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Molecular characterisation and developmental expression analysis of the 5-HT7 receptor in Chrysopa formosa

Published online by Cambridge University Press:  18 March 2025

Fei Li
Affiliation:
Engineering Research Center of Natural Enemies, Jilin Province International Cooperation Key Laboratory for Biological Control of Agricultural Pests, Institute of Biological Control, Jilin Agricultural University, Changchun, PR China State Key Laboratory for Biology of Plant Diseases and Insect Pests, Key Laboratory of Natural Enemy Insects, Ministry of Agriculture and Rural Affairs, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, PR China
Longrui Wang
Affiliation:
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Key Laboratory of Natural Enemy Insects, Ministry of Agriculture and Rural Affairs, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, PR China
Yujia Li
Affiliation:
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Key Laboratory of Natural Enemy Insects, Ministry of Agriculture and Rural Affairs, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, PR China
Xuyang Tian
Affiliation:
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Key Laboratory of Natural Enemy Insects, Ministry of Agriculture and Rural Affairs, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, PR China
Jiayue Wang
Affiliation:
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Key Laboratory of Natural Enemy Insects, Ministry of Agriculture and Rural Affairs, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, PR China
Zhongjian Shen
Affiliation:
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Key Laboratory of Natural Enemy Insects, Ministry of Agriculture and Rural Affairs, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, PR China
Junjie Zhang*
Affiliation:
Engineering Research Center of Natural Enemies, Jilin Province International Cooperation Key Laboratory for Biological Control of Agricultural Pests, Institute of Biological Control, Jilin Agricultural University, Changchun, PR China
Lisheng Zhang
Affiliation:
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Key Laboratory of Natural Enemy Insects, Ministry of Agriculture and Rural Affairs, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, PR China Key Laboratory of Animal Biosafety Risk Prevention and Control (North) of Ministry of Agriculture and Rural Affairs, Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Shanghai, PR China
Yuyan Li*
Affiliation:
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Key Laboratory of Natural Enemy Insects, Ministry of Agriculture and Rural Affairs, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, PR China
*
Corresponding author: Yuyan Li; Email: [email protected]; Junjie Zhang; Email: [email protected]
Corresponding author: Yuyan Li; Email: [email protected]; Junjie Zhang; Email: [email protected]

Abstract

Serotonin (5-hydroxytryptamine, 5-HT) is a key monoamine neurotransmitter in insects, which regulates neural functions and influences various developmental and physiological processes by binding to its receptors. In this study, we investigate the molecular characteristics, phylogenetic relationships, and expression patterns of the 5-HT7 receptor (Cf5-HT7) in Chrysopa formosa, with a focus on its potential involvement in developmental and diapause regulation. The Cf5-HT7 gene was identified and cloned from the C. formosa transcriptome, revealing an open reading frame of 1788 bp encoding a 596 amino acid protein. Sequence analysis confirmed that Cf5-HT7 is a typical class A G protein-coupled receptor, characterised by seven transmembrane domains and several post-translational modifications, including palmitoylation and N-glycosylation sites. Phylogenetic analysis revealed that Cf5-HT7 is most closely related to the 5-HT7 receptor from Chrysoperla carnea, with high conservation of key motifs involved in ligand binding and receptor activation. Expression analysis across different developmental stages of C. formosa showed that Cf5-HT7 is highly expressed in the first instar larvae, with significant upregulation observed during the prepupal stage. Under diapause-inducing conditions, Cf5-HT7 expression is modulated in a stage-specific manner, showing a marked decrease at the onset of diapause, followed by a significant increase during the mid-to-late diapause maintenance phase. These findings suggest that it plays a pivotal role in regulating development and diapause processes in C. formosa, offering new insights into the molecular mechanisms governing insect life cycle transitions. This study lays the groundwork for future research into the functional roles of 5-HT7 receptors in insect physiology and their potential applications in manipulating diapause.

Type
Research Paper
Copyright
© The Author(s), 2025. Published by Cambridge University Press.

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References

Andreatta, G, Kyriacou, CP, Flatt, T and Costa, R (2018) Aminergic signaling controls ovarian dormancy in Drosophila. Scientific Reports 8, .CrossRefGoogle ScholarPubMed
Apeksha, S, Lathika, G, Nayana, G, Oishi, C, Praseeda, M and Kumar, MP (2018) The 5-Hydroxytryptamine signaling map: An overview of serotonin-serotonin receptor mediated signaling network. Journal of Cell Communication & Signaling 12, 731735.Google Scholar
Blenau, W, and Thamm, M (2011) Distribution of serotonin (5-HT) and its receptors in the insect brain with focus on the mushroom bodies: lessons from Drosophila melanogaster and Apis mellifera. Arthropod Structure & Development 40, 381394.CrossRefGoogle ScholarPubMed
Chen, WB, Gao, XY, Wang, HX, Xie, GY, An, SH, Du, YK, and Zhao, XC (2023) Identification and pharmacological characterization of two serotonin type 7 receptor isoforms from Mythimna separata. International Journal of Molecular Sciences 24, .Google Scholar
Dacks, AM, Dacks, JB, Christensen, TA and Nighorn, AJ (2006) The cloning of one putative octopamine receptor and two putative serotonin receptors from the Tobacco hawkmoth. Manduca Sexta. Insect Biochemistry and Molecular Biology 36, 741747.CrossRefGoogle ScholarPubMed
Dacks, AM, Reale, V, Pi, YL, Zhang, WJ, Dacks, JB, Nighorn, AJ and Evans, PD (2013) A characterization of the Manduca sexta serotonin receptors in the context of olfactory neuromodulation. PLoS One 8, .CrossRefGoogle ScholarPubMed
Denlinger, DL (2022a) Insect Diapause. Cambridge University Press: Cambridge.CrossRefGoogle ScholarPubMed
Denlinger, DL (2022b) Exploiting tools for manipulating insect diapause. Bulletin of Entomological Research 112, 715723.CrossRefGoogle ScholarPubMed
Duhr, F, Déléris, P, Raynaud, F, Séveno, M, Morisset-Lopez, S, Mannoury la Cour, C, Millan, MJ, Bockaert, J, Marin, P and Chaumont-Dubel, S (2014) Cdk5 induces constitutive activation of 5-HT6 receptors to promote neurite growth. Nature Chemical Biology 10, 590597.CrossRefGoogle ScholarPubMed
Falibene, A, Rssler, W, and Josens, R (2012) Serotonin depresses feeding behaviour in ants. Journal of Insect Physiology 58, 717.CrossRefGoogle ScholarPubMed
Fried, SDE, Hewage, KSK, Eitel, AR, Struts, AV, Weerasinghe, N, Perera, SMDC and Brown, MF (2022) Hydration-mediated G-protein–coupled receptor activation. Proceedings of the National Academy of Sciences 119, .CrossRefGoogle ScholarPubMed
Fritze, O, Filipek, S, Kuksa, V, Palczewski, K, Hofmann, KP and Ernst, OP (2003) Role of the conserved NPxxY(x)5,6F motif in the rhodopsin ground state and during activation. Proceedings of the National Academy of Sciences 100, 22902295.CrossRefGoogle ScholarPubMed
Ganguly, A, Qi, C, Bajaj, J and Lee, D (2020) Serotonin receptor 5-HT7 in Drosophila mushroom body neurons mediates larval appetitive olfactory learning. Scientific Reports 10, .CrossRefGoogle ScholarPubMed
Gasque, G, Conway, S, Huang, J, Rao, Y and Vosshall, LB (2013) Small molecule drug screening in Drosophila identifies the 5HT2A receptor as a feeding modulation target. Scientific Reports 3, .CrossRefGoogle ScholarPubMed
Hahn, DA and Denlinger, DL (2011) Energetics of insect diapause. Annual Review of Entomology 56, 103121.CrossRefGoogle ScholarPubMed
Huang, SJ, Xu, PY, Shen, DD, Simon, IA, Mao, CY, Tan, YX, Zhang, HB, Harpsøe, K, Li, HD, Zhang, YM, You, CZ, Yu, XK, Jiang, Y, Zhang, Y, Gloriam, DE and Xu, HE (2022) GPCRs steer G(i) and G(s) selectivity via TM5-TM6 switches as revealed by structures of serotonin receptors. Molecular Cell. 82, 26812695.CrossRefGoogle Scholar
Iglesias, A, Cimadevila, M, La Fuente, RAD, Martí-Solano, M, Cadavid, MI, Castro, M, Selent, J, Loza, MI and Brea, J (2017) Serotonin 2A receptor disulfide bridge integrity is crucial for ligand binding to different signalling states but not for its homodimerization. European Journal of Pharmacology 815, 138146.CrossRefGoogle Scholar
Isabel, G, Gourdoux, L, and Moreau, R (2001) Changes of biogenic amine levels in haemolymph during diapausing and non-diapausing status in Pieris brassicae L. Comparative Biochemistry and Physiology A: Molecular and Integrative Physiology 128, 117127.CrossRefGoogle ScholarPubMed
Kostal, V, Noguchi, H, Shimada, K, and Hayakawa, Y (1999) Dopamine and serotonin in the larval CNS of a drosophilid fly, Chymomyza costata: are they involved in the regulation of diapause? Archives of Insect Biochemistry and Physiology 42, 147162.3.0.CO;2-X>CrossRefGoogle ScholarPubMed
Li, MZ, Zhang, L, Wu, YC, Li, Y, Chen, X, Chen, J, Wang, QH, Liao, CH, and Han, Q (2022) Deletion of the serotonin receptor 7 gene changed the development and behavior of the mosquito, Aedes aegypti. Insects 13, .CrossRefGoogle ScholarPubMed
Li, YY, Wang, MZ, Gao, F, Zhang, HZ, Chen, HY, Wang, MQ, Liu, CX and Zhang, LS (2018) Exploiting diapause and cold tolerance to enhance the use of the green lacewing Chrysopa formosa for biological control. Biological Control 127, 116126.CrossRefGoogle Scholar
Li, YY, Wang, YN, Zhang, HZ, Zhang, MS, Wang, MQ, Mao, JJ and Zhang, LS (2023) The green lacewing Chrysopa formosa as a potential biocontrol agent for managing Spodoptera frugiperda and Spodoptera litura. Bulletin of Entomological Research 113, 4962.CrossRefGoogle ScholarPubMed
Liao, SF, Broughton, S and Nassel, DR (2017) Behavioral senescence and aging-related changes in motor neurons and brain neuromodulator levels are ameliorated by lifespan-extending reproductive dormancy in Drosophila. Frontiers in Cellular Neuroscience 11, .CrossRefGoogle ScholarPubMed
Ling, L, and Raikhel, AS (2018) Serotonin signaling regulates insulin-like peptides for growth, reproduction, and metabolism in the disease vector Aedes aegypti. Proceedings of the National Academy of Sciences 115, E9822E9831.CrossRefGoogle ScholarPubMed
Luo, JN, Becnel, J, Nichols, CD and Nssel, DR (2012) Insulin-producing cells in the brain of adult Drosophila are regulated by the serotonin 5-HT1A receptor. Cellular and Molecular Life Sciences 69, 471484.CrossRefGoogle ScholarPubMed
Matsumoto, M and Takeda, M (2002) Changes in brain monoamine contents in diapause pupae of Antheraea pernyi when activated under long-day and by chilling. Journal of Insect Physiology 48, 765771.CrossRefGoogle ScholarPubMed
Millan, MJ, Marin, P, Bockaert, J, and Cour, CML (2008) Signaling at G-protein-coupled serotonin receptors: recent advances and future research directions. Trends in Pharmacological Sciences. 29, 454464.CrossRefGoogle ScholarPubMed
Moncalvo, VGR and Campos, AR (2009) Role of serotonergic neurons in the Drosophila larval response to light. BioMedical Central Neuroscience 10, .Google Scholar
Movassaghi, CS and Milasincic, AA (2024) Call me serotonin. Nature Chemistry 16, 670670.CrossRefGoogle Scholar
Mykytyn K and Askwith C (2017) G-Protein-coupled receptor signaling in cilia. Cold Spring Harbor Perspectives in Biology 9, . doi:10.1101/cshperspect.a028183Google Scholar
Paluzzi, JP, Bhatt, G, Wang, CH, Zandawala, M, Lange, AB and Orchard, I (2015) Identification, functional characterization, and pharmacological profile of a serotonin type-2b receptor in the medically important insect, Rhodnius prolixus. Frontiers in Cellular Neuroscience 9, .Google ScholarPubMed
Patwardhan, A, Cheng, N and Trejo, J (2021) Post-translational modifications of G Protein-coupled receptors control cellular signaling dynamics in space and time. Pharmacological Reviews 73, 120151.CrossRefGoogle ScholarPubMed
Pietrantonio, PV, Jagge, C and Mcdowell, C (2001) Cloning and expression analysis of a 5HT7-like serotonin receptor cDNA from mosquito Aedes aegypti female excretory and respiratory systems. Insect Molecular Biology 10, 357369.CrossRefGoogle ScholarPubMed
Qi, YX, Xia, RY, Wu, YS, Stanley, D, Huang, J and Ye, GY (2014) Larvae of the small white butterfly, Pieris rapae, express a novel serotonin receptor. Journal of Neurochemistry 131, 767777.CrossRefGoogle ScholarPubMed
Rao, XJ, Zhan, MY, Pan, YM, Liu, S, Yang, PJ, Yang, LL and Yu, XQ (2017) Immune functions of insect βGRPs and their potential application. Developmental & Comparative Immunology 83, 8088.CrossRefGoogle ScholarPubMed
Röser, C, Jordan, N, Balfanz, S, Baumann, A, Walz, B, Baumann, O, and Blenau, W (2012) Molecular and pharmacological characterization of serotonin 5-HT2α and 5-HT7 receptors in the salivary glands of the blowfly Calliphora vicina. PLoS One 7, .CrossRefGoogle ScholarPubMed
Saifullah, ASM and Tomioka, K (2002) Serotonin sets the day state in the neurons that control coupling between the optic lobe circadian pacemakers in the cricket Gryllus bimaculatus. Journal of Experimental Biology 205, 13051314.CrossRefGoogle Scholar
Sato, T (2020) Serotonin signaling in the control of molting in Tenebrio molitor. Insect Biochemistry and Molecular Biology 122, .Google Scholar
Schlenstedt, J, Balfanz, S, Baumann, A, and Blenau, W (2006) Am5-HT7: molecular and pharmacological characterization of the first serotonin receptor of the honeybee (Apis mellifera). Journal of Neurochemistry 98, 19851998.CrossRefGoogle ScholarPubMed
Shimada-Niwa, Y and Niwa, R (2014) Serotonergic neurons respond to nutrients and regulate the timing of steroid hormone biosynthesis in Drosophila. Nature Communications 5, .CrossRefGoogle ScholarPubMed
Silva, B, Goles, NI, Varas, R, and Campusano, JM (2014) Serotonin receptors expressed in Drosophila mushroom bodies differentially modulate larval locomotion. PLoS One 9, .Google ScholarPubMed
Sitaraman, D, Laferriere, H, Birman, S and Zars, T (2012) Serotonin is critical for rewarded olfactory short-term memory in Drosophila. Journal of Neurogenetics 26, 238244.CrossRefGoogle ScholarPubMed
Sprouse, J, Reynolds, L, Li, XF, Braselton, J, and Schmidt, A (2004) 8-OH-DPAT as a 5-HT7 agonist: phase shifts of the circadian biological clock through increases in cAMP production. Neuropharmacology 46, 5262.CrossRefGoogle ScholarPubMed
Takeda, M, and Suzuki, T (2022) Circadian and neuroendocrine basis of photoperiodism controlling diapause in insects and mites: a review. Frontiers in Physiology 13, .CrossRefGoogle ScholarPubMed
Thamm, M, Balfanz, S, Scheiner, R, Baumann, A and Blenau, W (2010) Characterization of the 5-HT1A receptor of the honeybee (Apis mellifera) and involvement of serotonin in phototactic behavior. Cellular and Molecular Life Sciences 67, 24672479.CrossRefGoogle ScholarPubMed
Ullah, F, Abbas, A, Gul, H, Güncan, A, Hafeez, M, Gadratagi, BG, Ciceri, L, Ramirez-Romero, R, Desneux, N, and Li, ZH (2024) Insect resilience: unraveling responses and adaptations to cold temperatures. Journal of Pest Science 97, 11531169.CrossRefGoogle Scholar
Van Bortle, K, Peterson, AJ, Takenaka, N, O’Connor, MB and Corces, VG (2015) CTCF-dependent co-localization of canonical Smad signaling factors at architectural protein binding sites in D. melanogaster. Cell. Cycle 14, 26772687.CrossRefGoogle Scholar
Veenstra, JA (2017) The salivary gland salivation stimulating peptide from Locusta migratoria (Lom-SG-SASP) is not a typical neuropeptide. PeerJ 5, .CrossRefGoogle Scholar
Venkatakrishnan, AJ, Deupi, X, Lebon, G, Tate, CG, Schertler, GF and Babu, MM (2013) Molecular signatures of G-protein-coupled receptors. Nature 494, 185194.CrossRefGoogle ScholarPubMed
Venkatakrishnan, AJ, Flock, T, Prado, DE, Oates, ME, Gough, J and Babu, MM (2014) Structured and disordered facets of the GPCR fold. Current Opinion in Structural Biology 27, 129137.CrossRefGoogle ScholarPubMed
Vesala, L, Salminen, TS, Laiho, A, Hoikkala, A and Kankare, M (2012) Cold tolerance and cold-induced modulation of gene expression in two Drosophila virilis group species with different distributions. Insect Molecular Biology 21, 107118.CrossRefGoogle ScholarPubMed
Vleugels, R, Lenaerts, C, Broeck, JV and Verlinden, H (2014) Signalling properties and pharmacology of a 5-HT7-type serotonin receptor from Tribolium castaneum. Insect Molecular Biology 23, 230243.CrossRefGoogle ScholarPubMed
Vleugels, R, Verlinden, H and Broeck, JV (2015) Serotonin, serotonin receptors and their actions in insects. Neurotransmitter 2, .Google Scholar
Vuorio, J, Škerlová, J, Fábry, M, Veverka, V, Vattulainen, I, Řezáčová, P and Martinez-Seara, H (2021) N-Glycosylation can selectively block or foster different receptor-ligand binding modes. Scientific Reports 11, .CrossRefGoogle ScholarPubMed
Wang, QS, Mohamed, AMM, and 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, .Google ScholarPubMed
Wang, YY, Chen, Y, Zhang, AL, Chen, KQ and Ouyang, P (2023) Advances in the microbial synthesis of the neurotransmitter serotonin. Applied Microbiology and Biotechnology 107, 47174725.CrossRefGoogle ScholarPubMed
Watanabe, T, Sadamoto, H and Aonuma, H (2011) Identification and expression analysis of the genes involved in serotonin biosynthesis and transduction in the field cricket Gryllus bimaculatus. Insect Molecular Biology 20, 619635.CrossRefGoogle ScholarPubMed
Witz, P, Amlaiky, N, Plassat, JL, Maroteaux, L, Borrelli, E and Hen, R (1990) Cloning and characterization of a Drosophila serotonin receptor that activates adenylate cyclase. Proceedings of the National Academy of Sciences 87, 89408944.CrossRefGoogle ScholarPubMed
Wu, K, Yang, B, Chen, RB, Majeed, R, Li, BL, Gong, LY, Wei, XF, Yang, JF, Tang, YY, Wang, AB, Toufeeq, S, Shaik, HA, Huang, WR, Guo, X and Ling, EJ (2024) Lack of signal peptide in insect prophenoloxidase to avoid glycosylation to damage the zymogen activity. Developmental & Comparative Immunology 160, .CrossRefGoogle ScholarPubMed
Yang, S, Xi, GS and Wang, GR (2019) Molecular cloning and expression analysis of 5-hydroxytryptamine receptor 7 in ant Polyrhachis vicina Roger (Hymenoptera: Formicidae). Journal of Insect Science 19(2), 19.CrossRefGoogle ScholarPubMed
Zeng, T, Su, HA, Liu, YL, Li, JF, Jiang, DX, Lu, YY and Qi, YX (2022) Serotonin modulates insect gut bacterial community homeostasis. BioMedical Central Biology 20, .Google ScholarPubMed
Zhang, QQ, Chang, YF, Zheng, CY and Sun, LJ (2023) Identification and expression profiling of the 5-HT receptor gene in Harmonia axyridis. Insects 14, .CrossRefGoogle ScholarPubMed
Zhao, WL, Wang, D, Liu, CY and Zhao, XF (2016) G-protein-coupled receptor kinase 2 terminates G-protein-coupled receptor function in steroid hormone 20-hydroxyecdysone signaling. Scientific Reports 6, .Google ScholarPubMed