Research Progress and Prospects of Circadian Clock in Lepidoptera

doi:10.11923/j.issn.2095-4050.cjas2022-0097

Abstract

Abstract:

A long period of evolution causes obviously diurnal and seasonal rhythmic changes in insect life and behavior-circadian clock. At present, Lepidoptera is the most species-rich group of insects, including about 160000 identified species of butterflies and moths, and nearly 70% of the important major agricultural and forestry pests belong to Lepidoptera. The research progress of the circadian clock in Lepidoptera is of great significance for in-depth analysis of variable physiological and behavioral regulation mechanisms of Lepidoptera, effective development of the production of economic insects, and the control of agricultural and forestry pests. In this paper, the effects of the circadian clock on hatching, eating, growth, metamorphosis, reproduction and diapause, courtship behavior and migration in Lepidoptera were summarized. And the critical research advances of molecular regulation of circadian clock and coordinated regulation of circadian clock and endocrine hormones in Lepidoptera were particularly described. Based on the circadian clock principle, we discussed the co-evolutionary relationship between Lepidoptera and plants and its important ecological implications, and the application prospect of circadian clock theory in agricultural pest control and economic insect rearing improvement.

Key words: Lepidoptera, circadian clock, signal transduction, circadian behaviors, metabolism, regulation mechanism

QUAN Linfa, YAO Qiong, DONG Yizhi, XU Shu, CHI Yanyan, CHEN Bingxu. Research Progress and Prospects of Circadian Clock in Lepidoptera[J]. Journal of Agriculture, 2023, 13(9): 38-45.

Figures/Tables 2

References 55

[1]	EELDERINK-CHEN Z, BOSMAN J, SARTOR F, et al. A circadian clock in a non-photosynthetic prokaryote[J]. Science advances, 2021, 7(2):2086.
[2]	陶卉, 徐世清. 鳞翅目昆虫昼夜节律的授时机制研究进展[J]. 生命科学, 2015, 27(11):1355-1363.
[3]	KONOPKA R J, BENZER S. Clock mutants of Drosophila melanogaster[J]. Proceedings of the National Academy of Sciences of the United States of America, 1971, 68(9).
[4]	KAWAHARA A Y, PLOTKIN D, ESPELAND M, et al. Phylogenomics reveals the evolutionary timing and pattern of butterflies and moths[J]. Proceedings of the National Academy of Sciences of the United States of America, 2019, 116(45).
[5]	ROE A, WELLER S, BAIXERAS J, et al. Evolutionary framework for Lepidoptera model systems. In: Genetics and molecular biology of lepidoptera[M]. Boca Raton: CRC Press, 2009:1-24.
[6]	WILLIAMS C M. Control of pupal diapause by the direct action of light on the insect brain[J]. Science, 1963, 140:386. pmid: 17815799
[7]	TRUMAN J W, RIDDIFORD L M. Neuroendocrine control of ecdysis in silk moths[J]. Science, 1970, 167:1624-1626. doi: 10.1126/science.167.3925.1624 URL
[8]	任爽, 魏慧敏, 郝友进, 等. 昆虫钟基因研究进展[J]. 昆虫学报, 2016, 59(3):353-364.
[9]	王文栋, 束梅影, 张达艳, 等. 家蚕昼夜节律生物钟基因的生物信息学分析[J]. 四川动物, 2016, 35(2):275-282.
[10]	ROSÉN W Q, HAN G B, LÖFSTEDT C. The circadian rhythm of the sex-pheromone-mediated behavioral response in the turnip moth, Agrotis segetum, is not controlled at the peripheral level[J]. Journal of biological rhythms, 2003, 18(5).
[11]	SILVEGREN G, LOFSTEDT C, ROSÉN W Q. Circadian mating activity and effect of pheromone pre-exposure on pheromone response rhythms in the moth Spodoptera littoralis[J]. Journal of insect physiology, 2005, 51:277-286. doi: 10.1016/j.jinsphys.2004.11.013 URL
[12]	LEVI-ZADA A, DAVID M, FEFER D, et al. Circadian release of male-specific components of the greater date moth, Aphomia (Arenipses) sabella, using sequential SPME/GC/MS analysis[J]. Journal of chemical ecology, 2014, 40(3):236-43. doi: 10.1007/s10886-014-0391-7 URL
[13]	冀佳悦. 粘虫生物钟基因的克隆、表达及功能分析[D]. 杨凌: 西北农林科技大学, 2017.
[14]	BRADY D, SAVIANE A, CAPPELLOZZA S, et al. The circadian clock in lepidoptera[J]. Frontiers in physiology, 2021, 17(12):776826.
[15]	KOTWICA J, BEBAS P, GVAKHARIA BO, et al. RNA interference of the period gene affects the rhythm of sperm release in moths[J]. Journal of biological rhythms, 2009, 24:25-34. doi: 10.1177/0748730408329109 pmid: 19150927
[16]	REPPERT S M, GEGEAR R J, MERLIN C. Navigational mechanisms of migrating monarch butterflies[J]. Trends neurosci, 2010, 33(9):399-406. doi: 10.1016/j.tins.2010.04.004 pmid: 20627420
[17]	MIZOGUCHI A, ISHIZAKI H. Prothoracic glands of the saturniid moth Samia cynthia ricini possess a circadian clock controlling gut purge timing[J]. Proceedings of the National Academy of Sciences of the United States of America, 1982, 79:2726-2730.
[18]	ZHANG J, LI S, LI W, et al. Circadian regulation of night feeding and daytime detoxification in a formidable Asian pest Spodoptera litura[J]. Communications biology, 2021, 4:286. doi: 10.1038/s42003-021-01816-9
[19]	SAUMAN I, REPPERT S M. Brain control of embryonic circadian rhythms in the silkmoth Antheraea pernyi[J]. Neuron, 1998, 20:741-748. doi: 10.1016/S0896-6273(00)81012-0 URL
[20]	SUSZCZYNSKA A, KANIEWSKA M M, BEBAS P, et al. Circadian regulation of caterpillar feeding and growth[J]. Journal of insect physiology, 2017, 101:113-122. doi: S0022-1910(17)30231-7 pmid: 28733238
[21]	徐继伟. 斜纹夜蛾生物钟基因的表达特征及Period基因的突变检测[D]. 淮北: 淮北师范大学, 2021.
[22]	牛小慧, 贺鹏, 张婷, 等. 甜菜夜蛾生物钟基因Per和Tim的分子克隆及昼夜表达动态[J]. 南京农业大学学报, 2012, 35(1):51-56.
[23]	JI J Y, LIU Y Q, ZHANG L, et al. The clock gene, period, influences migratory flight and reproduction of the oriental armyworm, Mythimna separata (Walker)[J]. Insect science, 2003, 30(3):650-660.
[24]	GVAKHARIA B O, KILGORE J A, BEBAS P, et al. Temporal and spatial expression of the period gene in the reproductive system of the codling moth[J]. Journal of biological rhythms, 2000, 15(1):4-12. pmid: 10677012
[25]	方海波, 张璟, 刘小侠, 等. 梨小食心虫生物钟基因Gmper和Gmtim的鉴定及其对羽化节律的影响[J]. 昆虫学报, 2020, 63(6):655-666.
[26]	闫硕, 刘彦君, 张馨方, 等. 棉铃虫生物钟基因HeDbt的克隆和表达模式分析[J]. 昆虫学报, 2018, 61(12):1393-1403.
[27]	刘孝明, 张松斗, 马木提, 等. 光周期和温度对生物钟基因cwo在棉铃虫幼虫节律表达的影响[J]. 应用昆虫学报, 2016, 53(5):942-952.
[28]	PALOMARES L A, JOOSTEN C E, HUGHES P R, et al. Novel insect cell line capable of complex N-glycosylation and sialylation of recombinant proteins[J]. Biotechnology progress, 2003, 19:185-192. pmid: 12573024
[29]	ZHU H, SAUMAN I, YUAN Q, et al. Cryptochromes define a novel circadian clock mechanism in monarch butterflies that may underlie sun compass navigation[J]. PLoS biology, 2008, 6:e4. doi: 10.1371/journal.pbio.0060004 URL
[30]	ZHU H, YUAN Q, BRISCOE A D, et al. The two CRYs of the butterfly[J]. Current biology, 2005, 15:R953-R954. doi: 10.1016/j.cub.2005.11.030 pmid: 16332522
[31]	YUAN Q, METTERVILLE D, BRISCOE A D, et al. Insect cryptochromes: Gene duplication and loss define diverse ways to construct insect circadian clocks[J]. Molecular biology and evolution, 2007, 24:948-955. doi: 10.1093/molbev/msm011 pmid: 17244599
[32]	ZHAN S, MERLIN C, BOORE J L, et al. The monarch butterfly genome yields insights into long-distance migration[J]. Cell, 2011, 147:1171-1185. doi: 10.1016/j.cell.2011.09.052 pmid: 22118469
[33]	MARKERT M J, ZHANG Y, ENUAMEH M S, et al. Genomic access to monarch migration using TALEN and CRISPR/Cas9-mediated targeted mutagenesis[J]. G3, 2016, 6:905-915. doi: 10.1534/g3.116.027029 URL
[34]	MERLIN C, BEAVER L E, TAYLOR O R, et al. Efficient targeted mutagenesis in the monarch butterfly using zinc-finger nucleases[J]. Genome research, 2013, 23:159-168. doi: 10.1101/gr.145599.112 pmid: 23009861
[35]	ZHANG Y, MARKERT M J, GROVES S C, et al. Vertebrate-like cryptochrome-2 from monarch regulates circadian transcription via independent repression of clock and Bmal1 activity[J]. Proceedings of the National Academy of Sciences of the United States of America, 2017, 114:E7516-E7525.
[36]	DERKS M F, SMIT S, SALIS L, et al. The genome of winter moth (Operophtera brumata) provides a genomic perspective on sexual dimorphism and phenology[J]. Genome biology and evolution, 2015, 7:2321-2332. doi: 10.1093/gbe/evv145 pmid: 26227816
[37]	TAO H, LI X, QIU J F, et al. The light cycle controls the hatching rhythm in Bombyx mori via negative feedback loop of the circadian oscillator[J]. Archives of insect biochemistry and physiology, 2017, 96:e21408. doi: 10.1002/arch.21408 URL
[38]	IKEDA K, DAIMON T, SEZUTSU H, et al. Involvement of the clock gene period in the circadian rhythm of the silkmoth Bombyx mori[J]. Journal of biological rhythms, 2019, 34:283-292. doi: 10.1177/0748730419841185 URL
[39]	NARTEY M A, SUN X, QIN S, et al. CRISPR/Cas9-based knockout reveals that the clock gene timeless is indispensable for regulating circadian behavioral rhythms in Bombyx mori[J]. Insect science, 2020, 28:1414-1425. doi: 10.1111/ins.v28.5 URL
[40]	SAUMAN I, REPPERT S M. Circadian clock neurons in the silkmoth Antheraea pernyi: Novel mechanisms of period protein regulation[J]. Neuron, 1996, 17:889-900. doi: 10.1016/S0896-6273(00)80220-2 URL
[41]	SINTUREL F, PETRENKO V, DIBNER C. Circadian clocks make metabolism run[J]. Journal of molecular biology, 2020, 432:3680-3699. doi: S0022-2836(20)30070-X pmid: 31996313
[42]	SUN S, HANZAWA F, KIM D, et al. Circadian rhythm-dependent induction of hepatic lipogenic gene expression in rats fed a high-sucrose diet[J]. Journal of biological chemistry, 2019, 294:15206-15217. doi: 10.1074/jbc.RA119.010328 pmid: 31481463
[43]	KUMAR JHA P, CHALLET E, KALSBEEK A. Circadian rhythms in glucose and lipid metabolism in nocturnal and diurnal mammals[J]. Molecular and cellular endocrinology, 2015, 418:74-88. doi: 10.1016/j.mce.2015.01.024 URL
[44]	BIANCOLIN A D, MARCHENKO A, MITTOVA E, et al. The core clock gene, Bmal1, and its downstream target, the snare regulatory protein secretagogin, are necessary for circadian secretion of glucagon-like peptide-1[J]. Molecular metabolism, 2020, 31:124-137. doi: S2212-8778(19)30931-7 pmid: 31918914
[45]	WALKER II W H, WALTON J C, DEVRIES A C, et al. Circadian rhythm disruption and mental health[J]. Translational psychiatry, 2020, 10:28. doi: 10.1038/s41398-020-0694-0 pmid: 32066704
[46]	CHAIX A, LIN T, LE H D, et al. Time-restricted feeding prevents obesity and metabolic syndrome in mice lacking a circadian clock[J]. Cell metabolism, 2019, 28:303-319.
[47]	IKEDA K, DAIMON T, SHIOMI K, et al, Involvement of the clock gene period in the photoperiodism of the silkmoth Bombyx mori[J]. Zoology Science, 2021, 38(6):523-530.
[48]	CUI W Z, QIU J F, DAI T M, et al. Circadian clock gene period contributes to diapause via GABAeric-diapause hormone pathway in Bombyx mori[J]. Biology, 2021, 30, 10(9):842.
[49]	BROADHEAD G T, BASU T, VON ARX M, et al. Diel rhythms and sex differences in the locomotor activity of hawkmoths[J]. Journal of experimental biology, 2017, 220:1472-1480.
[50]	FENSKE M P, NGUYEN L P, HORN E K, et al. Circadian clocks of both plants and pollinators influence flower seeking behavior of the pollinator hawkmoth Manduca sexta[J]. Science reports, 2018, 8(1):2842.
[51]	GOODSPEED D, CHENAB EW, MIN-VENDITTI A, et al. Arabidopsis synchronizes jasmonate-mediated defense with insect circadian behavior[J]. Proceedings of the National Academy of Sciences of the United States of America, 2012, 109:4674-4677. doi: 10.1073/pnas.1116368109 pmid: 22331878
[52]	KIM Y, HONG Y. Regulation of hemolymph trehalose level by an insulin-like peptide through diel feeding rhythm of the beet armyworm Spodoptera exigua[J]. Peptides, 2015, 68:91-98. doi: 10.1016/j.peptides.2015.02.003 URL
[53]	郭金虎, 徐璎, 张二荃, 等. 生物钟研究进展及重要前沿科学问题[J]. 中国科学基金, 2014, 28(3):179-186.
[54]	XIA Q, LI S, FENG Q. Advances in silkworm studies accelerated by the genome sequencing of Bombyx mori[J]. Annual review of entomology, 2014, 59:513-536. doi: 10.1146/ento.2013.59.issue-1 URL
[55]	龙定沛, 郝占章, 向仲怀, 等. 家蚕基因组靶向编辑技术研究进展[J]. 昆虫学报, 2018, 61(3):371-384. doi: 10.16380/j.kcxb.2018.03.012