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Identification and dynamic expression profiling of circadian clock genes in Spodoptera litura provide new insights into the regulation of sex pheromone communication

Published online by Cambridge University Press:  14 July 2021

Ji-Wei Xu ,
Lu-Lu Li ,
Meng Wang ,
Hui-Hui Yang ,
Wei-Chen Yao ,
Youssef Dewer ,
Xiu-Yun Zhu  and
Ya-Nan Zhang Open the ORCID record for Ya-Nan Zhang [Opens in a new window]
Ji-Wei Xu
Affiliation:
Anhui Province Key Laboratory of Pollutant Sensitive Materials and Environmental Remediation, College of Life Sciences, Huaibei Normal University, 100 Dongshan Road, Huaibei 235000, China
Lu-Lu Li
Affiliation:
Anhui Province Key Laboratory of Pollutant Sensitive Materials and Environmental Remediation, College of Life Sciences, Huaibei Normal University, 100 Dongshan Road, Huaibei 235000, China
Meng Wang
Affiliation:
Anhui Province Key Laboratory of Pollutant Sensitive Materials and Environmental Remediation, College of Life Sciences, Huaibei Normal University, 100 Dongshan Road, Huaibei 235000, China
Hui-Hui Yang
Affiliation:
Anhui Province Key Laboratory of Pollutant Sensitive Materials and Environmental Remediation, College of Life Sciences, Huaibei Normal University, 100 Dongshan Road, Huaibei 235000, China
Wei-Chen Yao
Affiliation:
Anhui Province Key Laboratory of Pollutant Sensitive Materials and Environmental Remediation, College of Life Sciences, Huaibei Normal University, 100 Dongshan Road, Huaibei 235000, China
Youssef Dewer
Affiliation:
Bioassay Research Department, Central Agricultural Pesticide Laboratory, Agricultural Research Center, 7 Nadi El-Seid Street, Dokki 12618, Giza, Egypt
Xiu-Yun Zhu*
Affiliation:
Anhui Province Key Laboratory of Pollutant Sensitive Materials and Environmental Remediation, College of Life Sciences, Huaibei Normal University, 100 Dongshan Road, Huaibei 235000, China
Ya-Nan Zhang*
Affiliation:
Anhui Province Key Laboratory of Pollutant Sensitive Materials and Environmental Remediation, College of Life Sciences, Huaibei Normal University, 100 Dongshan Road, Huaibei 235000, China
*
Author for correspondence: Xiu-Yun Zhu, Email: xyzhuhbnu@163.com; Ya-Nan Zhang, Email: ynzhang_insect@163.com
Author for correspondence: Xiu-Yun Zhu, Email: xyzhuhbnu@163.com; Ya-Nan Zhang, Email: ynzhang_insect@163.com
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Abstract

Spodoptera litura is an important pest that causes significant economic damage to numerous crops worldwide. Sex pheromones (SPs) mediate sexual communication in S. litura and show a characteristic degree of rhythmic activity, occurring mainly during the scotophase; however, the specific regulatory mechanisms remain unclear. Here, we employed a genome-wide analysis to identify eight candidate circadian clock genes in S. litura. Sequence characteristics and expression patterns were analyzed. Our results demonstrated that some circadian clock genes might regulate the biosynthesis and perception of SPs by regulating the rhythmic expression of SP biosynthesis-related genes and SP perception-related genes. Interestingly, all potential genes exhibited peak expression in the scotophase, consistent with the SP could mediate courtship and mating behavior in S. litura. Our findings are helpful in elucidating the molecular mechanism by which circadian clock genes regulate sexual communication in S. litura.

Keywords

Circadian clock genesdynamic expressionsex pheromone biosynthesissex pheromone perceptionSpodoptera litura
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 112 , Issue 1 , February 2022 , pp. 78 - 90
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Ando, T and Yamakawa, R (2011) Analyses of lepidopteran sex pheromones by mass spectrometry. Trac Trends in Analytical Chemistry 30, 990–1002.CrossRefGoogle Scholar
Beaver, LM, Rush, BL, Gvakharia, BO and Giebultowicz, JM (2003) Noncircadian regulation and function of clock genes period and timeless in oogenesis of Drosophila melanogaster. Journal of Biological Rhythms 18, 463–472.CrossRefGoogle ScholarPubMed
Benito, J, Hoxha, V, Lama, C, Lazareva, AA, Ferveur, JF, Hardin, PE and Dauwalder, B (2010) The circadian output gene takeout is regulated by Pdp1. Proceedings of the National Academy of Sciences 107, 2544–2549.CrossRefGoogle Scholar
Chen, C, Xu, M, Anantaprakorn, Y, Rosing, M and Stanewsky, R (2018) nocte is required for integrating light and temperature inputs in circadian clock neurons of Drosophila. Current Biology 28, 1595–1605 e1593.CrossRefGoogle ScholarPubMed
Cheng, T, Wu, J, Wu, Y, Chilukuri, RV, Huang, L, Yamamoto, K, Feng, L, Li, W, Chen, Z, Guo, H, Liu, J, Li, S, Wang, X, Peng, L, Liu, D, Guo, Y, Fu, B, Li, Z, Liu, C, Chen, Y, Tomar, A, Hilliou, F, Montagne, N, Jacquin-Joly, E, D'alencon, E, Seth, RK, Bhatnagar, RK, Jouraku, A, Shiotsuki, T, Kadono-Okuda, K, Promboon, A, Smagghe, G, Arunkumar, KP, Kishino, H, Goldsmith, MR, Feng, Q, Xia, Q and Mita, K (2017) Genomic adaptation to polyphagy and insecticides in a major east Asian noctuid pest. Nature Ecology & Evolution 1, 1747–1756.CrossRefGoogle Scholar
Crosby, P, Hamnett, R, Putker, M, Hoyle, NP, Reed, M, Karam, CJ, Maywood, ES, Stangherlin, A, Chesham, JE, Hayter, EA, Rosenbrier-Ribeiro, L, Newham, P, Clevers, H, Bechtold, DA and O'Neill, JS (2019) Insulin/IGF-1 drives PERIOD synthesis to entrain circadian rhythms with feeding time. Cell 177, 896–909.e820.CrossRefGoogle ScholarPubMed
Cuesta, IH, Lahiri, K, Lopez-Olmeda, JF, Loosli, F, Foulkes, NS and Vallone, D (2014) Differential maturation of rhythmic clock gene expression during early development in medaka (Oryzias latipes). Chronobiology International 31, 468–478.CrossRefGoogle Scholar
Dinesh-Kumar, A, Srimaan, E, Chellappandian, M, Vasantha-Srinivasan, P, Karthi, S, Thanigaivel, A, Ponsankar, A, Muthu-Pandian Chanthini, K, Shyam-Sundar, N, Annamalai, M, Kalaivani, K, Hunter, WB and Senthil-Nathan, S (2018) Target and non-target response of Swietenia mahagoni Jacq. chemical constituents against tobacco cutworm Spodoptera litura Fab. and earthworm, Eudrilus eugeniae Kinb. Chemosphere 199, 35–43.CrossRefGoogle ScholarPubMed
George, H and Terracol, R (1997) The vrille gene of Drosophila is a maternal enhancer of decapentaplegic and encodes a new member of the bZIP family of transcription factors. Genetics 146, 1345–1363.CrossRefGoogle ScholarPubMed
Goto, SG and Matsumoto, K (2018) Photoperiodism, insects. In Skinner, MK (ed.), Encyclopedia of Reproduction. Osaka, Japan: Osaka City University, pp. 420–425.CrossRefGoogle Scholar
Groot, AT (2014) Circadian rhythms of sexual activities in moths: a review. Frontiers in Ecology and Evolution 2, 43.CrossRefGoogle Scholar
Huang, Z, Curtin, K and Rosbash, M (1995) PER protein interactions and temperature compensation of a circadian clock in Drosophila. Science (New York, N.Y.) 267, 1169–1172.CrossRefGoogle ScholarPubMed
Jiang, YD, Yuan, X, Bai, YL, Wang, GY, Zhou, WW and Zhu, ZR (2018) Knockdown of timeless disrupts the circadian behavioral rhythms in Laodelphax striatellus (Hemiptera: Delphacidae). Environmental Entomology 47, 1216–1225.CrossRefGoogle Scholar
Konopka, RJ and Benzer, S (1971) Clock mutants of Drosophila melanogaster. Proceedings of the National Academy of Sciences of the USA 68, 2112–2116.CrossRefGoogle ScholarPubMed
Leal, WS (2013) Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Annual Review of Entomology 58, 373–391.CrossRefGoogle ScholarPubMed
Li, CJ, Yun, XP, Yu, XJ and Li, B (2018 a) Functional analysis of the circadian clock gene timeless in Tribolium castaneum. Insect Science 25, 418–428.CrossRefGoogle ScholarPubMed
Li, K, Chen, J, Jin, P, Li, J, Wang, J and Shu, Y (2018 b) Effects of Cd accumulation on cutworm Spodoptera litura larvae via Cd treated Chinese flowering cabbage Brassica campestris and artificial diets. Chemosphere 200, 151–163.CrossRefGoogle Scholar
Lin, Hy, Qian, K, Bai, Jx, Zhang, Dg, Lu, R and Wan, Xl (2017) Circadian rhythm of olfactory response and its regulation mechanism of Spodoptera litura. Journal of Wenzhou Medical University 47, 553–560.Google Scholar
Liu, NY, He, P and Dong, SL (2012) Binding properties of pheromone-binding protein 1 from the common cutworm Spodoptera litura. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 161, 295–302.CrossRefGoogle ScholarPubMed
Liu, NY, Liu, CC and Dong, SL (2013) Functional differentiation of pheromone-binding proteins in the common cutworm Spodoptera litura. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 165, 254–262.CrossRefGoogle ScholarPubMed
Liu, D, Jia, ZQ, Peng, YC, Sheng, CW, Tang, T, Xu, L, Han, ZJ and Zhao, CQ (2018) Toxicity and sublethal effects of fluralaner on Spodoptera litura Fabricius (Lepidoptera: Noctuidae). Pesticide Biochemistry and Physiology 152, 8–16.CrossRefGoogle Scholar
Lu, Q, Huang, LY, Liu, FT, Wang, XF, Chen, P, Xu, J, Deng, JY and Ye, H (2017) Sex pheromone titre in the glands of Spodoptera litura females: circadian rhythm and the effects of age and mating. Physiological Entomology 42, 156–162.CrossRefGoogle Scholar
Luo, LZ, Cao, WJ, Qian, K and Hu, Y (2003) Mating behavior and capacity of the beet armyworm, Spodoptera exigua (Lepidoptera: Noctuidae). Acta Entomologica Sinica 46, 494–499.Google Scholar
Lupien, M, Marshall, S, Leser, W, Pollack, GS and Honegger, H-W (2003) Antibodies against the PER protein of Drosophila label neurons in the optic lobe, central brain, and thoracic ganglia of the crickets Teleogryllus commodus and Teleogryllus oceanicus. Cell and Tissue Research 312, 377–391.CrossRefGoogle ScholarPubMed
Merlin, C, Lucas, P, Rochat, D, François, M-C, Maïbèche-Coisne, M and Jacquin-Joly, E (2007) An antennal circadian clock and circadian rhythms in peripheral pheromone reception in the moth Spodoptera littoralis. Journal of Biological Rhythms 22, 502–514.CrossRefGoogle ScholarPubMed
Meuti, ME, Stone, M, Ikeno, T and Denlinger, DL (2015) Functional circadian clock genes are essential for the overwintering diapause of the Northern house mosquito, Culex pipiens. Journal of Experimental Biology 218, 412–422.CrossRefGoogle ScholarPubMed
Muller, PY, Janovjak, H and Miserez, AZ (2002) Processing of gene expression data generated by quantitative real-time RT-PCR. Biotechniques 32, 1372–1374.Google ScholarPubMed
Nagari, M, Szyszka, P, Galizia, G and Bloch, G (2017) Task-related phasing of circadian rhythms in antennal responsiveness to odorants and pheromones in honeybees. Journal of Biological Rhythms 32, 593–608.CrossRefGoogle ScholarPubMed
Ozturk, N (2016) Phylogenetic and functional classification of the Photolyase/Cryptochrome family. Photochemistry and Photobiology 93, 104–111.CrossRefGoogle Scholar
Perret, M, Aujard, F, Seguy, M and Schilling, A (2003) Olfactory bulbectomy modifies photic entrainment and circadian rhythms of body temperature and locomotor activity in a nocturnal primate. Journal of Biological Rhythms 18, 392–401.CrossRefGoogle Scholar
Richier, B, Michard-Vanhée, C, Lamouroux, A, Papin, C and Rouyer, F (2008) The clockwork orange Drosophila protein functions as both an activator and a repressor of clock gene expression. Journal of Biological Rhythms 23, 103–116.CrossRefGoogle Scholar
Roelofs, WL (1995) Chemistry of sex attraction. Proceedings of the National Academy of Sciences of the USA 92, 44–49.CrossRefGoogle ScholarPubMed
Roelofs, WL and Jurenka, RA (1996) Biosynthetic enzymes regulating ratios of sex pheromone components in female redbanded leafroller moths. Bioorganic & Medicinal Chemistry 4, 461–466.CrossRefGoogle ScholarPubMed
Rosén, W (2002) Endogenous control of circadian rhythms of pheromone production in the turnip moth, Agrotis segetum. Archives of Insect Biochemistry and Physiology 50, 21–30.CrossRefGoogle ScholarPubMed
Rothenfluh, A, Young, MW and Saez, L (2000 a) A TIMELESS independent function for PERIOD protein in the Drosophila clock. Neuron 26, 505–514.CrossRefGoogle ScholarPubMed
Rothenfluh, A, Abodeely, M and Young, MW (2000 b) Short-period mutations of per affect a double-time-dependent step in the Drosophila circadian clock. Current Biology 19, 1399–1402.CrossRefGoogle Scholar
Rubin, EB, Shemesh, Y, Cohen, M, Elgavish, S, Robertson, HM and Bloch, G (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 Research 16, 1352–1365.CrossRefGoogle ScholarPubMed
Sauman, I and Reppert, SM (1996) Circadian clock neurons in the silkmoth Antheraea pernyi: novel mechanisms of period protein regulation. Neuron 17, 889–900.CrossRefGoogle ScholarPubMed
Seay, DJ and Thummel, CS (2011) The circadian clock, light, and cryptochrome regulate feeding and metabolism in Drosophila. Journal of Biological Rhythms 26, 497–506.CrossRefGoogle ScholarPubMed
Shad, SA, Sayyed, AH, Fazal, S, Saleem, MA and Zaka, SM (2012) Field evolved resistance to carbamates, organophosphates, pyrethroids, and new chemistry insecticides in Spodoptera litura Fab. (Lepidoptera: Noctuidae). Journal of Pest Science 85, 153–162.CrossRefGoogle Scholar
Shakeel, M, He, XZ, Martin, NA, Hanan, A and Wang, Q (2009) Diurnal periodicity of adult eclosion, mating and oviposition of the European leafminer Scaptomyza flava (Fallén) (Diptera: Drosophilidae). New Zealand Plant Protection 62, 80–85.CrossRefGoogle Scholar
Simon, P (2003) Q-Gene: processing quantitative real-time RT-PCR data. Bioinformatics (Oxford, England) 19, 1439–1440.CrossRefGoogle ScholarPubMed
Sun, F, Hu, YY and Du, JW (2002) The sex pheromone communication system of Spodoptera litura (Fabricius). Acta Entomologica Sinica 45, 404–407.Google Scholar
Tamura, K, Stecher, G, Peterson, D, Filipski, A and Kumar, S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.CrossRefGoogle ScholarPubMed
Tobback, J, Boerjan, B, Vandersmissen, HP and Huybrechts, R (2011) The circadian clock genes affect reproductive capacity in the desert locust Schistocerca gregaria. Insect Biochemistry and Molecular Biology 41, 313–321.CrossRefGoogle ScholarPubMed
Tobback, J, Boerjan, B, Vandersmissen, HP and Huybrechts, R (2012) Male reproduction is affected by RNA interference of period and timeless in the desert locust Schistocerca gregaria. Insect Biochemistry and Molecular Biology 42, 109–115.CrossRefGoogle ScholarPubMed
Tokuoka, A, Itoh, TQ, Hori, S, Uryu, O, Danbara, Y, Nose, M, Bando, T, Tanimura, T and Tomioka, K (2017) Cryptochrome genes form an oscillatory loop independent of the per/tim loop in the circadian clockwork of the cricket Gryllus bimaculatus. Zoological Letters 3, 5.CrossRefGoogle ScholarPubMed
Tomioka, K and Matsumoto, A (2015) Circadian molecular clockworks in non-model insects. Current Opinion in Insect Science 7, 58–64.CrossRefGoogle ScholarPubMed
Vogt, RG (2005) Molecular basis of pheromone detection in insects. In Gilbert, LI, Iatro, K and Gill, SS (eds), Life Sciences. London: Elsevier, pp. 753–804.Google Scholar
Wan, X, Qian, K and Du, Y (2015) Synthetic pheromones and plant volatiles alter the expression of chemosensory genes in Spodoptera exigua. Scientific Reports 5, 17320.CrossRefGoogle ScholarPubMed
Wang, X, Huang, Q, Hao, Q, Ran, S, Wu, Y, Cui, P, Yang, J, Jiang, C and Yang, Q (2018) Insecticide resistance and enhanced cytochrome P450 monooxygenase activity in field populations of Spodoptera litura from Sichuan, China. Crop Protection 106, 110–116.CrossRefGoogle Scholar
Xia, YH, Zhang, YN, Ding, BJ, Wang, HL and Lofstedt, C (2019) Multi-functional desaturases in two Spodoptera moths with 11 and 12 desaturation activities. Journal of Chemical Ecology 45, 378–387.CrossRefGoogle ScholarPubMed
Xu, L, Liang, H, Gan, LP, Wang, WD, Sima, YH and Xu, SQ (2011) Timeless is a critical gene in the diapause of silkworm, Bombyx mori. African Journal of Biotechnology 10, 16594–16601.Google Scholar
Zhang, J, Yan, S, Liu, Y, Jacquin-Joly, E, Dong, S and Wang, G (2015 a) Identification and functional characterization of sex pheromone receptors in the common cutworm (Spodoptera litura). Chemical Senses 40, 7–16.CrossRefGoogle Scholar
Zhang, YN, Zhu, XY, Fang, LP, He, P, Wang, ZQ, Chen, G, Sun, L, Ye, ZF, Deng, DG and Li, JB (2015 b) Identification and expression profiles of sex pheromone biosynthesis and transport related genes in Spodoptera litura. PLoS ONE 10, e0140019.CrossRefGoogle ScholarPubMed
Zhang, YN, Li, JB, He, P, Sun, L, Li, ZQ, Fang, LP, Ye, ZF, Deng, DG and Zhu, XY (2016) Molecular identification and expression patterns of carboxylesterase genes based on transcriptome analysis of the common cutworm, Spodoptera litura (Lepidoptera: Noctuidae). Journal of Asia-Pacific Entomology 19, 989–994.CrossRefGoogle Scholar
Zhang, YN, Zhang, XQ, Zhu, GH, Zheng, MY, Yan, Q, Zhu, XY, Xu, JW, Zhang, YY, He, P, Sun, L, Palli, SR, Zhang, LW and Dong, SL (2019) A Delta9 desaturase (SlitDes11) is associated with the biosynthesis of ester sex pheromone components in Spodoptera litura. Pesticide Biochemistry and Physiology 156, 152–159.CrossRefGoogle ScholarPubMed
Zhu, H, Sauman, I, Yuan, Q, Casselman, A, Emery-Le, M, Emery, P and Reppert, SM (2008) Cryptochromes define a novel circadian clock mechanism in monarch butterflies that may underlie sun compass navigation. PLoS Biology 6, e4.CrossRefGoogle ScholarPubMed
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