex differences in infection pathology in Drosophila melanogaster Proc Natl Acad Sci 118(32):e2026554118. (PMID: 34341118836418310.1073/pnas.2026554118) Wallace DC (1994) Mitochondrial DNA sequence variation in human evolution and disease. Proc Natl Acad Sci USA 91(19):8739–8746. (PMID: 80907164468210.1073/pnas.91.19.8739) Wang C, Youle RJ (2009) The role of mitochondria in apoptosis*. Annu Rev Genet 43(1):95–118. (PMID: 19659442476202910.1146/annurev-genet-102108-134850) Wickham H (2009). ggplot2: elegant graphics for data analysis. Use R: 1–212. Wickham H, Francois R, Henry L, Müller K (2019) dplyr: a grammar of data manipulation. R package version 0801:1–212. Willett CS, Burton RS (2003) Environmental influences on epistatic interactions: viabilities of cytochrome c genotypes in interpopulation crosses. Evolution 57(10):2286–2292. (PMID: 1462891610.1111/j.0014-3820.2003.tb00240.x) Yee WKW, Sutton KL, Dowling DK (2013) In vivo male fertility is affected by naturally occurring mitochondrial haplotypes. Curr Biol 23(2):R55–R56. (PMID: 2334793510.1016/j.cub.2012.12.002) Zhu C-T, Ingelmo P, Rand DM (2014) G×G×E for lifespan in drosophila: mitochondrial, nuclear, and dietary interactions that modify longevity. PLOS Genet 10(5):e1004354. (PMID: 24832080402246910.1371/journal.pgen.1004354) |
المشرفين على المادة: | 0 (DNA, Mitochondrial) 8L70Q75FXE (Adenosine Triphosphate) |
تواريخ الأحداث: | Date Created: 20220628 Date Completed: 20220930 Latest Revision: 20221110 |
رمز التحديث: | 20221213 |
مُعرف محوري في PubMed: | PMC9519576 |
DOI: | 10.1038/s41437-022-00554-w |
PMID: | 35764697 |
قاعدة البيانات: | MEDLINE |
تدمد: | 1365-2540 |
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DOI: | 10.1038/s41437-022-00554-w |