{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,17]],"date-time":"2026-10-17T15:10:07Z","timestamp":1792249807863,"version":"4.4.0"},"reference-count":77,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2021,7,2]],"date-time":"2021-07-02T00:00:00Z","timestamp":1625184000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Physiol."],"abstract":"<jats:p>Circadian clocks prepare the organism to cyclic environmental changes in light, temperature, or food availability. Here, we characterized the master clock in the brain of a strongly photoperiodic insect, the aphid <jats:italic>Acyrthosiphon pisum<\/jats:italic>, immunohistochemically with antibodies against <jats:italic>A. pisum<\/jats:italic> Period (PER), <jats:italic>Drosophila melanogaster<\/jats:italic> Cryptochrome (CRY1), and crab Pigment-Dispersing Hormone (PDH). The latter antibody detects all so far known PDHs and PDFs (Pigment-Dispersing Factors), which play a dominant role in the circadian system of many arthropods. We found that, under long days, PER and CRY are expressed in a rhythmic manner in three regions of the brain: the dorsal and lateral protocerebrum and the lamina. No staining was detected with anti-PDH, suggesting that aphids lack PDF. All the CRY1-positive cells co-expressed PER and showed daily PER\/CRY1 oscillations of high amplitude, while the PER oscillations of the CRY1-negative PER neurons were of considerable lower amplitude. The CRY1 oscillations were highly synchronous in all neurons, suggesting that aphid CRY1, similarly to Drosophila CRY1, is light sensitive and its oscillations are synchronized by light-dark cycles. Nevertheless, in contrast to <jats:italic>Drosophila<\/jats:italic> CRY1, aphid CRY1 was not degraded by light, but steadily increased during the day and decreased during the night. PER was always located in the nuclei of the clock neurons, while CRY was predominantly cytoplasmic and revealed the projections of the PER\/CRY1-positive neurons. We traced the PER\/CRY1-positive neurons through the aphid protocerebrum discovering striking similarities with the circadian clock of <jats:italic>D. melanogaster<\/jats:italic>: The CRY1 fibers innervate the dorsal and lateral protocerebrum and putatively connect the different PER-positive neurons with each other. They also run toward the pars intercerebralis, which controls hormone release <jats:italic>via<\/jats:italic> the neurohemal organ, the corpora cardiaca. In contrast to <jats:italic>Drosophila<\/jats:italic>, the CRY1-positive fibers additionally travel directly toward the corpora cardiaca and the close-by endocrine gland, corpora allata. This suggests a direct link between the circadian clock and the photoperiodic control of hormone release that can be studied in the future.<\/jats:p>","DOI":"10.3389\/fphys.2021.705048","type":"journal-article","created":{"date-parts":[[2021,7,2]],"date-time":"2021-07-02T07:05:43Z","timestamp":1625209543000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":25,"title":["Antibodies Against the Clock Proteins Period and Cryptochrome Reveal the Neuronal Organization of the Circadian Clock in the Pea Aphid"],"prefix":"10.3389","volume":"12","author":[{"given":"Francesca Sara","family":"Colizzi","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katharina","family":"Beer","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paolo","family":"Cuti","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter","family":"Deppisch","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David","family":"Mart\u00ednez Torres","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Taishi","family":"Yoshii","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Charlotte","family":"Helfrich-F\u00f6rster","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2021,7,2]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"103185","DOI":"10.1016\/j.ibmb.2019.103185","article-title":"Insulin-like peptides involved in photoperiodism in the aphid Acyrthosiphon pisum","volume":"112","author":"Barber\u00e0","year":"2019","journal-title":"Insect Biochem. Mol. Biol."},{"key":"ref2","doi-asserted-by":"publisher","first-page":"54","DOI":"10.1016\/j.ibmb.2017.02.006","article-title":"Characterisation, analysis of expression and localisation of circadian clock genes from the perspective of photoperiodism in the aphid Acyrthosiphon pisum","volume":"83","author":"Barber\u00e0","year":"2017","journal-title":"Insect Biochem. Mol. Biol."},{"key":"ref3","doi-asserted-by":"publisher","first-page":"601676","DOI":"10.3389\/fnbeh.2020.601676","article-title":"Model and non-model insects in chronobiology","volume":"14","author":"Beer","year":"2020","journal-title":"Front. Behav. Neurosci."},{"key":"ref4","doi-asserted-by":"publisher","first-page":"170224","DOI":"10.1098\/rsob.170224","article-title":"Pigment-dispersing factor-expressing neurons convey circadian information in the honey bee brain","volume":"8","author":"Beer","year":"2018","journal-title":"Open Biol."},{"key":"ref5","first-page":"39","article-title":"Natural variation and genetics of photoperiodism in Wyeomyia smithii","volume-title":"Advances in Genetics.","author":"Bradshaw","year":"2017"},{"key":"ref6","doi-asserted-by":"publisher","first-page":"590","DOI":"10.1111\/j.1438-8677.1937.tb01941.x","article-title":"Die endogene tagesrhythmik als grundlage der photoperiodischen reaktion","volume":"54","author":"B\u00fcnning","year":"1936","journal-title":"Der Dtsch. Bot. Ges."},{"key":"ref7","doi-asserted-by":"publisher","first-page":"123","DOI":"10.1111\/j.1365-2583.2009.00931.x","article-title":"Identification and characterization of circadian clock genes in the pea aphid Acyrthosiphon pisum: aphid clock genes","volume":"19","author":"Cort\u00e9s","year":"2010","journal-title":"Insect Mol. Biol."},{"key":"ref9","doi-asserted-by":"publisher","first-page":"99","DOI":"10.3389\/fphys.2020.00099","article-title":"One actor, multiple roles: the performances of cryptochrome in Drosophila","volume":"11","author":"Damulewicz","year":"2020","journal-title":"Front. Physiol."},{"key":"ref10","doi-asserted-by":"publisher","first-page":"377","DOI":"10.1007\/BF00219082","article-title":"The ultrastructure of nerve endings containing pigment-dispersing hormone (PDH) in crustacean sinus glands: identification by an antiserum against a synthetic PDH","volume":"250","author":"Dircksen","year":"1987","journal-title":"Cell Tissue Res."},{"key":"ref11","doi-asserted-by":"publisher","first-page":"493","DOI":"10.1016\/S0896-6273(00)81181-2","article-title":"Drosophila CRY is a deep brain circadian photoreceptor","volume":"26","author":"Emery","year":"2000","journal-title":"Neuron"},{"key":"ref12","doi-asserted-by":"publisher","first-page":"401","DOI":"10.1002\/cne.1148","article-title":"Candidates for extraocular photoreceptors in the cockroach suggest homology to the lamina and lobula organs in beetles","volume":"433","author":"Fleissner","year":"2001","journal-title":"J. Comp. Neurol."},{"key":"ref13","doi-asserted-by":"publisher","first-page":"411","DOI":"10.1007\/s004410050711","article-title":"Staining in the brain of Pachymorpha sexguttata mediated by an antibody against a Drosophila clock-gene product: labeling of cells with possible importance for the beetle\u2019s circadian rhythms","volume":"286","author":"Frisch","year":"1996","journal-title":"Cell Tissue Res."},{"key":"ref14","doi-asserted-by":"publisher","first-page":"170047","DOI":"10.1098\/rsob.170047","article-title":"Neuronal circadian clock protein oscillations are similar in behaviourally rhythmic forager honeybees and in arrhythmic nurses","volume":"7","author":"Fuchikawa","year":"2017","journal-title":"Open Biol."},{"key":"ref15","doi-asserted-by":"publisher","first-page":"1067","DOI":"10.1111\/ejn.13863","article-title":"GABA- and serotonin-expressing neurons take part in inhibitory as well as excitatory input pathways to the circadian clock of the madeira cockroach Rhyparobia maderae","volume":"47","author":"Giese","year":"2018","journal-title":"Eur. J. Neurosci."},{"key":"ref16","doi-asserted-by":"publisher","first-page":"390","DOI":"10.1002\/cne.20712","article-title":"Synaptic connections between pigment-dispersing factor-immunoreactive neurons and neurons in the pars lateralis of the blow fly Protophormia terraenovae","volume":"491","author":"Hamanaka","year":"2005","journal-title":"J. Comp. Neurol."},{"key":"ref17","doi-asserted-by":"publisher","first-page":"821","DOI":"10.1016\/S0022-1910(01)00055-5","article-title":"Aphid photoperiodic clocks","volume":"47","author":"Hardie","year":"2001","journal-title":"J. Insect Physiol."},{"key":"ref18","doi-asserted-by":"publisher","first-page":"612","DOI":"10.1073\/pnas.92.2.612","article-title":"The period clock gene is expressed in central nervous system neurons which also produce a neuropeptide that reveals the projections of circadian pacemaker cells within the brain of Drosophila melanogaster","volume":"92","author":"Helfrich-F\u00f6rster","year":"1995","journal-title":"Proc. Natl. Acad. Sci."},{"key":"ref19","doi-asserted-by":"publisher","first-page":"957","DOI":"10.1042\/BST0330957","article-title":"Organization of endogenous clocks in insects","volume":"33","author":"Helfrich-F\u00f6rster","year":"2005","journal-title":"Biochem. Soc. Trans."},{"key":"ref20","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1007\/978-81-322-3688-7_6","article-title":"The drosophila clock system","volume-title":"Biological Timekeeping: Clocks, Rhythms and Behaviour.","author":"Helfrich-F\u00f6rster","year":"2017"},{"key":"ref21","doi-asserted-by":"publisher","first-page":"259","DOI":"10.1007\/s00359-019-01379-5","article-title":"Light input pathways to the circadian clock of insects with an emphasis on the fruit fly Drosophila melanogaster","volume":"206","author":"Helfrich-F\u00f6rster","year":"2020","journal-title":"J. Comp. Physiol. A"},{"key":"ref22","doi-asserted-by":"publisher","first-page":"567","DOI":"10.3109\/07420529808993195","article-title":"Organization of the circadian system in insects","volume":"15","author":"Helfrich-F\u00f6rster","year":"1998","journal-title":"Chronobiol. Int."},{"key":"ref23","doi-asserted-by":"publisher","first-page":"343","DOI":"10.1007\/BF00318190","article-title":"Comparative anatomy of pigment-dispersing hormone-immunoreactive neurons in the brain of orthopteroid insects","volume":"266","author":"Homberg","year":"1991","journal-title":"Cell Tissue Res."},{"key":"ref24","doi-asserted-by":"publisher","first-page":"372","DOI":"10.1177\/0748730410379711","article-title":"JTK_CYCLE: an efficient non-parametric algorithm for detecting rhythmic components in genome-scale datasets","volume":"25","author":"Hughes","year":"2010","journal-title":"J. Biol. Rhythm."},{"key":"ref25","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1111\/j.1365-2583.2009.00951.x","article-title":"Neuropeptide and neurohormone precursors in the pea aphid, Acyrthosiphon pisum","volume":"19","author":"Huybrechts","year":"2010","journal-title":"Insect Mol. Biol."},{"key":"ref26","doi-asserted-by":"publisher","first-page":"453","DOI":"10.1242\/jeb.091801","article-title":"Involvement of the brain region containing pigment-dispersing factor-immunoreactive neurons in the photoperiodic response of the bean bug, Riptortus pedestris","volume":"217","author":"Ikeno","year":"2014","journal-title":"J. Exp. Biol."},{"key":"ref27","doi-asserted-by":"publisher","first-page":"255","DOI":"10.1177\/0748730418764738","article-title":"The circadian clock of the ant Camponotus floridanus is localized in dorsal and lateral neurons of the brain","volume":"33","author":"Kay","year":"2018","journal-title":"J. Biol. Rhythm."},{"key":"ref28","doi-asserted-by":"publisher","first-page":"268","DOI":"10.1111\/ejn.14092","article-title":"Molecular and circuit mechanisms mediating circadian clock output in the Drosophila brain","volume":"51","author":"King","year":"2020","journal-title":"Eur. J. Neurosci."},{"key":"ref29","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1186\/s40851-015-0011-6","article-title":"Green-sensitive opsin is the photoreceptor for photic entrainment of an insect circadian clock","volume":"1","author":"Komada","year":"2015","journal-title":"Zool. Lett."},{"key":"ref30","doi-asserted-by":"publisher","first-page":"26","DOI":"10.1186\/s40851-018-0109-8","article-title":"A novel photic entrainment mechanism for the circadian clock in an insect: involvement of c-fos and cryptochromes","volume":"4","author":"Kutaragi","year":"2018","journal-title":"Zool. Lett."},{"key":"ref31","doi-asserted-by":"publisher","first-page":"92","DOI":"10.1016\/0022-1910(59)90024-1","article-title":"The role of photoperiod and temperature in the determination of parthenogenetic and sexual forms in the aphid Megoura viciae buckton\u2014I: the influence of these factors on apterous virginoparae and their progeny","volume":"3","author":"Lees","year":"1959","journal-title":"J. Insect Physiol."},{"key":"ref32","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.gene.2013.01.061","article-title":"Comparative genomic analysis and evolution of family-B G protein-coupled receptors from six model insect species","volume":"519","author":"Li","year":"2013","journal-title":"Gene"},{"key":"ref33","doi-asserted-by":"publisher","first-page":"640","DOI":"10.3389\/fendo.2020.00640","article-title":"Identification and characterization of neuropeptides and their G protein-coupled receptors (GPCRs) in the cowpea aphid Aphis craccivora","volume":"11","author":"Li","year":"2020","journal-title":"Front. Endocrinol."},{"key":"ref34","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1101\/gr.6714008","article-title":"Genomics, transcriptomics, and peptidomics of neuropeptides and protein hormones in the red flour beetle Tribolium castaneum","volume":"18","author":"Li","year":"2008","journal-title":"Genome Res."},{"key":"ref35","doi-asserted-by":"publisher","first-page":"159","DOI":"10.3389\/fneur.2016.00159","article-title":"Phosphorylation regulating the ratio of intracellular CRY1 protein determines the circadian period","volume":"7","author":"Liu","year":"2016","journal-title":"Front. Neurol."},{"key":"ref36","first-page":"513","article-title":"The migration of the Aphididae and the appearance of the sexual forms as affected by the relative length of daily light exposure","volume":"27","author":"Marcovitch","year":"1924","journal-title":"J. Agric. Res."},{"key":"ref37","doi-asserted-by":"publisher","first-page":"1865","DOI":"10.1002\/cne.23767","article-title":"Evolution of pigment-dispersing factor neuropeptides in panarthropoda: insights from onychophora (velvet worms) and tardigrada (water bears)","volume":"523","author":"Mayer","year":"2015","journal-title":"J. Comp. Neurol."},{"key":"ref38","doi-asserted-by":"publisher","first-page":"229","DOI":"10.3389\/fphys.2020.00229","article-title":"A functional clock within the main morning and evening neurons of D. melanogaster is not sufficient for wild-type locomotor activity under changing day length","volume":"11","author":"Menegazzi","year":"2020","journal-title":"Front. Physiol."},{"key":"ref39","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1177\/0748730412471303","article-title":"Drosophila clock neurons under natural conditions","volume":"28","author":"Menegazzi","year":"2013","journal-title":"J. Biol. Rhythm."},{"key":"ref40","doi-asserted-by":"publisher","first-page":"271","DOI":"10.1007\/s00018-015-2063-3","article-title":"Insulin\/IGF signaling in drosophila and other insects: factors that regulate production, release and post-release action of the insulin-like peptides","volume":"73","author":"N\u00e4ssel","year":"2016","journal-title":"Cell. Mol. Life Sci."},{"key":"ref41","doi-asserted-by":"publisher","first-page":"10","DOI":"10.1186\/s40851-014-0003-y","article-title":"Common features in diverse insect clocks","volume":"1","author":"Numata","year":"2015","journal-title":"Zool. Lett."},{"key":"ref42","doi-asserted-by":"publisher","first-page":"241","DOI":"10.1016\/j.cub.2008.12.042","article-title":"Light-dependent interactions between the drosophila circadian clock factors cryptochrome, jetlag, and timeless","volume":"19","author":"Peschel","year":"2009","journal-title":"Curr. Biol."},{"key":"ref43","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1007\/BF00319128","article-title":"Immunocytochemical characterization of the accessory medulla in the cockroach Leucophaea maderae","volume":"282","author":"Petri","year":"1995","journal-title":"Cell Tissue Res."},{"key":"ref44","doi-asserted-by":"publisher","first-page":"227","DOI":"10.1007\/s00424-017-2103-y","article-title":"The role of the circadian clock system in physiology","volume":"470","author":"Pilorz","year":"2018","journal-title":"Pfl\u00fcgers Archiv. Eur. J. Physiol."},{"key":"ref45","doi-asserted-by":"publisher","first-page":"1877","DOI":"10.1242\/jeb.00373","article-title":"Ectopic transplantation of the accessory medulla restores circadian locomotor rhythms in arrhythmic cockroaches (Leucophaea maderae)","volume":"206","author":"Reischig","year":"2003","journal-title":"J. Exp. Biol."},{"key":"ref46","doi-asserted-by":"publisher","first-page":"233","DOI":"10.1016\/j.cell.2006.01.009","article-title":"A colorful model of the circadian clock","volume":"124","author":"Reppert","year":"2006","journal-title":"Cell"},{"key":"ref47","doi-asserted-by":"publisher","first-page":"1352","DOI":"10.1101\/gr.5094806","article-title":"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","volume":"16","author":"Rubin","year":"2006","journal-title":"Genome Res."},{"key":"ref48","doi-asserted-by":"publisher","first-page":"821","DOI":"10.2108\/zsj.19.821","article-title":"A circadian neuropeptide, pigment-dispersing factor\u2013pdf, in the last-summer cicada Meimuna opalifera: DNA cloning and immunocytochemistry","volume":"19","author":"Sato","year":"2002","journal-title":"Zool. Sci."},{"key":"ref49","doi-asserted-by":"publisher","first-page":"457","DOI":"10.1016\/j.neuron.2005.03.014","article-title":"Connecting the navigational clock to sun compass input in monarch butterfly brain","volume":"46","author":"Sauman","year":"2005","journal-title":"Neuron"},{"key":"ref50","doi-asserted-by":"publisher","first-page":"418","DOI":"10.1006\/dbio.1996.0228","article-title":"Molecular characterization of prothoracicotropic hormone (PTTH) from the giant silkmoth Antheraea pernyi: developmental appearance of PTTH-expressing cells and relationship to circadian clock cells in central brain","volume":"178","author":"Sauman","year":"","journal-title":"Dev. Biol."},{"key":"ref51","doi-asserted-by":"publisher","first-page":"889","DOI":"10.1016\/S0896-6273(00)80220-2","article-title":"Circadian clock neurons in the silkmoth antheraea pernyi: novel mechanisms of period protein regulation","volume":"17","author":"Sauman","year":"","journal-title":"Neuron"},{"key":"ref52","doi-asserted-by":"publisher","first-page":"1","DOI":"10.14411\/eje.2021.001","article-title":"Insect photoperiodism: b\u00fcnning\u2019s hypothesis, the history and development of an idea","volume":"118","author":"Saunders","year":"2021","journal-title":"Eur. J. Entomol."},{"key":"ref53","doi-asserted-by":"publisher","first-page":"676","DOI":"10.1038\/nmeth.2019","article-title":"Fiji: an open-source platform for biological-image analysis","volume":"9","author":"Schindelin","year":"2012","journal-title":"Nat. Methods"},{"key":"ref54","doi-asserted-by":"publisher","first-page":"1209","DOI":"10.1002\/cne.24406","article-title":"Neuroanatomical details of the lateral neurons of Drosophila melanogaster support their functional role in the circadian system","volume":"526","author":"Schubert","year":"2018","journal-title":"J. Comp. Neurol."},{"key":"ref55","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1007\/s00441-003-0705-5","article-title":"Immunocytochemical distribution of pigment-dispersing hormone in the cephalic ganglia of polyneopteran insects","volume":"312","author":"Sehadov\u00e1","year":"2003","journal-title":"Cell Tissue Res."},{"key":"ref56","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1016\/j.cois.2014.05.002","article-title":"Pigment-dispersing factor signaling and circadian rhythms in insect locomotor activity","volume":"1","author":"Shafer","year":"2014","journal-title":"Curr. Opn. Ins. Sci."},{"key":"ref57","doi-asserted-by":"publisher","first-page":"867","DOI":"10.1242\/jeb.027003","article-title":"Roles of PER immunoreactive neurons in circadian rhythms and photoperiodism in the blow fly, Protophormia terraenovae","volume":"212","author":"Shiga","year":"2009","journal-title":"J. Exp. Biol."},{"key":"ref58","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1104\/pp.16.01327","article-title":"Circadian clock and photoperiodic flowering in arabidopsis: constans is a hub for signal integration","volume":"173","author":"Shim","year":"2017","journal-title":"Plant Physiol."},{"key":"ref59","doi-asserted-by":"publisher","first-page":"1880","DOI":"10.1016\/j.cub.2016.05.018","article-title":"Visualizing and quantifying intracellular behavior and abundance of the core circadian clock protein PERIOD2","volume":"26","author":"Smyllie","year":"2016","journal-title":"Curr. Biol."},{"key":"ref60","doi-asserted-by":"publisher","first-page":"307","DOI":"10.1016\/0016-6480(77)90095-8","article-title":"The neurosecretory system in the aphid Megoura viciae, with reference to unusual features associated with long distance transport of neurosecretion","volume":"31","author":"Steel","year":"1977","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref61","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1242\/jeb.67.1.117","article-title":"The role of neurosecretion in the photoperiodic control of polymorphism in the aphid Megoura viciae","volume":"67","author":"Steel","year":"1977","journal-title":"J. Exp. Biol."},{"key":"ref62","doi-asserted-by":"publisher","first-page":"44","DOI":"10.1016\/j.conb.2016.07.010","article-title":"Peptidergic circadian clock circuits in the Madeira cockroach","volume":"41","author":"Stengl","year":"2016","journal-title":"Curr. Opin. Neurobiol."},{"key":"ref63","doi-asserted-by":"publisher","first-page":"203","DOI":"10.1007\/BF00215116","article-title":"Pigment-dispersing hormone-immunoreactive neurons in the cockroach Leucophaea maderae share properties with circadian pacemaker neurons","volume":"175","author":"Stengl","year":"1994","journal-title":"J. Comp. Physiol. A"},{"key":"ref64","doi-asserted-by":"publisher","first-page":"398","DOI":"10.2108\/zs170069","article-title":"Identification and characterization of novel genes expressed preferentially in the corpora allata or corpora cardiaca during the juvenile hormone synthetic period in the silkworm, Bombyx mori","volume":"34","author":"Taguchi","year":"2017","journal-title":"Zool. Sci."},{"key":"ref65","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1186\/s40851-017-0066-7","article-title":"Cryptochrome genes form an oscillatory loop independent of the per\/tim loop in the circadian clockwork of the cricket Gryllus bimaculatus","volume":"3","author":"Tokuoka","year":"2017","journal-title":"Zool. Lett."},{"key":"ref66","doi-asserted-by":"publisher","first-page":"624","DOI":"10.2108\/zs140024","article-title":"Chronobiology of crickets: a review","volume":"31","author":"Tomioka","year":"2014","journal-title":"Zool. Sci."},{"key":"ref67","doi-asserted-by":"publisher","first-page":"747","DOI":"10.1016\/0022-1910(86)90077-6","article-title":"Circadian rhythm in the neurally isolated lamina-medulla-complex of the cricket, Gryllus bimaculatus","volume":"32","author":"Tomioka","year":"1986","journal-title":"J. Insect Physiol."},{"key":"ref68","doi-asserted-by":"publisher","first-page":"285","DOI":"10.1111\/phen.12258","article-title":"Cryptochrome genes mediate photoperiodic responses in the cricket Modicogryllus siamensis","volume":"43","author":"Ueda","year":"2018","journal-title":"Physiol. Entomol."},{"key":"ref69","doi-asserted-by":"publisher","first-page":"277","DOI":"10.1016\/j.ygcen.2012.08.018","article-title":"Insulin-like and testis ecdysiotropin neuropeptides are regulated by the circadian timing system in the brain during larval\u2013adult development in the insect Rhodnius prolixus (Hemiptera)","volume":"179","author":"Vafopoulou","year":"2012","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref70","doi-asserted-by":"publisher","first-page":"e7144","DOI":"10.7717\/peerj.7144","article-title":"Coleoptera genome and transcriptome sequences reveal numerous differences in neuropeptide signaling between species","volume":"7","author":"Veenstra","year":"2019","journal-title":"Peer J."},{"key":"ref71","doi-asserted-by":"publisher","first-page":"215","DOI":"10.1002\/arch.20236","article-title":"Mapping the cellular network of the circadian clock in two cockroach species","volume":"68","author":"Wen","year":"2008","journal-title":"Arch. Ins. Biochem. Physiol."},{"key":"ref72","doi-asserted-by":"publisher","first-page":"366","DOI":"10.1002\/cne.10242","article-title":"Neuroanatomical studies of period gene expression in the hawkmoth, Manduca sexta","volume":"447","author":"Wise","year":"2002","journal-title":"J. Comp. Neurol."},{"key":"ref73","doi-asserted-by":"publisher","first-page":"4291","DOI":"10.1038\/s41467-020-18061-z","article-title":"Circadian clock mechanism driving mammalian photoperiodism","volume":"11","author":"Wood","year":"2020","journal-title":"Nat. Commun."},{"key":"ref74","doi-asserted-by":"publisher","first-page":"33","DOI":"10.1007\/s00441-015-2192-x","article-title":"Neuroanatomy of pars intercerebralis neurons with special reference to their connections with neurons immunoreactive for pigment-dispersing factor in the blow fly Protophormia terraenovae","volume":"362","author":"Yasuyama","year":"2015","journal-title":"Cell Tissue Res."},{"key":"ref75","doi-asserted-by":"publisher","first-page":"952","DOI":"10.1002\/cne.21702","article-title":"Cryptochrome is present in the compound eyes and a subset of Drosophila\u2019s clock neurons","volume":"508","author":"Yoshii","year":"2008","journal-title":"J. Comp. Neurol."},{"key":"ref76","doi-asserted-by":"publisher","first-page":"948","DOI":"10.1093\/molbev\/msm011","article-title":"Insect cryptochromes: gene duplication and loss define diverse ways to construct insect circadian clocks","volume":"24","author":"Yuan","year":"2007","journal-title":"Mol. Biol. Evol."},{"key":"ref77","doi-asserted-by":"publisher","first-page":"106","DOI":"10.1177\/0748730403251711","article-title":"Distribution of per protein, pigment-dispersing hormone, prothoracicotropic hormone, and eclosion hormone in the cephalic nervous system of insects","volume":"18","author":"Z\u00e1vodsk\u00e1","year":"2003","journal-title":"J. Biol. Rhythm."},{"key":"ref78","doi-asserted-by":"publisher","first-page":"R953","DOI":"10.1016\/j.cub.2005.11.030","article-title":"The two CRYs of the butterfly","volume":"15","author":"Zhu","year":"2005","journal-title":"Curr. Biol."}],"container-title":["Frontiers in Physiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fphys.2021.705048\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,7,21]],"date-time":"2021-07-21T17:16:28Z","timestamp":1626887788000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fphys.2021.705048\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,7,2]]},"references-count":77,"alternative-id":["10.3389\/fphys.2021.705048"],"URL":"https:\/\/doi.org\/10.3389\/fphys.2021.705048","relation":{},"ISSN":["1664-042X"],"issn-type":[{"value":"1664-042X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,7,2]]},"article-number":"705048"}}