Daily Activity of the Housefly, Musca domestica, Is Influenced by Temperature Independent of 3' UTR period Gene Splicing
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
28620087
PubMed Central
PMC5555469
DOI
10.1534/g3.117.042374
PII: g3.117.042374
Knihovny.cz E-zdroje
- Klíčová slova
- circadian clock genes, locomotor activity, mRNA splicing, temperature compensation of circadian rhythms, transcription,
- MeSH
- 3' nepřekládaná oblast genetika MeSH
- časové faktory MeSH
- cirkadiánní rytmus genetika MeSH
- Drosophila melanogaster genetika MeSH
- exony genetika MeSH
- fotoperioda MeSH
- fylogeneze MeSH
- hmyzí geny * MeSH
- introny genetika MeSH
- kondiční příprava zvířat MeSH
- kryptochromy genetika MeSH
- messenger RNA genetika metabolismus MeSH
- moucha domácí MeSH
- pohybová aktivita MeSH
- promotorové oblasti (genetika) genetika MeSH
- regulace genové exprese MeSH
- sestřih RNA genetika MeSH
- teplota * MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- 3' nepřekládaná oblast MeSH
- kryptochromy MeSH
- messenger RNA MeSH
Circadian clocks orchestrate daily activity patterns and free running periods of locomotor activity under constant conditions. While the first often depends on temperature, the latter is temperature-compensated over a physiologically relevant range. Here, we explored the locomotor activity of the temperate housefly Musca domestica Under low temperatures, activity was centered round a major and broad afternoon peak, while high temperatures resulted in activity throughout the photophase with a mild midday depression, which was especially pronounced in males exposed to long photoperiods. While period (per) mRNA peaked earlier under low temperatures, no temperature-dependent splicing of the last per 3' end intron was identified. The expression of timeless, vrille, and Par domain protein 1 was also influenced by temperature, each in a different manner. Our data indicated that comparable behavioral trends in daily activity distribution have evolved in Drosophila melanogaster and M. domestica, yet the behaviors of these two species are orchestrated by different molecular mechanisms.
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Abascal F., Zardoya R., Posada D., 2005. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104–2105. PubMed
Bajgar A., Dolezel D., Hodkova M., 2013a Endocrine regulation of non-circadian behavior of circadian genes in insect gut. J. Insect Physiol. 59: 881–886. PubMed
Bajgar A., Jindra M., Dolezel D., 2013b Autonomous regulation of the insect gut by circadian genes acting downstream of juvenile hormone signaling. Proc. Natl. Acad. Sci. USA 110: 4416–4421. PubMed PMC
Bazalova O., Kvicalova M., Valkova T., Slaby P., Bartos P., et al. , 2016. Cryptochrome 2 mediates directional magnetoreception in cockroaches. Proc. Natl. Acad. Sci. USA. 113: 1660–1665. PubMed PMC
Beaver L. M., Rush B. L., Gvakharia B. O., Giebultowicz J. M., 2003. Noncircadian regulation and function of clock genes period and timeless in oogenesis of Drosophila melanogaster. J. Biol. Rhythms 18: 463–472. PubMed
Boothroyd C. E., Wijnen H., Naef F., Saez L., Young M. W., 2007. Integration of light and temperature in the regulation of circadian gene expression in Drosophila. PLoS Genet. 3: e54. PubMed PMC
Cao W., Edery I., 2017. Mid-day siesta in natural populations of D. melanogaster from Africa exhibits an altitudinal cline and is regulated by splicing of a thermosensitive intron in the period clock gene. BMC Evol. Biol. 17: 32. PubMed PMC
Codd V., Dolezel D., Stehlik J., Piccin A., Garner K. J., et al. , 2007. Circadian rhythm gene regulation in the housefly Musca domestica. Genetics 177: 1539–1551. PubMed PMC
Collins B. H., Rosato E., Kyriacou C. P., 2004. Seasonal behavior in Drosophila melanogaster requires the photoreceptors, the circadian clock, and phospholipase C. Proc. Natl. Acad. Sci. USA 101: 1945–1950. PubMed PMC
Cyran S. A., Buchsbaum A. M., Reddy K. L., Lin M. C., Glossop N. R. J., et al. , 2003. vrille, Pdp1, and dClock form a second feedback loop in the Drosophila circadian clock. Cell 112: 329–341. PubMed
Damulewicz M., Loboda A., Bukowska-Strakova K., Jozkowicz A., Dulak J., et al. , 2015. Clock and clock-controlled genes are differently expressed in the retina, lamina and in selected cells of the visual system of Drosophila melanogaster. Front. Cell. Neurosci. 9: 353. PubMed PMC
Dolezel D., Sauman I., Kost’al V., Hodkova M., 2007. Photoperiodic and food signals control expression pattern of the clock gene, period, in the linden bug, Pyrrhocoris apterus. J. Biol. Rhythms 22: 335–342. PubMed
Dolezel D., Zdechovanova L., Sauman I., Hodkova M., 2008. Endocrine-dependent expression of circadian clock genes in insects. Cell. Mol. Life Sci. 65: 964–969. PubMed PMC
Dolezelova E., Dolezel D., Hall J. C., 2007. Rhythm defects caused by newly engineered null mutations in Drosophila’s cryptochrome gene. Genetics 177: 329–345. PubMed PMC
Emery P., So W. V., Kaneko M., Hall J. C., Rosbash M., 1998. CRY, a Drosophila clock and light-regulated cryptochrome, is a major contributor to circadian rhythm resetting and photosensitivity. Cell 95: 669–679. PubMed
Emery P., Stanewsky R., Helfrich-Forster C., Emery-Le M., Hall J. C., et al. , 2000. Drosophila CRY is a deep brain circadian photoreceptor. Neuron 26: 493–504. PubMed
Green E. W., O’Callaghan E. K., Hansen C. N., Bastianello S., Bhutani S., et al. , 2015. Drosophila circadian rhythms in seminatural environments: summer afternoon component is not an artifact and requires TrpA1 channels. Proc. Natl. Acad. Sci. USA 112: 8702–8707. PubMed PMC
Harding H. P., Lazar M. A., 1993. The orphan receptor Rev-ErbA alpha activates transcription via a novel response element. Mol. Cell. Biol. 13: 3113–3121. PubMed PMC
Hediger M., Niessen M., Wimmer E. A., Dubendorfer A., Bopp D., 2001. Genetic transformation of the housefly Musca domestica with the lepidopteran derived transposon piggyBac. Insect Mol. Biol. 10: 113–119. PubMed
Iwai S., Fukui Y., Fujiwara Y., Takeda M., 2006. Structure and expressions of two circadian clock genes, period and timeless in the commercial silkmoth, Bombyx mori. J. Insect Physiol. 52: 625–637. PubMed
Kadener S., Menet J. S., Sugino K., Horwich M. D., Weissbein U., et al. , 2009. A role for microRNAs in the Drosophila circadian clock. Genes Dev. 23: 2179–2191. PubMed PMC
Kauranen H., Menegazzi P., Costa R., Helfrich-Forster C., Kankainen A., et al. , 2012. Flies in the north: locomotor behavior and clock neuron organization of Drosophila montana. J. Biol. Rhythms 27: 377–387. PubMed
Kelley J. L., Peyton J. T., Fiston-Lavier A. S., Teets N. M., Yee M. C., et al. , 2014. Compact genome of the Antarctic midge is likely an adaptation to an extreme environment. Nat. Commun. 5: 4611. PubMed PMC
Kidd P. B., Young M. W., Siggia E. D., 2015. Temperature compensation and temperature sensation in the circadian clock. Proc. Natl. Acad. Sci. USA 112: E6284–E6292. PubMed PMC
Kobelkova A., Bajgar A., Dolezel D., 2010. Functional molecular analysis of a circadian clock gene timeless promoter from the Drosophilid fly Chymomyza costata. J. Biol. Rhythms 25: 399–409. PubMed
Kobelkova A., Zavodska R., Sauman I., Bazalova O., Dolezel D., 2015. Expression of clock genes period and timeless in the central nervous system of the Mediterranean flour moth, Ephestia kuehniella. J. Biol. Rhythms. 30: 104–116. PubMed
Kostal V., Tollarova M., Dolezel D., 2008. Dynamism in physiology and gene transcription during reproductive diapause in a heteropteran bug, Pyrrhocoris apterus. J. Insect Physiol. 54: 77–88. PubMed
Kula-Eversole E., Nagoshi E., Shang Y. H., Rodriguez J., Allada R., et al. , 2010. Surprising gene expression patterns within and between PDF-containing circadian neurons in Drosophila. Proc. Natl. Acad. Sci. USA 107: 13497–13502. PubMed PMC
Lankinen P., 1986. Geographical variation in circadian eclosion rhythm and photoperiodic adult diapause in Drosophila-littoralis. J. Comp. Physiol. A 159: 123–142. PubMed
Low K. H., Lim C., Ko H. W., Ederyl I., 2008. Natural variation in the splice site strength of a clock gene and species-specific thermal adaptation. Neuron 60: 1054–1067. PubMed PMC
Majercak J., Sidote D., Hardin P. E., Edery I., 1999. How a circadian clock adapts to seasonal decreases in temperature and day length. Neuron 24: 219–230. PubMed
Majercak J., Chen W. F., Edery I., 2004. Splicing of the period gene 3’-terminal intron is regulated by light, circadian clock factors, and phospholipase C. Mol. Cell. Biol. 24: 3359–3372. PubMed PMC
Markert M. J., Zhang Y., Enuameh M. S., Reppert S. M., Wolfe S. A., et al. , 2016. Genomic access to monarch migration using TALEN and CRISPR/Cas9-mediated targeted mutagenesis. G3 6: 905–915. PubMed PMC
Matsushima A., Sato S., Chuman Y., Takeda Y., Yokotani S., et al. , 2004. cDNA cloning of the housefly pigment-dispersing factor (PDF) precursor protein and its peptide comparison among the insect circadian neuropeptides. J. Pept. Sci. 10: 82–91. PubMed
Meireles-Filho A. C., Bardet A. F., Yanez-Cuna J. O., Stampfel G., Stark A., 2014. cis-regulatory requirements for tissue-specific programs of the circadian clock. Curr. Biol. 24: 1–10. PubMed
Miskiewicz K., Schurmann F. W., Pyza E., 2008. Circadian release of pigment-dispersing factor in the visual system of the housefly, Musca domestica. J. Comp. Neurol. 509: 422–435. PubMed
Misof B., Liu S., Meusemann K., Peters R. S., Donath A., et al. , 2014. Phylogenomics resolves the timing and pattern of insect evolution. Science 346: 763–767. PubMed
Montelli S., Mazzotta G., Vanin S., Caccin L., Corra S., et al. , 2015. period and timeless mRNA splicing profiles under natural conditions in Drosophila melanogaster. J. Biol. Rhythms 30: 217–227. PubMed
Piccin A., Couchman M., Clayton J. D., Chalmers D., Costa R., et al. , 2000. The clock gene period of the housefly, Musca domestica, rescues behavioral rhythmicity in Drosophila melanogaster. Evidence for intermolecular coevolution? Genetics 154: 747–758. PubMed PMC
Pyza E., Meinertzhagen I. A., 1997. Neurites of period-expressing PDH cells in the fly’s optic lobe exhibit circadian oscillations in morphology. Eur. J. Neurosci. 9: 1784–1788. PubMed
Rakshit K., Krishnan N., Guzik E. M., Pyza E., Giebultowicz J. M., 2012. Effects of aging on the molecular circadian oscillations in Drosophila. Chronobiol. Int. 29: 5–14. PubMed PMC
Rosato E., Kyriacou C. P., 2006. Analysis of locomotor activity rhythms in Drosophila. Nat. Protoc. 1: 559–568. PubMed
Rubin E. B., Shemesh Y., Cohen M., Elgavish S., Robertson H. M., et al. , 2006. Molecular and phylogenetic analyses reveal mammalian-like clockwork in the honey bee (Apis mellifera) and shed new light on the molecular evolution of the circadian clock. Genome Res. 16: 1352–1365. PubMed PMC
Scott J. G., Warren W. C., Beukeboom L. W., Bopp D., Clark A. G., et al. , 2014. Genome of the house fly, Musca domestica L., a global vector of diseases with adaptations to a septic environment. Genome Biol. 15: 466. PubMed PMC
Schmid B., Helfrich-Forster C., Yoshii T., 2011. A new ImageJ plug-in “ActogramJ” for chronobiological analyses. J. Biol. Rhythms 26: 464–467. PubMed
Sharma A., Heinze S. D., Wu Y., Kohlbrenner T., Morilla I., et al. , 2017. Male sex in houseflies is determined by Mdmd, a paralog of the generic splice factor gene CWC22. Science 356: 642–645. PubMed
Stanewsky R., Kaneko M., Emery P., Beretta B., Wager-Smith K., et al. , 1998. The cry(b) mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell 95: 681–692. PubMed
Syrova Z., Dolezel D., Saumann I., Hodkova M., 2003. Photoperiodic regulation of diapause in linden bugs: are period and clock genes involved? Cell. Mol. Life Sci. 60: 2510–2515. PubMed PMC
Tomioka K., Uryu O., Kamae Y., Umezaki Y., Yoshii T., 2012. Peripheral circadian rhythms and their regulatory mechanism in insects and some other arthropods: a review. J. Comp. Physiol. B 182: 729–740. PubMed
Vanin S., Bhutani S., Montelli S., Menegazzi P., Green E. W., et al. , 2012. Unexpected features of Drosophila circadian behavioural rhythms under natural conditions. Nature 484: 371–375. PubMed
Yuan Q., Metterville D., Briscoe A. D., Reppert S. M., 2007. Insect cryptochromes: gene duplication and loss define diverse ways to construct insect circadian clocks. Mol. Biol. Evol. 24: 948–955. PubMed
Zavodska R., Fexova S., von Wowern G., Han G. B., Dolezel D., et al. , 2012. Is the sex communication of two pyralid moths, Plodia interpunctella and Ephestia kuehniella, under circadian clock regulation? J. Biol. Rhythms 27: 206–216. PubMed
Circadian rhythms and circadian clock gene homologs of complex alga Chromera velia
Evolution of casein kinase 1 and functional analysis of new doubletime mutants in Drosophila
Light and Temperature Synchronizes Locomotor Activity in the Linden Bug, Pyrrhocoris apterus