Abstract
This chapter closely focuses on the molecular elements involved in each physiological module in photoperiodism, i.e., photoreceptors, a photoperiodic time measurement system, circadian clocks, and a counter. Multiple opsins are the photopigments in photoperiodism. Drosophila-type cryptochrome also acts as a photopigment, but further experiments are necessary. These photopigments may play distinct roles. A circadian clock consisting of circadian clock genes, such as period, timeless, cycle, Clock, and mammalian-type cryptochrome, controls the photoperiodic time measurement system. However, circadian clocks or each circadian clock gene itself also plays a critical role in other photoperiodic processes, which reside downstream of photoperiodic time measurement, and therefore careful interpretation is necessary. Possible neuropeptides and neurotransmitters are proposed as circadian output molecules. Pigment-dispersing factor (PDF), short neuropeptide F (sNPF), and glutamate are promising candidates. In contrast to recent advances in our understanding of the circadian clock, the molecular mechanisms of photoperiodic time measurement are still largely unknown. The counter system may be operated by biogenic amines, but this has been investigated in only a few species. Further extensive studies are awaited.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abrieux A, Xue Y, Cai Y, Lewald KM, Nguyen HN, Zhang Y et al (2020) EYES ABSENT and TIMELESS integrate photoperiodic and temperature cues to regulate seasonal physiology in Drosophila. Proc Natl Acad Sci USA 117:15293–15304. https://doi.org/10.1073/pnas.2004262117
Anduaga AM, Nagy D, Costa R, Kyriacou CP (2018) Diapause in Drosophila melanogaster—photoperiodicity, cold tolerance and metabolites. J Insect Physiol 105:46–53. https://doi.org/10.1016/j.jinsphys.2018.01.003
Bajgar A, Jindra M, Dolezel D (2013) Autonomous regulation of the insect gut by circadian genes acting downstream of juvenile hormone signaling. Proc Natl Acad Sci USA 110:4416–4421. https://doi.org/10.1073/pnas.1217060110
Barberà M, Escrivá L, Collantes-Alegre JM, Meca G, Rosato E, Martínez-Torres D (2020) Melatonin in the seasonal response of the aphid Acyrthosiphon pisum. Insect Sci 27:224–238. https://doi.org/10.1111/1744-7917.12652
Berndt A, Kottke T, Breitkreuz H, Dvorsky R, Hennig S, Alexander M et al (2007) A novel photoreaction mechanism for the circadian blue light photoreceptor Drosophila cryptochrome. J Biol Chem 282:13011–13021. https://doi.org/10.1074/jbc.M608872200
Bosse TC, Veerman A (1996) Involvement of vitamin A in the photoperiodic induction of diapause in the spider mite Tetranychus urticae is demonstrated by rearing an albino mutant on a semi-synthetic diet with and without β-carotene or vitamin A. Physiol Entomol 21:188–192. https://doi.org/10.1111/j.1365-3032.1996.tb00854.x
Bryon A, Kurlovs AH, Dermauw W, Greenhalgh R, Riga M, Grbic M et al (2017) Disruption of a horizontally transferred phytoene desaturase abolishes carotenoid accumulation and diapause in Tetranychus urticae. Proc Natl Acad Sci USA 114:E5871–E5880. https://doi.org/10.1073/pnas.1706865114
Bünning E (1936) Die endonome Tagesrhythmik als Grundlage der photoperiodischen Reaktion. Ber Dtsch Bot Ges 54:590–607
Chang V, Meuti ME (2020) Circadian transcription factors differentially regulate features of the adult overwintering diapause in the Northern house mosquito, Culex pipiens. Insect Biochem Mol Biol 121:103365. https://doi.org/10.1016/j.ibmb.2020.103365
Cui W-Z, Qiu J-F, Dai T-M, Chen Z, Li J-L, Liu K et al (2021) Circadian clock gene period contributes to diapause via GABAeric-diapause hormone pathway in Bombyx mori. Biology (Basel) 10:842. https://doi.org/10.3390/biology10090842
Dalla Benetta E, Beukeboom LW, Van De Zande L (2019) Adaptive differences in circadian clock gene expression patterns and photoperiodic diapause induction in Nasonia vitripennis. Am Nat 193:881–896. https://doi.org/10.1086/703159
Denlinger DL (2022) Insect diapause. Cambridge University Press, Cambridge
Des Marteaux L, Xi J, Mano G, Goto SG (2022) Circadian clock outputs regulating insect photoperiodism: a potential role for glutamate transporter. Biochem Biophys Res Commun 589:100–106. https://doi.org/10.1016/j.bbrc.2021.12.014
Dong L, Udaka H, Numata H, Ito C (2021) Regulation of Krüppel homolog 1 expression by photoperiod in the bean bug, Riptortus pedestris. Physiol Entomol 46:82–93. https://doi.org/10.1111/phen.12347sp
Emerson KJ, Uyemura AM, McDaniel KL, Schmidt PS, Bradshaw WE, Holzapfel CM (2009) Environmental control of ovarian dormancy in natural populations of Drosophila melanogaster. J Comp Physiol A 195:825–829. https://doi.org/10.1007/s00359-009-0460-5
Emery P, So WV, Kaneko M, Hall JC, 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. https://doi.org/10.1016/S0092-8674(00)81637-2
Emery P, Stanewsky R, Helfrich-Förster C, Emery-Le M, Hall JC, Rosbash M (2000) Drosophila CRY is a deep brain circadian photoreceptor. Neuron 26:493–504. https://doi.org/10.1016/S0896-6273(00)81181-2
Erickson PA, Weller CA, Song DY, Bangerter AS, Schmidt P, Bergland AO (2020) Unique genetic signatures of local adaptation over space and time for diapause, an ecologically relevant complex trait, in Drosophila melanogaster. PLoS Genet 16:e1009110. https://doi.org/10.1371/JOURNAL.PGEN.1009110
Fujiwara Y, Hermann-Luibl C, Katsura M, Sekiguchi M, Ida T, Helfrich-Förster C et al (2018) The CCHamide1 neuropeptide expressed in the anterior dorsal neuron 1 conveys a circadian signal to the ventral lateral neurons in Drosophila melanogaster. Front Physiol 9:1276. https://doi.org/10.3389/FPHYS.2018.01276/BIBTEX
Gibbs D (1975) Reversal of pupal diapause in Sarcophaga argyrostoma by temperature shifts after puparium formation. J Insect Physiol 21:1179–1186. https://doi.org/10.1016/0022-1910(75)90085-2
Goto SG (2022) Photoperiodic time measurement, photoreception, and circadian clocks in insect photoperiodism. Appl Entomol Zool 57:193–212. https://doi.org/10.1007/s13355-022-00785-7
Goto SG, Nagata M (2022) The circadian clock gene (Clock) regulates photoperiodic time measurement and its downstream process in maternal induction of embryonic diapause in a cricket. Eur J Entomol 119:12–22. https://doi.org/10.14411/eje.2022.002
Goto SG, Doi K, Nakayama S, Numata H (2008) Maternal control of cold and desiccation tolerance in eggs of the band-legged ground cricket Dianemobius nigrofasciatus in relation to embryonic diapause. Entomol Res 38:17–23. https://doi.org/10.1111/j.1748-5967.2008.00140.x
Goto SG, Shiga S, Numata H (2010) Photoperiodism in insects: perception of light and the role of clock genes. In: Nelson RJ, Denlinger DL, Somers DE (eds) Photoperiodism: the biological calendar. Oxford University Press, Oxford, pp 258–286
Hase H, Koukai M, Hamanaka Y, Goto SG, Tachibana S-I, Shiga S (2017) Transcriptome analysis of the brain under diapause and nondiapause conditions in the blowfly Protophormia terraenovae. Physiol Entomol 42:282–289. https://doi.org/10.1111/phen.12205
Hasebe M, Shiga S (2021) Oviposition-promoting pars intercerebralis neurons show period-dependent photoperiodic changes in their firing activity in the bean bug. Proc Natl Acad Sci USA 118:e2018823118. https://doi.org/10.1073/pnas.2018823118
Hasebe M, Shiga S (2022) Clock gene-dependent glutamate dynamics in the bean bug brain regulate photoperiodic reproduction. PLoS Biol 20:e3001734. https://doi.org/10.1371/journal.pbio.3001734
Hasebe M, Kotaki T, Shiga S (2022) Pigment-dispersing factor is involved in photoperiodic control of reproduction in the brown-winged green bug, Plautia stali. J Insect Physiol 137:104359. https://doi.org/10.1016/j.jinsphys.2022.104359
Hejnikova M, Paroulek M, Hodkova M (2016) Decrease in Methoprene tolerant and Taiman expression reduces juvenile hormone effects and enhances the levels of juvenile hormone circulating in males of the linden bug Pyrrhocoris apterus. J Insect Physiol 93–94:72–80. https://doi.org/10.1016/j.jinsphys.2016.08.009
Hejníková M, Nouzova M, Ramirez CE, Fernandez-Lima F, Noriega FG, Doležel D (2022) Sexual dimorphism of diapause regulation in the hemipteran bug Pyrrhocoris apterus. Insect Biochem Mol Biol 142:103721. https://doi.org/10.1016/j.ibmb.2022.103721
Herman WS (1981) Studies on the adult reproductive diapause of the monarch butterfly, Danaus plexippus. Biol Bull 160:89–106. https://doi.org/10.2307/1540903
Hermann C, Yoshii T, Dusik V, Helfrich-Förster C (2012) Neuropeptide F immunoreactive clock neurons modify evening locomotor activity and free-running period in Drosophila melanogaster. J Comp Neurol 520:970–987. https://doi.org/10.1002/cne.22742
Hermann-Luibl C, Yoshii T, Senthilan PR, Dircksen H, Helfrich-Förster C (2014) The ion transport peptide is a new functional clock neuropeptide in the fruit fly Drosophila melanogaster. J Neurosci 34:9522–9536. https://doi.org/10.1523/JNEUROSCI.0111-14.2014
Hirai M, Yuda M, Shinoda T, Chinzei Y (1998) Identification and cDNA cloning of novel juvenile hormone responsive genes from fat body of the bean bug, Riptortus clavatus by mRNA differential display. Insect Biochem Mol Biol 28:181–189. https://doi.org/10.1016/S0965-1748(97)00116-1
Iiams SE, Lugena AB, Zhang Y, Hayden AN, Merlin C (2019) Photoperiodic and clock regulation of the vitamin A pathway in the brain mediates seasonal responsiveness in the monarch butterfly. Proc Natl Acad Sci USA 116:25214–25221. https://doi.org/10.1073/pnas.1913915116
Ikeda K, Daimon T, Shiomi K, Udaka H, Numata H (2021) Involvement of the clock gene period in the photoperiodism of the silkmoth Bombyx mori. Zool Sci 38:523–530. https://doi.org/10.2108/zs210081
Ikeno T, Tanaka SI, Numata H, Goto SG (2010) Photoperiodic diapause under the control of circadian clock genes in an insect. BMC Biol 8:116. https://doi.org/10.1186/1741-7007-8-116
Ikeno T, Numata H, Goto SG (2011a) Photoperiodic response requires mammalian-type cryptochrome in the bean bug Riptortus pedestris. Biochem Biophys Res Commun 410:394–397. https://doi.org/10.1016/j.bbrc.2011.05.142
Ikeno T, Numata H, Goto SG (2011b) Circadian clock genes period and cycle regulate photoperiodic diapause in the bean bug Riptortus pedestris males. J Insect Physiol 57:935–938. https://doi.org/10.1016/j.jinsphys.2011.04.006
Ikeno T, Ishikawa K, Numata H, Goto SG (2013) Circadian clock gene Clock is involved in the photoperiodic response of the bean bug Riptortus pedestris. Physiol Entomol 38:157–162. https://doi.org/10.1111/phen.12013
Ikeno T, Numata H, Goto SG, Shiga S (2014) Involvement of the brain region containing pigment-dispersing factor-immunoreactive neurons in the photoperiodic response of the bean bug, Riptortus pedestris. J Exp Biol 217:453–462. https://doi.org/10.1242/jeb.091801
Johard HAD, Yoshii T, Dircksen H, Cusumano P, Rouyer F, Helfrich-Förster C et al (2009) Peptidergic clock neurons in Drosophila: ion transport peptide and short neuropeptide F in subsets of dorsal and ventral lateral neurons. J Comp Neurol 516:59–73. https://doi.org/10.1002/cne.22099
Kang DS, Denlinger DL, Sim C (2014) Suppression of allatotropin simulates reproductive diapause in the mosquito Culex pipiens. J Insect Physiol 64:48–53. https://doi.org/10.1016/j.jinsphys.2014.03.005
Kidokoro T, Masaki S (1978) Photoperiodic response in relation to variable voltinism in the ground cricket, Pteronemobius fascipes Walker (Orthoptera: Gryllidae). Jpn J Ecol 28:291–298. https://doi.org/10.18960/SEITAI.28.4_291
King AN, Sehgal A (2020) Molecular and circuit mechanisms mediating circadian clock output in the Drosophila brain. Eur J Neurosci 51:268–281. https://doi.org/10.1111/ejn.14092
Kobayashi S, Numata H (1993) Photoperiodic responses controlling the induction of adult diapause and the determination of seasonal form in the bean bug, Riptortus clavatus. Zool Sci 10:983–990
Koide R, Xi J, Hamanaka Y, Shiga S (2021) Mapping PERIOD-immunoreactive cells with neurons relevant to photoperiodic response in the bean bug Riptortus pedestris. Cell Tissue Res 385:571–583. https://doi.org/10.1007/s00441-021-03451-6
Koštál V (2006) Eco-physiological phases of insect diapause. J Insect Physiol 52:113–127. https://doi.org/10.1016/j.jinsphys.2005.09.008
Koštál V, Stetina T, Poupardin R, Korbelová J, Bruce AW (2017) Conceptual framework of the eco-physiological phases of insect diapause development justified by transcriptomic profiling. Proc Natl Acad Sci USA 114:8532–8537. https://doi.org/10.1073/pnas.1707281114
Kotwica-Rolinska J, Pivarciova L, Vaneckova H, Dolezel D (2017) The role of circadian clock genes in the photoperiodic timer of the linden bug Pyrrhocoris apterus during the nymphal stage. Physiol Entomol 42:266–273. https://doi.org/10.1111/phen.12197
Kotwica-Rolinska J, Chodáková L, Smýkal V, Damulewicz M, Provazník J, Wu BC-H et al (2022a) Loss of timeless underlies an evolutionary transition within the circadian clock. Mol Biol Evol 39:msab346. https://doi.org/10.1093/molbev/msab346
Kotwica-Rolinska J, Damulewicz M, Chodakova L, Kristofova L, Dolezel D (2022b) Pigment dispersing factor is a circadian clock output and regulates photoperiodic response in the linden bug, Pyrrhocoris apterus. Front Physiol 13:884909. https://doi.org/10.3389/fphys.2022.884909
Kutaragi Y, Tokuoka A, Tomiyama Y, Nose M, Watanabe T, Bando T et al (2018) A novel photic entrainment mechanism for the circadian clock in an insect: involvement of c-fos and cryptochromes. Zool Lett 4:26. https://doi.org/10.1186/s40851-018-0109-8
Mano G, Goto SG (2022) Photoperiod controls insulin and juvenile hormone signaling pathways via the circadian clock in the bean bug Riptortus pedestris. Appl Entomol Zool 57:363–377. https://doi.org/10.1007/s13355-022-00795-5
Meiselman MR, Alpert MH, Cui X, Shea J, Gregg I, Gallio M et al (2022) Recovery from cold-induced reproductive dormancy is regulated by temperature-dependent AstC signaling. Curr Biol 32:1362–1375. https://doi.org/10.1016/j.cub.2022.01.061
Meuti ME, Stone M, Ikeno T, Denlinger DL (2015) Functional circadian clock genes are essential for the overwintering diapause of the Northern house mosquito, Culex pipiens. J Exp Biol 218:412–422. https://doi.org/10.1242/jeb.113233
Miki T, Shinohara T, Chafino S, Noji S, Tomioka K (2020) Photoperiod and temperature separately regulate nymphal development through JH and insulin/TOR signaling pathways in an insect. Proc Natl Acad Sci USA 117:5525–5531. https://doi.org/10.1073/pnas.1922747117
Mizoguchi A, Ohsumi S, Kobayashi K, Okamoto N, Yamada N, Tateishi K et al (2013) Prothoracicotropic hormone acts as a neuroendocrine switch between pupal diapause and adult development. PLoS One 8:e608824. https://doi.org/10.1371/journal.pone.0060824
Mohamed AAM, Wang Q, Bembenek J, Ichihara N, Hiragaki S, Suzuki T et al (2014) N-acetyltransferase (nat) is a critical conjunct of photoperiodism between the circadian system and endocrine axis in Antheraea pernyi. PLoS One 9:e92680. https://doi.org/10.1371/journal.pone.0092680
Morita A, Numata H (1997) Role of the neuroendocrine complex in the control of adult diapause in the bean bug, Riptortus clavatus. Arch Insect Biochem Physiol 35:347–355. https://doi.org/10.1002/(sici)1520-6327(199705)35:3%3C347::aid-arch8%3E3.0.co;2-q
Morita A, Soga K, Hoson T, Kamisaka S, Numata H (1999) Changes in mechanical properties of the cuticle and lipid accumulation in relation to adult diapause in the bean bug, Riptortus clavatus. J Insect Physiol 45:241–247. https://doi.org/10.1016/S0022-1910(98)00119-X
Mukai A, Goto SG (2016) The clock gene period is essential for the photoperiodic response in the jewel wasp Nasonia vitripennis (Hymenoptera: Pteromalidae). Appl Entomol Zool 51:185–194. https://doi.org/10.1007/s13355-015-0384-1
Nagy D, Cusumano P, Andreatta G, Anduaga AM, Hermann-Luibl C, Reinhard N et al (2019) Peptidergic signaling from clock neurons regulates reproductive dormancy in Drosophila melanogaster. PLoS Genet 15:e1008158. https://doi.org/10.1371/journal.pgen.1008158
Nelson RJ, Denlinger DL, Somers DE (2010) Photoperiodism: the biological calendar. Oxford University Press, Oxford
Noguchi H, Hayakawa Y (1997) Role of dopamine at the onset of pupal diapause in the cabbage armyworm Mamestra brassicae. FEBS Lett 413:157–161. https://doi.org/10.1016/S0014-5793(97)00848-X
Noguchi H, Hayakawa Y (2001) Dopamine is a key factor for the induction of egg diapause of the silkworm, Bombyx mori. Eur J Biochem 268:774–780. https://doi.org/10.1046/j.1432-1327.2001.01933.x
Numata H, Hidaka T (1982) Photoperiodic control of adult diapause in the bean bug, Riptortus clavatus Thunberg (Heteroptera: Coreidae) I. Reversible induction and termination of diapause. Appl Entomol Zool 17:530–538. https://doi.org/10.1303/aez.17.530
Numata H, Hidaka T (1984) Termination of adult diapause by a juvenile hormone analogue in the bean bug, Riptortus clavatus. Zool Sci 1:751–754
Numata H, Kobayashi S (1989) Morphological and behavioral character of adult diapause and its termination by a juvenile hormone analogue in Riptortus clavatus. In: Tonner M, Soldan T, Bennettova B (eds) Regulation of insect reproduction IV, Proceedings of a symposium held in Zinkovy, Sept 1987. Academia Publishing House of the Czech Academy of Sciences, Praha, pp 401–411
Omura S, Numata H, Goto SG (2016) Circadian clock regulates photoperiodic responses governed by distinct output pathways in the bean bug, Riptortus pedestris. Biol Rhythm Res 47:937–945. https://doi.org/10.1080/09291016.2016.1212515
Pavelka J, Shimada K, Kostal V (2003) TIMELESS: a link between fly’s circadian and photoperiodic clocks? Eur J Entomol 100:255–265. https://doi.org/10.14411/eje.2003.041
Pittendrigh CS, Minis DH (1964) The entrainment of circadian oscillations by light and their role as photoperiodic clocks. Am Nat 98:261–294. https://doi.org/10.1086/282327
Poupardin R, Schöttner K, Korbelová J, Provazník J, Doležel D, Pavlinic D et al (2015) Early transcriptional events linked to induction of diapause revealed by RNAseq in larvae of drosophilid fly, Chymomyza costata. BMC Genomics 16:1–19. https://doi.org/10.1186/s12864-015-1907-4
Sakamoto T, Tomioka K (2007) Effects of unilateral compound-eye removal on the photoperiodic responses of nymphal development in the cricket Modicogryllus siamensis. Zool Sci 24:604–610. https://doi.org/10.2108/zsj.24.604
Sakamoto T, Uryu O, Tomioka K (2009) The clock gene period plays an essential role in photoperiodic control of nymphal development in the cricket Modicogryllus siamensis. J Biol Rhythm 24:379–390. https://doi.org/10.1177/0748730409341523
Sandrelli F, Tauber E, Pegoraro M, Mazzotta G, Cisotto P, Landskron J et al (2007) A molecular basis for natural selection at the timeless locus in Drosophila melanogaster. Science 316:1898–1900. https://doi.org/10.1126/science.1138426
Saunders D (2021) Insect photoperiodism: Bünning’s hypothesis, the history and development of an idea. Eur J Entomol 118:1–13. https://doi.org/10.14411/EJE.2021.001
Saunders DS, Henrich VC, Gilbert LI (1989) Induction of diapause in Drosophila melanogaster: photoperiodic regulation and the impact of arrhythmic clock mutations on time measurement. Proc Natl Acad Sci USA 86:3748–3752. https://doi.org/10.1073/pnas.86.10.3748
Senthilan PR, Grebler R, Reinhard N, Rieger D, Helfrich-Förster C (2019) Role of rhodopsins as circadian photoreceptors in the Drosophila melanogaster. Biology (Basel) 8:6. https://doi.org/10.3390/biology8010006
Shafer OT, Helfrich-Förster C, Renn SCP, Taghert PH (2006) Reevaluation of Drosophila melanogaster’s neuronal circadian pacemakers reveals new neuronal classes. J Comp Neurol 498:180–193. https://doi.org/10.1002/CNE.21021
Shiomi K, Takasu Y, Kunii M, Tsuchiya R, Mukaida M et al (2015) Disruption of diapause induction by TALEN-based gene mutagenesis in relation to a unique neuropeptide signaling pathway in Bombyx. Sci Rep 5:15566. https://doi.org/10.1038/srep15566
Sim C, Denlinger DL (2008) Insulin signaling and FOXO regulate the overwintering diapause of the mosquito Culex pipiens. Proc Natl Acad Sci USA 105:6777–6781. https://doi.org/10.1073/pnas.0802067105
Sim C, Denlinger DL (2009) A shut-down in expression of an insulin-like peptide, ILP-1, halts ovarian maturation during the overwintering diapause of the mosquito Culex pipiens. Insect Mol Biol 18:325–332. https://doi.org/10.1111/j.1365-2583.2009.00872.x
Sim C, Denlinger DL (2013) Juvenile hormone III suppresses forkhead of transcription factor in the fat body and reduces fat accumulation in the diapausing mosquito, Culex pipiens. Insect Mol Biol 22:1–11. https://doi.org/10.1111/j.1365-2583.2012.01166.x
Song SH, Öztürk N, Denaro TR, Arat NÖ, Kao YT, Zhu H et al (2007) Formation and function of flavin anion radical in cryptochrome 1 blue-light photoreceptor of monarch butterfly. J Biol Chem 282:17608–17612. https://doi.org/10.1074/jbc.M702874200
Tagaya J, Numata H, Goto SG (2010) Sexual difference in the photoperiodic induction of pupal diapause in the flesh fly Sarcophaga similis. Entomol Sci 13:311–319. https://doi.org/10.1111/j.1479-8298.2010.00394.x
Tamai T, Shiga S, Goto SG (2019) Roles of the circadian clock and endocrine regulator in the photoperiodic response of the brown-winged green bug Plautia stali. Physiol Entomol 44:43–52. https://doi.org/10.1111/phen.12274
Tamaki S, Takemoto S, Uryu O, Kamae Y, Tomioka K (2013) Opsins are involved in nymphal photoperiodic responses in the cricket Modicogryllus siamensis. Physiol Entomol 38:163–172. https://doi.org/10.1111/phen.12015
Tauber E, Zordan M, Sandrelli F, Pegoraro M, Osterwalder N, Breda C et al (2007) Natural selection favors a newly derived timeless allele in Drosophila melanogaster. Science 316:1895–1898. https://doi.org/10.1126/science.1138412
Tobita H, Kiuchi T (2022) Knockouts of positive and negative elements of the circadian clock disrupt photoperiodic diapause induction in the silkworm, Bombyx mori. Insect Biochem Mol Biol 149:103842. https://doi.org/10.1016/j.ibmb.2022.103842
Tokuoka A, Itoh TQ, Hori S, Uryu O, Danbara Y, Nose M et al (2017) Cryptochrome genes form an oscillatory loop independent of the per/tim loop in the circadian clockwork of the cricket Gryllus bimaculatus. Zool Lett 3:1–14. https://doi.org/10.1186/s40851-017-0066-7
Tsuchiya R, Kaneshima A, Kobayashi M, Yamazaki M, Takasu Y, Sezutsu H et al (2021) Maternal GABAergic and GnRH/corazonin pathway modulates egg diapause phenotype of the silkworm Bombyx mori. Proc Natl Acad Sci USA 118:e2020028008. https://doi.org/10.1073/pnas.2020028118
Tyshchenko VP (1966) Two-oscillatory model of the physiological mechanism of insect photoperiodic reaction. Zh Obshch Biol 27:209–222. (in Russian)
Ueda H, Tamaki S, Miki T, Uryu O, Kamae Y, Nose M et al (2018) cryptochrome genes mediate photoperiodic responses in the cricket Modicogryllus siamensis. Physiol Entomol 43:285–294. https://doi.org/10.1111/phen.12258
Urbanová V, Bazalová O, Vaněčková H, Dolezel D (2016) Photoperiod regulates growth of male accessory glands through juvenile hormone signaling in the linden bug, Pyrrhocoris apterus. Insect Biochem Mol Biol 70:184–190. https://doi.org/10.1016/j.ibmb.2016.01.003
Uryu M, Ninomiya Y, Yokoi T, Tsuzuki S, Hayakawa Y (2003) Enhanced expression of genes in the brains of larvae of Mamestra brassicae (Lepidoptera: Noctuidae) exposed to short daylength or fed Dopa. Eur J Entomol 100:245–250
Van Der Kooi CJ, Stavenga DG, Arikawa K, Belušič G, Kelber A (2021) Evolution of insect color vision: from spectral sensitivity to visual ecology. Annu Rev Entomol 66:435–461. https://doi.org/10.1146/annurev-ento-061720-071644
Vaz Nunes M, Saunders D (1999) Photoperiodic time measurement in insects: a review of clock models. J Biol Rhythm 14:84–104. https://doi.org/10.1177/074873049901400202
Veerman A (1980) Functional involvement of carotenoids in photoperiodic induction of diapause in the spider mite, Tetranychus urticae. Physiol Entomol 5:291–300. https://doi.org/10.1111/j.1365-3032.1980.tb00237.x
Wang Q, Mohamed AAM, Takeda M (2013) Serotonin receptor B may lock the gate of PTTH release/synthesis in the Chinese silk moth, Antheraea pernyi; a diapause initiation/maintenance mechanism? PLoS One 8:1–13. https://doi.org/10.1371/journal.pone.0079381
Wang Q, Egi Y, Takeda M, Oishi K, Sakamoto K (2015a) Melatonin pathway transmits information to terminate pupal diapause in the Chinese oak silkmoth Antheraea pernyi and through reciprocated inhibition of dopamine pathway functions as a photoperiodic counter. Entomol Sci 18:74–84. https://doi.org/10.1111/ens.12083
Wang Q, Hanatani I, Takeda M, Oishi K, Sakamoto K (2015b) D2-like dopamine receptors mediate regulation of pupal diapause in Chinese oak silkmoth Antheraea pernyi. Entomol Sci 18:193–198. https://doi.org/10.1111/ens.12099
Yamada H, Yamamoto MT (2011) Association between circadian clock genes and diapause incidence in Drosophila triauraria. PLoS One 6:e27493. https://doi.org/10.1371/journal.pone.0027493
Yamada N, Kataoka H, Mizoguchi A (2017) Myosuppressin is involved in the regulation of pupal diapause in the cabbage army moth Mamestra brassicae. Sci Rep 7:1–9. https://doi.org/10.1038/srep41651
Yamashita O (1996) Diapause hormone of the silkworm, Bombyx mori: structure, gene expression and function. J Insect Physiol 42:669–679. https://doi.org/10.1016/0022-1910(96)00003-0
Yuan Q, Metterville D, Briscoe AD, Reppert SM (2007) Insect cryptochromes: gene duplication and loss define diverse ways to construct insect circadian clocks. Mol Biol Evol 24:948–955. https://doi.org/10.1093/molbev/msm011
Zhu L, Tian Z, Guo S, Liu W, Zhu F, Wang X-P (2019) Circadian clock genes link photoperiodic signals to lipid accumulation during diapause preparation in the diapause-destined female cabbage beetles Colaphellus bowringi. Insect Biochem Mol Biol 104:1–10. https://doi.org/10.1016/j.ibmb.2018.11.001
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2023 The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd.
About this chapter
Cite this chapter
Goto, S.G. (2023). Molecular Mechanisms of Photoperiodism. In: Numata, H., Tomioka, K. (eds) Insect Chronobiology. Entomology Monographs. Springer, Singapore. https://doi.org/10.1007/978-981-99-0726-7_13
Download citation
DOI: https://doi.org/10.1007/978-981-99-0726-7_13
Published:
Publisher Name: Springer, Singapore
Print ISBN: 978-981-99-0725-0
Online ISBN: 978-981-99-0726-7
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)