Capsaicin Functions as Drosophila Ovipositional Repellent and Causes Intestinal Dysplasia.
Animals
Behavior, Animal
/ drug effects
Capsaicin
/ pharmacology
Capsicum
/ chemistry
Digestive System Diseases
/ chemically induced
Drosophila
/ drug effects
Drosophila Proteins
/ metabolism
Female
Insect Repellents
/ pharmacology
Intestines
/ drug effects
Ion Channels
/ metabolism
Neurons
/ drug effects
Oviposition
/ drug effects
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
19 06 2020
19 06 2020
Historique:
received:
12
02
2020
accepted:
28
05
2020
entrez:
21
6
2020
pubmed:
21
6
2020
medline:
15
12
2020
Statut:
epublish
Résumé
Plants generate a plethora of secondary compounds (toxins) that potently influence the breadth of the breeding niches of animals, including Drosophila. Capsaicin is an alkaloid irritant from hot chili peppers, and can act as a deterrent to affect animal behaviors, such as egg laying choice. However, the mechanism underlying this ovipositional avoidance remains unknown. Here, we report that Drosophila females exhibit a robust ovipositional aversion to capsaicin. First, we found that females were robustly repelled from laying eggs on capsaicin-containing sites. Second, genetic manipulations show that the ovipositional aversion to capsaicin is mediated by activation of nociceptive neurons expressing the painless gene. Finally, we found that capsaicin compromised the health and lifespan of flies through intestinal dysplasia and oxidative innate immunity. Overall, our study suggests that egg-laying sensation converts capsaicin into an aversive behavior for female Drosophila, mirroring an adaptation to facilitate the survival and fitness of both parents and offspring.
Identifiants
pubmed: 32561812
doi: 10.1038/s41598-020-66900-2
pii: 10.1038/s41598-020-66900-2
pmc: PMC7305228
doi:
Substances chimiques
Drosophila Proteins
0
Insect Repellents
0
Ion Channels
0
pain protein, Drosophila
0
Capsaicin
S07O44R1ZM
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
9963Références
Sandi, C. & Haller, J. Stress and the social brain: behavioural effects and neurobiological mechanisms. Nature Reviews Neuroscience 16, 290–304, https://doi.org/10.1038/nrn3918 (2015).
doi: 10.1038/nrn3918
pubmed: 25891510
McCarty, M. F., DiNicolantonio, J. J. & O’Keefe, J. H. Capsaicin may have important potential for promoting vascular and metabolic health: Table 1. Open Heart 2, https://doi.org/10.1136/openhrt-2015-000262 (2015).
Caterina, M. J. & Schumacher, M. A. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389, 816–824, https://doi.org/10.1038/39807 (1997).
doi: 10.1038/39807
pubmed: 9349813
Al-Anzi, B., Tracey, W. D. Jr. & Benzer, S. Response of Drosophila to wasabi is mediated by painless, the fly homolog of mammalian TRPA1/ANKTM1. Curr Biol 16, 1034–1040, https://doi.org/10.1016/j.cub.2006.04.002 (2006).
doi: 10.1016/j.cub.2006.04.002
pubmed: 16647259
Antonious, G. F., Meyer, J. E. & Snyder, J. C. Toxicity and repellency of hot pepper extracts to spider mite, Tetranychus urticae Koch. J Environ Sci Health B 41, 1383–1391, https://doi.org/10.1080/0360123060096419 (2006).
doi: 10.1080/0360123060096419
pubmed: 17090499
Cowles, R. S., Keller, J. E. & Miller, J. R. Pungent spices, ground red pepper, and synthetic capsaicin as onion fly ovipositional deterrents. Journal of Chemical Ecology 15, 719–730, https://doi.org/10.1007/BF01014714 (1989).
doi: 10.1007/BF01014714
pubmed: 24271812
Lale, N. E. S. Oviposition-deterrent and repellent effects of products from dry chilli pepper fruits, Capsicum species on Callosobruchus maculatus. Postharcest Biology and Technology 1, 343–348, https://doi.org/10.1016/0925-5214(92)90036-O (1992).
doi: 10.1016/0925-5214(92)90036-O
Olszewska, J. & Tegowska, E. Opposite effect of capsaicin and capsazepine on behavioral thermoregulation in insects. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 197, 1021–1026, https://doi.org/10.1007/s00359-011-0657-2 (2011).
doi: 10.1007/s00359-011-0657-2
pubmed: 21667066
pmcid: 3176404
Spurr, E. B. & Mcgregor, P. G. Potential invertebrate antifeedants for toxic baits used for vertebrate pest control: A literature review. Science for Conservation (2003).
Liu, W. et al. Enterococci Mediate the Oviposition Preference of Drosophila melanogaster through Sucrose Catabolism. Sci Rep 7, 13420, https://doi.org/10.1038/s41598-017-13705-5 (2017).
doi: 10.1038/s41598-017-13705-5
pubmed: 29044155
pmcid: 5647369
Yang, C. H., Belawat, P., Hafen, E., Jan, L. Y. & Jan, Y. N. Drosophila Egg-Laying Site Selection as a System to Study Simple Decision-Making Processes. Science 319, 1679–1683, https://doi.org/10.1126/science.1151842 (2008).
doi: 10.1126/science.1151842
pubmed: 18356529
pmcid: 2581776
Su, W., Liu, J., Bai, P., Ma, B. & Liu, W. Pathogenic fungi-induced susceptibility is mitigated by mutual Lactobacillus plantarum in the Drosophila melanogaster model. BMC Microbiol 19, 302, https://doi.org/10.1186/s12866-019-1686-1 (2019).
doi: 10.1186/s12866-019-1686-1
pubmed: 31864308
pmcid: 6925846
Stensmyr, M. C. et al. A conserved dedicated olfactory circuit for detecting harmful microbes in Drosophila. Cell 151, 1345–1357, https://doi.org/10.1016/j.cell.2012.09.046 (2012).
doi: 10.1016/j.cell.2012.09.046
pubmed: 23217715
Dweck, H. K. et al. Olfactory preference for egg laying on citrus substrates in Drosophila. Curr Biol 23, 2472–2480, https://doi.org/10.1016/j.cub.2013.10.047 (2013).
doi: 10.1016/j.cub.2013.10.047
pubmed: 24316206
Wang, X., Li, G., Liu, J., Liu, J. & Xu, X. Z. TMC-1 Mediates Alkaline Sensation in C. elegans through Nociceptive Neurons. Neuron 91, 146–154, https://doi.org/10.1016/j.neuron.2016.05.023 (2016).
doi: 10.1016/j.neuron.2016.05.023
pubmed: 27321925
pmcid: 4938749
Lemaitre, B. & Miguel-Aliaga, I. The digestive tract of Drosophila melanogaster. Annu Rev Genet 47, 377–404, https://doi.org/10.1146/annurev-genet-111212-133343 (2013).
doi: 10.1146/annurev-genet-111212-133343
pubmed: 24016187
Miguel-Aliaga, I., Jasper, H. & Lemaitre, B. Anatomy and Physiology of the Digestive Tract of Drosophila melanogaster. Genetics 210, 357–396, https://doi.org/10.1534/genetics.118.300224 (2018).
doi: 10.1534/genetics.118.300224
pubmed: 30287514
pmcid: 6216580
Rera, M., Clark, R. I. & Walker, D. W. Intestinal barrier dysfunction links metabolic and inflammatory markers of aging to death in Drosophila. Proc Natl Acad Sci USA 109, 21528–21533, https://doi.org/10.1073/pnas.1215849110 (2012).
doi: 10.1073/pnas.1215849110
pubmed: 23236133
Wei, G. et al. Insect pathogenic fungus interacts with the gut microbiota to accelerate mosquito mortality. Proc Natl Acad Sci USA 114, 5994–5999, https://doi.org/10.1073/pnas.1703546114 (2017).
doi: 10.1073/pnas.1703546114
pubmed: 28533370
Xiao, X. et al. A Mesh-Duox pathway regulates homeostasis in the insect gut. Nat Microbiol 2, 17020, https://doi.org/10.1038/nmicrobiol.2017.20 (2017).
doi: 10.1038/nmicrobiol.2017.20
pubmed: 28248301
pmcid: 5332881
Joseph, R. M., Devineni, A. V., King, I. F. G. & Heberlein, U. Oviposition preference for and positional avoidance of acetic acid provide a model for competing behavioral drives in Drosophila. PNAS 106, 11352–11357, https://doi.org/10.1073/pnas.0901419106 (2009).
doi: 10.1073/pnas.0901419106
pubmed: 19541615
Karageorgi, M. et al. Evolution of Multiple Sensory Systems Drives Novel Egg-Laying Behavior in the Fruit Pest Drosophila suzukii. Curr Biol 27, 847–853, https://doi.org/10.1016/j.cub.2017.01.055 (2017).
doi: 10.1016/j.cub.2017.01.055
pubmed: 28285999
pmcid: 5364372
Solar, E. D., Guijón, A. M. & Walker, L. Choice of Colored Substrates for Oviposition inDrosophila Melanogaster. Bolletino di zoologia 41, 253–260, https://doi.org/10.1080/11250007409430120 (2009).
doi: 10.1080/11250007409430120
Amrein, H. & Thorne, N. Gustatory perception and behavior in Drosophila melanogaster. Curr Biol 15, R673–684, https://doi.org/10.1016/j.cub.2005.08.021 (2005).
doi: 10.1016/j.cub.2005.08.021
pubmed: 16139201
Jordt, S. E. & Julius, D. Molecular Basis for Species-Specific Sensitivity to “Hot” Chili Peppers. Cell 108, 421–430, https://doi.org/10.1016/s0092-8674(02)00637-2 (2002).
doi: 10.1016/s0092-8674(02)00637-2
pubmed: 11853675
Bandell, M. et al. Noxious Cold Ion Channel TRPA1 Is Activated by Pungent Compounds and Bradykinin. Neuron 41, 849–857 (2004).
doi: 10.1016/S0896-6273(04)00150-3
Clark, R. I. et al. Distinct Shifts in Microbiota Composition during Drosophila Aging Impair Intestinal Function and Drive Mortality. Cell Rep 12, 1656–1667, https://doi.org/10.1016/j.celrep.2015.08.004 (2015).
doi: 10.1016/j.celrep.2015.08.004
pubmed: 26321641
pmcid: 26321641
Liu, W., Jiang, F., Bi, X. & Zhang, Y. Q. Drosophila FMRP participates in the DNA damage response by regulating G2/M cell cycle checkpoint and apoptosis. Hum Mol Genet 21, 4655–4668, https://doi.org/10.1093/hmg/dds307 (2012).
doi: 10.1093/hmg/dds307
pubmed: 22843500
Buchon, N., Silverman, N. & Cherry, S. Immunity in Drosophila melanogaster–from microbial recognition to whole-organism physiology. Nat Rev Immunol 14, 796–810, https://doi.org/10.1038/nri3763 (2014).
doi: 10.1038/nri3763
pubmed: 6190593
pmcid: 6190593
Ibáñez-Álamo, J. D. & Soler, M. Male and female Blackbirds (Turdus merula) respond similarly to the risk of nest predation. Journal of Ornithology 158, 533–539, https://doi.org/10.1007/s10336-016-1403-x (2016).
doi: 10.1007/s10336-016-1403-x
Aranha, M. M. & Vasconcelos, M. L. Deciphering Drosophila female innate behaviors. Curr Opin Neurobiol 52, 139–148, https://doi.org/10.1016/j.conb.2018.06.005 (2018).
doi: 10.1016/j.conb.2018.06.005
pubmed: 29940518
Richmond, R. C. & Gerking, J. L. Oviposition site preference in Drosophila. Behavior Genetics 9, 233–241, https://doi.org/10.1007/BF01071304 (1979).
doi: 10.1007/BF01071304
pubmed: 115458
Caterina, M. J. et al. Impaired Nociception and Pain Sensation in Mice Lacking the Capsaicin Receptor. Science 288, 306–313, https://doi.org/10.1126/science.288.5464.306 (2000).
doi: 10.1126/science.288.5464.306
pubmed: 10764638
Baliki, M. N. & Apkarian, A. V. Nociception, Pain, Negative Moods, and Behavior Selection. Neuron 87, 474–491, https://doi.org/10.1016/j.neuron.2015.06.005 (2015).
doi: 10.1016/j.neuron.2015.06.005
pubmed: 26247858
pmcid: 26247858
Biteau, B., Hochmuth, C. E. & Jasper, H. JNK activity in somatic stem cells causes loss of tissue homeostasis in the aging Drosophila gut. Cell Stem Cell 3, 442–455, https://doi.org/10.1016/j.stem.2008.07.024 (2008).
doi: 10.1016/j.stem.2008.07.024
pubmed: 18940735
pmcid: 3225008
Khan, S. J., Abidi, S. N. F., Skinner, A., Tian, Y. & Smith-Bolton, R. K. The Drosophila Duox maturation factor is a key component of a positive feedback loop that sustains regeneration signaling. PLoS Genet 13, e1006937, https://doi.org/10.1371/journal.pgen.1006937 (2017).
doi: 10.1371/journal.pgen.1006937
pubmed: 28753614
pmcid: 5550008
Wu, S. C., Cao, Z. S., Chang, K. M. & Juang, J. L. Intestinal microbial dysbiosis aggravates the progression of Alzheimer’s disease in Drosophila. Nat Commun 8, 24, https://doi.org/10.1038/s41467-017-00040-6 (2017).
doi: 10.1038/s41467-017-00040-6
pubmed: 28634323
pmcid: 5478647
Qi, X. J., Pang, X., Cao, J. Q. & Du, S. S. Comparative analysis on bioactivity against three stored insects of Ligusticum pteridophyllum Franch. rhizomes essential oil and supercritical fluid (SFE-CO2) extract. Environ Sci Pollut Res Int 27, 15584–15591, https://doi.org/10.1007/s11356-020-08043-5 (2020).
doi: 10.1007/s11356-020-08043-5
pubmed: 32078128
Pan, J. C. Research on the function of rgn gene in Drosophila gut and innate immunity Doctor thesis, Northeast forestry university (2014).
Madabattula, S. T. et al. Quantitative Analysis of Climbing Defects in a Drosophila Model of Neurodegenerative Disorders. J Vis Exp, e52741, https://doi.org/10.3791/52741 (2015).
Choi, N. H., Kim, J. G., Yang, D. J., Kim, Y. S. & Yoo, M. A. Age-related changes in Drosophila midgut are associated with PVF2, a PDGF/VEGF-like growth factor. Aging Cell 7, 318–334, https://doi.org/10.1111/j.1474-9726.2008.00380.x (2008).
doi: 10.1111/j.1474-9726.2008.00380.x
pubmed: 18284659
pmcid: 2408640
Zhou, J., Edgar, B. A. & Boutros, M. ATF3 acts as a rheostat to control JNK signalling during intestinal regeneration. Nat Commun 8, 14289, https://doi.org/10.1038/ncomms14289 (2017).
doi: 10.1038/ncomms14289
pubmed: 28272390
pmcid: 5344978