Juvenile hormone suppresses aggregation behavior through influencing antennal gene expression in locusts

Autoři: Wei Guo aff001;  Juan Song aff001;  Pengcheng Yang aff003;  Xiangyong Chen aff001;  Dafeng Chen aff001;  Dani Ren aff001;  Le Kang aff001;  Xianhui Wang aff001
Působiště autorů: State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China aff001;  CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing, China aff002;  Beijing Institutes of Life Science, Chinese Academy of Sciences, Beijing, China aff003
Vyšlo v časopise: Juvenile hormone suppresses aggregation behavior through influencing antennal gene expression in locusts. PLoS Genet 16(4): e32767. doi:10.1371/journal.pgen.1008762
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008762


Animals often exhibit dramatically behavioral plasticity depending on their internal physiological state, yet little is known about the underlying molecular mechanisms. The migratory locust, Locusta migratoria, provides an excellent model for addressing these questions because of their famous phase polyphenism involving remarkably behavioral plasticity between gregarious and solitarious phases. Here, we report that a major insect hormone, juvenile hormone, is involved in the regulation of this behavioral plasticity related to phase change by influencing the expression levels of olfactory-related genes in the migratory locust. We found that the treatment of juvenile hormone analog, methoprene, can significantly shift the olfactory responses of gregarious nymphs from attraction to repulsion to the volatiles released by gregarious nymphs. In contrast, the repulsion behavior of solitarious nymphs significantly decreased when they were treated with precocene or injected with double-stranded RNA of JHAMT, a juvenile hormone acid O-methyltransferase. Further, JH receptor Met or JH-response gene Kr-h1 knockdown phenocopied the JH-deprivation effects on olfactory behavior. RNA-seq analysis identified 122 differentially expressed genes in antennae after methoprene application on gregarious nymphs. Interestingly, several olfactory-related genes were especially enriched, including takeout (TO) and chemosensory protein (CSP) which have key roles in behavioral phase change of locusts. Furthermore, methoprene application and Met or Kr-h1 knockdown resulted in simultaneous changes of both TO1 and CSP3 expression to reverse pattern, which mediated the transition between repulsion and attraction responses to gregarious volatiles. Our results suggest the regulatory roles of a pleiotropic hormone in locust behavioral plasticity through modulating gene expression in the peripheral olfactory system.

Klíčová slova:

Acetones – Animal antennae – Animal behavior – Decision making – Gene expression – Gene regulation – Locusts – Nymphs


1. Hamilton AR, Shpigler H, Bloch G, Wheeler DE, Robinson GE. Endocrine influences on insect societies. In: Joëls M, editor. Hormones, Brain and Behavior (Third Edition). Oxford: Academic Press; 2017. p. 421–51.

2. Korb J. Juvenile hormone: a central regulator of termite caste polyphenism. Adv Insect Physiol. 2015;48:131–61.

3. Kou R, Chang HW, Chen SC, Ho HY. Suppression pheromone and cockroach rank formation. Naturwissenschaften. 2009;96(6):691–701. doi: 10.1007/s00114-009-0522-0 19280169.

4. Wheeler MM, Ament SA, Rodriguez-Zas SL, Southey B, Robinson GE. Diet and endocrine effects on behavioral maturation-related gene expression in the pars intercerebralis of the honey bee brain. J Exp Biol. 2015;218(Pt 24):4005–14. doi: 10.1242/jeb.119420 26567353.

5. Wang Y, Brent CS, Fennern E, Amdam GV. Gustatory perception and fat body energy metabolism are jointly affected by vitellogenin and juvenile hormone in honey bees. Plos Genet. 2012;8(6). doi: 10.1371/journal.pgen.1002779 22761585.

6. Wang XH, Kang L. Molecular mechanisms of phase change in locusts. Annu Rev Entomol. 2014;59:225–44. doi: 10.1146/annurev-ento-011613-162019 24160426.

7. Pener MP, Simpson SJ. Locust phase polyphenism: an update. Adv Insect Physiol. 2009;36:1–272.

8. Pener MP. Locust phase polymorphism and its endocrine relations. Adv Insect Physiol. 1991;23(1):79.

9. Wei J, Shao W, Cao M, Ge J, Yang P, Chen L, et al. Phenylacetonitrile in locusts facilitates an antipredator defense by acting as an olfactory aposematic signal and cyanide precursor. Sci Adv. 2019;5(1):eaav5495. doi: 10.1126/sciadv.aav5495 30746481

10. Guo X, Ma Z, Du B, Li T, Li W, Xu L, et al. Dop1 enhances conspecific olfactory attraction by inhibiting miR-9a maturation in locusts. Nat Commun. 2018;9(1):1193. doi: 10.1038/s41467-018-03437-z 29567955.

11. Wei J, Shao W, Wang X, Ge J, Chen X, Yu D, et al. Composition and emission dynamics of migratory locust volatiles in response to changes in developmental stages and population density. Insect Sci. 2017;24(1):60–72. doi: 10.1111/1744-7917.12396 27554189.

12. Li Y, Zhang J, Chen D, Yang P, Jiang F, Wang X, et al. CRISPR/Cas9 in locusts: successful establishment of an olfactory deficiency line by targeting the mutagenesis of an odorant receptor co-receptor (Orco). Insect Biochem Mol Biol. 2016;79:27–35. doi: 10.1016/j.ibmb.2016.10.003 27744049.

13. Wang Z, Yang P, Chen D, Jiang F, Li Y, Wang X, et al. Identification and functional analysis of olfactory receptor family reveal unusual characteristics of the olfactory system in the migratory locust. Cell Mol Life Sci. 2015;72(22):4429–43. doi: 10.1007/s00018-015-2009-9 26265180.

14. Ma Z, Guo X, Lei H, Li T, Hao S, Kang L. Octopamine and tyramine respectively regulate attractive and repulsive behavior in locust phase changes. Sci Rep. 2015;5:8036. doi: 10.1038/srep08036 25623394.

15. Guo W, Wang X, Ma Z, Xue L, Han J, Yu D, et al. CSP and takeout genes modulate the switch between attraction and repulsion during behavioral phase change in the migratory locust. Plos Genet. 2011;7(2):e1001291. doi: 10.1371/journal.pgen.1001291 21304893.

16. Guo X, Ma Z, Kang L. Two dopamine receptors play different roles in phase change of the migratory locust. Front Behav Neuros. 2015;9:80. doi: 10.3389/fnbeh.2015.00080 25873872.

17. Ma Z, Guo W, Guo X, Wang X, Kang L. Modulation of behavioral phase changes of the migratory locust by the catecholamine metabolic pathway. P Natl Acad Sci USA. 2011;108(10):3882–7. doi: 10.1073/pnas.1015098108 21325054.

18. Ochieng SA, Hansson BS. Responses of olfactory receptor neurones to behaviourally important odours in gregarious and solitarious desert locust, Schistocerca gregaria. Physiol Entomol. 1999;24:28–36.

19. Applebaum SW, Avisar E, Heifetz Y. Juvenile hormone and locust phase. Arch Insect Biochem Physiol. 1997;35(4):375–91.

20. Kang L, Chen XY, Zhou Y, Liu BW, Zheng W, Li RQ, et al. The analysis of large-scale gene expression correlated to the phase changes of the migratory locust. P Natl Acad Sci USA. 2004;101(51):17611–5. doi: 10.1073/pnas.0407753101 15591108.

21. Tawfik AI, Treiblmayr K, Hassanali A, Osir EO. Time-course haemolymph juvenile hormone titres in solitarious and gregarious adults of Schistocerca gregaria, and their relation to pheromone emission, CA volumetric changes and oocyte growth. J Insect Physiol. 2000;46(7):1143–50. doi: 10.1016/s0022-1910(99)00225-5 10817841.

22. Tawfik AI, Osir EO, Hassanali A, Ismail SH. Effects of juvenile hormone treatment on phase changes and pheromone production in the desert locust, Schistocerca gregaria (Forskal) (Orthoptera: Acrididae). J Insect Physiol. 1997;43(12):1177–82. doi: 10.1016/s0022-1910(97)00079-6 12770490.

23. Anton S, Dufour MC, Gadenne C. Plasticity of olfactory-guided behaviour and its neurobiological basis: lessons from moths and locusts. Entomol Exp Appl. 2007;123(1):1–11.

24. Wiesel G, Tappermann S, Dorn A. Effects of juvenile hormone and juvenile hormone analogues on the phase behaviour of Schistocerca gregaria and Locusta migratoria. J Insect Physiol. 1996;42(4):385–95.

25. Marchal E, Zhang J, Badisco L, Verlinden H, Hult EF, Van Wielendaele P, et al. Final steps in juvenile hormone biosynthesis in the desert locust, Schistocerca gregaria. Insect Biochem Mol Biol. 2011;41(4):219–27. doi: 10.1016/j.ibmb.2010.12.007 21195178.

26. Ojani R, Fu X, Ahmed T, Liu P, Zhu J. Kruppel homologue 1 acts as a repressor and an activator in the transcriptional response to juvenile hormone in adult mosquitoes. Insect Mol Biol. 2018;27(2):268–78. doi: 10.1111/imb.12370 29314423.

27. Ignell R, Couillaud F, Anton S. Juvenile-hormone-mediated plasticity of aggregation behaviour and olfactory processing in adult desert locusts. J Exp Biol. 2001;204(Pt 2):249–59.11136611.

28. Bowen MF. The sensory physiology of host-seeking behavior in mosquitoes. Annu Rev Entomol. 1991;36:139–58. doi: 10.1146/annurev.en.36.010191.001035 1672499.

29. Gadenne C, Renou M, Sreng L. Hormonal control of pheromone responsiveness in the male black cutworm Agrotis ipsilon. Experientia. 1993;49(8):721–4.

30. Sullivan JP, Fahrbach SE, Robinson GE. Juvenile hormone paces behavioral development in the adult worker honey bee. Horm Behav. 2000;37(1):1–14. doi: 10.1006/hbeh.1999.1552 10712853.

31. Lin HH, Cao DS, Sethi S, Zeng Z, Chin JSR, Chakraborty TS, et al. Hormonal modulation of pheromone detection enhances male courtship success. Neuron. 2016;90(6):1272–85. doi: 10.1016/j.neuron.2016.05.004 27263969.

32. Kamita SG, Hammock BD. Juvenile hormone esterase: biochemistry and structure. J Pest Sci. 2010;35(3):265–74. doi: 10.1584/jpestics.R10-09 23543805.

33. Guittard E, Blais C, Maria A, Parvy JP, Pasricha S, Lumb C, et al. CYP18A1, a key enzyme of Drosophila steroid hormone inactivation, is essential for metamorphosis. Dev Biol. 2011;349(1):35–45. doi: 10.1016/j.ydbio.2010.09.023 20932968.

34. Gadenne C, Barrozo RB, Anton S. Plasticity in insect olfaction: to smell or not to smell? Annu Rev Entomol. 2016;61:317–33. doi: 10.1146/annurev-ento-010715-023523 26982441.

35. Lin X, Zhang L, Jiang Y. Distinct roles of Met and interacting proteins on the expressions of takeout family genes in brown planthopper. Front Physiol. 2017;8:100. doi: 10.3389/fphys.2017.00100 28270774.

36. Du J, Hiruma K, Riddiford LM. A novel gene in the takeout gene family is regulated by hormones and nutrients in Manduca larval epidermis. Insect Biochem Mol Biol. 2003;33(8):803–14. doi: 10.1016/s0965-1748(03)00079-1 12878227.

37. Schwinghammer MA, Zhou X, Kambhampati S, Bennett GW, Scharf ME. A novel gene from the takeout family involved in termite trail-following behavior. Gene. 2011;474(1–2):12–21. doi: 10.1016/j.gene.2010.11.012 21134424.

38. Hagai T, Cohen M, Bloch G. Genes encoding putative takeout/juvenile hormone binding proteins in the honeybee (Apis mellifera) and modulation by age and juvenile hormone of the takeout-like gene GB19811. Insect Biochem Mol Biol. 2007;37(7):689–701. doi: 10.1016/j.ibmb.2007.04.002 17550825.

39. Jordan MD, Stanley D, Marshall SDG, De Silva D, Crowhurst RN, Gleave AP, et al. Locust phase polyphenism: an update. Insect Mol Biol. 2008;17(4):361–73. doi: 10.1111/j.1365-2583.2008.00812.x 18651918

40. Fujikawa K, Seno K, Ozaki M. A novel takeout-like protein expressed in the taste and olfactory organs of the blowfly, Phormia regina. FASEB J. 2006;273(18):4311–21. doi: 10.1111/j.1742-4658.2006.05422.x 16930135.

41. Guo W, Wu Z, Song J, Jiang F, Wang Z, Deng S, et al. Juvenile hormone-receptor complex acts on mcm4 and mcm7 to promote polyploidy and vitellogenesis in the migratory locust. Plos Genet. 2014;10:e1004702. doi: 10.1371/journal.pgen.1004702 25340846.

42. Jindra M, Palli SR, Riddiford LM. The juvenile hormone signaling pathway in insect development. Annu Rev Entomol. 2013;58(1):181–204. doi: 10.1146/annurev-ento-120811-153700 22994547.

43. Riddiford LM. How does juvenile hormone control insect metamorphosis and reproduction? Gen Comp Endocr. 2012;179(3):477–84. doi: 10.1016/j.ygcen.2012.06.001 22728566.

44. Wang XH, Fang XD, Yang PC, Jiang XT, Jiang F, Zhao DJ, et al. The locust genome provides insight into swarm formation and long-distance flight. Nat Commun. 2014;5:1–9. doi: 10.1038/ncomms3957 24423660.

45. Lemmen J, Evenden M. Peripheral and behavioral plasticity of pheromone response and its hormonal control in a long-lived moth. J Exp Biol. 2009;212(Pt 13):2000–6. doi: 10.1242/jeb.030858 19525425.

46. Hancock RG, Foster WA. Exogenous juvenile hormone and methoprene, but not male accessory gland substances or ovariectomy, affect the blood/nectar choice of female Culex nigripalpus mosquitoes. Med Vet Entomol. 2000;14(4):376–82. doi: 10.1046/j.1365-2915.2000.00253.x 11129701.

47. Hartfelder K. Insect juvenile hormone: from "status quo" to high society. Braz J Med Biol Res. 2000;33(2):157–77. doi: 10.1590/s0100-879x2000000200003 10657056.

48. Strambi C, Cayre M, Strambi A. Neural plasticity in the adult insect brain and its hormonal control. Int Rev Cytol. 1999;190:137–74.

49. Ma Z, Guo X, Kang L. Octopamine and tyramine signaling in locusts: relevance to olfactory decision-making. In: Farooqui AA, editor. Trace Amines and Neurological Disorders. San Diego: Academic Press; 2016. p. 221–33.

50. Guo X, Ma Z, Kang L. Serotonin enhances solitariness in phase transition of the migratory locust. Front Behav Neurosci. 2013;7:129. doi: 10.3389/fnbeh.2013.00129 24109441.

51. Guo W, Wu Z, Yang L, Cai Z, Zhao L, Zhou S. Juvenile hormone-dependent Kazal-type serine protease inhibitor Greglin safeguards insect vitellogenesis and egg production. FASEB J. 2019;33(1):917–27. doi: 10.1096/fj.201801068R 30063437.

52. Jiang F, Liu Q, Liu X, Wang XH, Kang L. Genomic data reveal high conservation but divergent evolutionary pattern of Polycomb/Trithorax group genes in arthropods. Insect Sci. 2019;26(1):20–34. doi: 10.1111/1744-7917.12558 29127737.

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