Functional characterization of a sex pheromone receptor in the pest moth Spodoptera littoralis by heterologous expression in Drosophila
Moth sex pheromone communication is recognised as a long‐standing model for insect olfaction studies, and a widespread knowledge has been accumulated on this subject thanks to numerous chemical, electrophysiological and behavioural studies. A key step has been the identification of candidate sex phe...
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| Published in | The European journal of neuroscience Vol. 36; no. 5; pp. 2588 - 2596 |
|---|---|
| Main Authors | , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Oxford, UK
Blackwell Publishing Ltd
01.09.2012
Wiley |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0953-816X 1460-9568 1460-9568 |
| DOI | 10.1111/j.1460-9568.2012.08183.x |
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| Abstract | Moth sex pheromone communication is recognised as a long‐standing model for insect olfaction studies, and a widespread knowledge has been accumulated on this subject thanks to numerous chemical, electrophysiological and behavioural studies. A key step has been the identification of candidate sex pheromone receptors, opening new routes to understanding the specificity and sensitivity of this communication system, but only few of these receptors have as yet been functionally characterised. In this context, we aim at unravelling the molecular bases of pheromone reception in the noctuid moth Spodoptera littoralis. Taking advantage of a collection of antennal‐expressed sequence tags, we previously identified three fragments of candidate pheromone receptors in this species. Here, we report full‐length cloning of one of these receptors, named SlitOR6. Both sequence and expression pattern analyses were consistent with its annotation as a pheromone receptor, which we further confirmed by functional characterization. Using Drosophila antennae as a heterologous expression system, we identified a single component of the pheromone blend of S. littoralis, (Z,E)‐9,12‐tetradecadienyl acetate, as the ligand of SlitOR6. Two strategies were employed: (i) expressing SlitOR6 in the majority of Drosophila olfactory neurons, in addition to endogenous receptors, and monitoring the responses to pheromone stimuli by electroantennography; (ii) replacing the Drosophila pheromone receptor OR67d with SlitOR6 and monitoring the response by single sensillum recordings. Results were fully congruent and responses to (Z,E)‐9,12‐tetradecadienyl acetate were highly specific in both heterologous systems. This approach appears to be efficient and reliable for studying moth pheromone receptors in an in vivo context.
A candidate pheromone receptor of the noctuid moth Spodoptera littoralis, was deorphanised using Drosophila antennae as a heterologous expression system. We identified a single component of the pheromone blend of S. littoralis, (Z,E)‐9,12‐tetradecadienyl acetate, as the ligand of this receptor, named SlitOR6. To our knowledge, we report here the first de novo deorphanization of an odorant receptor outside Diptera using heterologous expression in Drosophila. |
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| AbstractList | Moth sex pheromone communication is recognised as a long-standing model for insect olfaction studies, and a widespread knowledge has been accumulated on this subject thanks to numerous chemical, electrophysiological and behavioural studies. A key step has been the identification of candidate sex pheromone receptors, opening new routes to understanding the specificity and sensitivity of this communication system, but only few of these receptors have as yet been functionally characterised. In this context, we aim at unravelling the molecular bases of pheromone reception in the noctuid moth Spodoptera littoralis. Taking advantage of a collection of antennal-expressed sequence tags, we previously identified three fragments of candidate pheromone receptors in this species. Here, we report full-length cloning of one of these receptors, named SlitOR6. Both sequence and expression pattern analyses were consistent with its annotation as a pheromone receptor, which we further confirmed by functional characterization. Using Drosophila antennae as a heterologous expression system, we identified a single component of the pheromone blend of S. littoralis, (Z,E)-9,12-tetradecadienyl acetate, as the ligand of SlitOR6. Two strategies were employed: (i) expressing SlitOR6 in the majority of Drosophila olfactory neurons, in addition to endogenous receptors, and monitoring the responses to pheromone stimuli by electroantennography; (ii) replacing the Drosophila pheromone receptor OR67d with SlitOR6 and monitoring the response by single sensillum recordings. Results were fully congruent and responses to (Z,E)-9,12-tetradecadienyl acetate were highly specific in both heterologous systems. This approach appears to be efficient and reliable for studying moth pheromone receptors in an in vivo context. Moth sex pheromone communication is recognised as a long-standing model for insect olfaction studies, and a widespread knowledge has been accumulated on this subject thanks to numerous chemical, electrophysiological and behavioural studies. A key step has been the identification of candidate sex pheromone receptors, opening new routes to understanding the specificity and sensitivity of this communication system, but only few of these receptors have as yet been functionally characterised. In this context, we aim at unravelling the molecular bases of pheromone reception in the noctuid moth Spodoptera littoralis. Taking advantage of a collection of antennal-expressed sequence tags, we previously identified three fragments of candidate pheromone receptors in this species. Here, we report full-length cloning of one of these receptors, named SlitOR6. Both sequence and expression pattern analyses were consistent with its annotation as a pheromone receptor, which we further confirmed by functional characterization. Using Drosophila antennae as a heterologous expression system, we identified a single component of the pheromone blend of S. littoralis, (Z,E)-9,12-tetradecadienyl acetate, as the ligand of SlitOR6. Two strategies were employed: (i) expressing SlitOR6 in the majority of Drosophila olfactory neurons, in addition to endogenous receptors, and monitoring the responses to pheromone stimuli by electroantennography; (ii) replacing the Drosophila pheromone receptor OR67d with SlitOR6 and monitoring the response by single sensillum recordings. Results were fully congruent and responses to (Z,E)-9,12-tetradecadienyl acetate were highly specific in both heterologous systems. This approach appears to be efficient and reliable for studying moth pheromone receptors in an in vivo context. A candidate pheromone receptor of the noctuid moth Spodoptera littoralis, was deorphanised using Drosophila antennae as a heterologous expression system. We identified a single component of the pheromone blend of S. littoralis, (Z,E)-9,12-tetradecadienyl acetate, as the ligand of this receptor, named SlitOR6. To our knowledge, we report here the first de novo deorphanization of an odorant receptor outside Diptera using heterologous expression in Drosophila. Moth sex pheromone communication is recognised as a long-standing model for insect olfaction studies, and a widespread knowledge has been accumulated on this subject thanks to numerous chemical, electrophysiological and behavioural studies. A key step has been the identification of candidate sex pheromone receptors, opening new routes to understanding the specificity and sensitivity of this communication system, but only few of these receptors have as yet been functionally characterised. In this context, we aim at unravelling the molecular bases of pheromone reception in the noctuid moth Spodoptera littoralis. Taking advantage of a collection of antennal-expressed sequence tags, we previously identified three fragments of candidate pheromone receptors in this species. Here, we report full-length cloning of one of these receptors, named SlitOR6. Both sequence and expression pattern analyses were consistent with its annotation as a pheromone receptor, which we further confirmed by functional characterization. Using Drosophila antennae as a heterologous expression system, we identified a single component of the pheromone blend of S. littoralis, (Z,E)-9,12-tetradecadienyl acetate, as the ligand of SlitOR6. Two strategies were employed: (i) expressing SlitOR6 in the majority of Drosophila olfactory neurons, in addition to endogenous receptors, and monitoring the responses to pheromone stimuli by electroantennography; (ii) replacing the Drosophila pheromone receptor OR67d with SlitOR6 and monitoring the response by single sensillum recordings. Results were fully congruent and responses to (Z,E)-9,12-tetradecadienyl acetate were highly specific in both heterologous systems. This approach appears to be efficient and reliable for studying moth pheromone receptors in an in vivo context.Moth sex pheromone communication is recognised as a long-standing model for insect olfaction studies, and a widespread knowledge has been accumulated on this subject thanks to numerous chemical, electrophysiological and behavioural studies. A key step has been the identification of candidate sex pheromone receptors, opening new routes to understanding the specificity and sensitivity of this communication system, but only few of these receptors have as yet been functionally characterised. In this context, we aim at unravelling the molecular bases of pheromone reception in the noctuid moth Spodoptera littoralis. Taking advantage of a collection of antennal-expressed sequence tags, we previously identified three fragments of candidate pheromone receptors in this species. Here, we report full-length cloning of one of these receptors, named SlitOR6. Both sequence and expression pattern analyses were consistent with its annotation as a pheromone receptor, which we further confirmed by functional characterization. Using Drosophila antennae as a heterologous expression system, we identified a single component of the pheromone blend of S. littoralis, (Z,E)-9,12-tetradecadienyl acetate, as the ligand of SlitOR6. Two strategies were employed: (i) expressing SlitOR6 in the majority of Drosophila olfactory neurons, in addition to endogenous receptors, and monitoring the responses to pheromone stimuli by electroantennography; (ii) replacing the Drosophila pheromone receptor OR67d with SlitOR6 and monitoring the response by single sensillum recordings. Results were fully congruent and responses to (Z,E)-9,12-tetradecadienyl acetate were highly specific in both heterologous systems. This approach appears to be efficient and reliable for studying moth pheromone receptors in an in vivo context. Moth sex pheromone communication is recognised as a long-standing model for insect olfaction studies, and a widespread knowledge has been accumulated on this subject thanks to numerous chemical, electrophysiological and behavioural studies. A key step has been the identification of candidate sex pheromone receptors, opening new routes to understanding the specificity and sensitivity of this communication system, but only few of these receptors have as yet been functionally characterised. In this context, we aim at unravelling the molecular bases of pheromone reception in the noctuid moth Spodoptera littoralis. Taking advantage of a collection of antennal-expressed sequence tags, we previously identified three fragments of candidate pheromone receptors in this species. Here, we report full-length cloning of one of these receptors, named SlitOR6. Both sequence and expression pattern analyses were consistent with its annotation as a pheromone receptor, which we further confirmed by functional characterization. Using Drosophila antennae as a heterologous expression system, we identified a single component of the pheromone blend of S. littoralis, (Z,E)-9,12-tetradecadienyl acetate, as the ligand of SlitOR6. Two strategies were employed: (i) expressing SlitOR6 in the majority of Drosophila olfactory neurons, in addition to endogenous receptors, and monitoring the responses to pheromone stimuli by electroantennography; (ii) replacing the Drosophila pheromone receptor OR67d with SlitOR6 and monitoring the response by single sensillum recordings. Results were fully congruent and responses to (Z,E)-9,12-tetradecadienyl acetate were highly specific in both heterologous systems. This approach appears to be efficient and reliable for studying moth pheromone receptors in an in vivo context. Moth sex pheromone communication is recognised as a long‐standing model for insect olfaction studies, and a widespread knowledge has been accumulated on this subject thanks to numerous chemical, electrophysiological and behavioural studies. A key step has been the identification of candidate sex pheromone receptors, opening new routes to understanding the specificity and sensitivity of this communication system, but only few of these receptors have as yet been functionally characterised. In this context, we aim at unravelling the molecular bases of pheromone reception in the noctuid moth Spodoptera littoralis. Taking advantage of a collection of antennal‐expressed sequence tags, we previously identified three fragments of candidate pheromone receptors in this species. Here, we report full‐length cloning of one of these receptors, named SlitOR6. Both sequence and expression pattern analyses were consistent with its annotation as a pheromone receptor, which we further confirmed by functional characterization. Using Drosophila antennae as a heterologous expression system, we identified a single component of the pheromone blend of S. littoralis, (Z,E)‐9,12‐tetradecadienyl acetate, as the ligand of SlitOR6. Two strategies were employed: (i) expressing SlitOR6 in the majority of Drosophila olfactory neurons, in addition to endogenous receptors, and monitoring the responses to pheromone stimuli by electroantennography; (ii) replacing the Drosophila pheromone receptor OR67d with SlitOR6 and monitoring the response by single sensillum recordings. Results were fully congruent and responses to (Z,E)‐9,12‐tetradecadienyl acetate were highly specific in both heterologous systems. This approach appears to be efficient and reliable for studying moth pheromone receptors in an in vivo context. A candidate pheromone receptor of the noctuid moth Spodoptera littoralis, was deorphanised using Drosophila antennae as a heterologous expression system. We identified a single component of the pheromone blend of S. littoralis, (Z,E)‐9,12‐tetradecadienyl acetate, as the ligand of this receptor, named SlitOR6. To our knowledge, we report here the first de novo deorphanization of an odorant receptor outside Diptera using heterologous expression in Drosophila. Moth sex pheromone communication is recognised as a long‐standing model for insect olfaction studies, and a widespread knowledge has been accumulated on this subject thanks to numerous chemical, electrophysiological and behavioural studies. A key step has been the identification of candidate sex pheromone receptors, opening new routes to understanding the specificity and sensitivity of this communication system, but only few of these receptors have as yet been functionally characterised. In this context, we aim at unravelling the molecular bases of pheromone reception in the noctuid moth Spodoptera littoralis . Taking advantage of a collection of antennal‐expressed sequence tags, we previously identified three fragments of candidate pheromone receptors in this species. Here, we report full‐length cloning of one of these receptors, named SlitOR6. Both sequence and expression pattern analyses were consistent with its annotation as a pheromone receptor, which we further confirmed by functional characterization. Using Drosophila antennae as a heterologous expression system, we identified a single component of the pheromone blend of S. littoralis , ( Z,E )‐9,12‐tetradecadienyl acetate, as the ligand of SlitOR6. Two strategies were employed: (i) expressing SlitOR6 in the majority of Drosophila olfactory neurons, in addition to endogenous receptors, and monitoring the responses to pheromone stimuli by electroantennography; (ii) replacing the Drosophila pheromone receptor OR67d with SlitOR6 and monitoring the response by single sensillum recordings. Results were fully congruent and responses to ( Z,E )‐9,12‐tetradecadienyl acetate were highly specific in both heterologous systems. This approach appears to be efficient and reliable for studying moth pheromone receptors in an in vivo context. |
| Author | Brigaud, Isabelle Larsson, Mattias C. Chertemps, Thomas François, Marie-Christine Montagné, Nicolas Jacquin-Joly, Emmanuelle Lucas, Philippe François, Adrien de Fouchier, Arthur |
| Author_xml | – sequence: 1 givenname: Nicolas surname: Montagné fullname: Montagné, Nicolas organization: UPMC - Université Paris 6, UMR-A 1272 Physiologie de l'Insecte : Signalisation et Communication, Paris, France – sequence: 2 givenname: Thomas surname: Chertemps fullname: Chertemps, Thomas organization: UPMC - Université Paris 6, UMR-A 1272 Physiologie de l'Insecte : Signalisation et Communication, Paris, France – sequence: 3 givenname: Isabelle surname: Brigaud fullname: Brigaud, Isabelle organization: UPMC - Université Paris 6, UMR-A 1272 Physiologie de l'Insecte : Signalisation et Communication, Paris, France – sequence: 4 givenname: Adrien surname: François fullname: François, Adrien organization: UPMC - Université Paris 6, UMR-A 1272 Physiologie de l'Insecte : Signalisation et Communication, Paris, France – sequence: 5 givenname: Marie-Christine surname: François fullname: François, Marie-Christine organization: UPMC - Université Paris 6, UMR-A 1272 Physiologie de l'Insecte : Signalisation et Communication, Paris, France – sequence: 6 givenname: Arthur surname: de Fouchier fullname: de Fouchier, Arthur organization: UPMC - Université Paris 6, UMR-A 1272 Physiologie de l'Insecte : Signalisation et Communication, Paris, France – sequence: 7 givenname: Philippe surname: Lucas fullname: Lucas, Philippe organization: UPMC - Université Paris 6, UMR-A 1272 Physiologie de l'Insecte : Signalisation et Communication, Paris, France – sequence: 8 givenname: Mattias C. surname: Larsson fullname: Larsson, Mattias C. organization: Swedish University of Agricultural Sciences, Department of Plant Protection Biology, Alnarp, Sweden – sequence: 9 givenname: Emmanuelle surname: Jacquin-Joly fullname: Jacquin-Joly, Emmanuelle organization: UPMC - Université Paris 6, UMR-A 1272 Physiologie de l'Insecte : Signalisation et Communication, Paris, France |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/22748123$$D View this record in MEDLINE/PubMed https://hal.science/hal-01001292$$DView record in HAL https://res.slu.se/id/publ/44035$$DView record from Swedish Publication Index |
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| ContentType | Journal Article |
| Copyright | 2012 The Authors. European Journal of Neuroscience © 2012 Federation of European Neuroscience Societies and Blackwell Publishing Ltd 2012 The Authors. European Journal of Neuroscience © 2012 Federation of European Neuroscience Societies and Blackwell Publishing Ltd. Distributed under a Creative Commons Attribution 4.0 International License |
| Copyright_xml | – notice: 2012 The Authors. European Journal of Neuroscience © 2012 Federation of European Neuroscience Societies and Blackwell Publishing Ltd – notice: 2012 The Authors. European Journal of Neuroscience © 2012 Federation of European Neuroscience Societies and Blackwell Publishing Ltd. – notice: Distributed under a Creative Commons Attribution 4.0 International License |
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| Issue | 5 |
| Keywords | olfaction electroantennography pheromone insects odorant receptor single sensillum recordings |
| Language | English |
| License | 2012 The Authors. European Journal of Neuroscience © 2012 Federation of European Neuroscience Societies and Blackwell Publishing Ltd. Distributed under a Creative Commons Attribution 4.0 International License: http://creativecommons.org/licenses/by/4.0 |
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| References_xml | – reference: Grosse-Wilde, E., Stieber, R., Forstner, M., Krieger, J., Wicher, D. & Hansson, B.S. (2010) Sex-specific odorant receptors of the tobacco hornworm Manduca sexta. Front. Cell. Neurosci., 4, 22. – reference: Witzgall, P., Kirsch, P. & Cork, A. (2010) Sex pheromones and their impact on pest management. J. Chem. Ecol., 36, 80-100. – reference: Jones, W.D., Nguyen, T.A., Kloss, B., Lee, K.J. & Vosshall, L.B. (2005) Functional conservation of an insect odorant receptor gene across 250 million years of evolution. Curr. Biol., 15, R119-R121. – reference: Jordan, M.D., Anderson, A., Begum, D., Carraher, C., Authier, A., Marshall, S.D., Kiely, A., Gatehouse, L.N., Greenwood, D.R., Christie, D.L., Kralicek, A.V., Trowell, S.C. & Newcomb, R.D. (2009) Odorant receptors from the light brown apple moth (Epiphyas postvittana) recognize important volatile compounds produced by plants. Chem. Senses, 34, 383-394. – reference: Forstner, M., Gohl, T., Gondesen, I., Raming, K., Breer, H. & Krieger, J. (2008) Differential expression of SNMP-1 and SNMP-2 proteins in pheromone-sensitive hairs of moths. Chem. Senses, 33, 291-299. – reference: Ljungberg, H., Anderson, P. & Hansson, B.S. (1993) Physiology and morphology of pheromone-specific sensilla on the antennae of male and female Spodoptera littoralis (Lepidoptera: Noctuidae). J. Insect Physiol., 39, 253-260. – reference: Jacquin-Joly, E., Bohbot, J., Francois, M.C., Cain, A.H. & Nagnan-Le Meillour, P. (2000) Characterization of the general odorant-binding protein 2 in the molecular coding of odorants in Mamestra brassicae. Eur. J. Biochem., 267, 6708-6714. – reference: Störtkuhl, K.F. & Kettler, R. (2001) Functional analysis of an olfactory receptor in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA, 98, 9381-9385. – reference: Wanner, K.W., Anderson, A.R., Trowell, S.C., Theilmann, D.A., Robertson, H.M. & Newcomb, R.D. (2007) Female-biased expression of odourant receptor genes in the adult antennae of the silkworm, Bombyx mori. Insect Mol. Biol., 16, 107-119. – reference: Krieger, J., Grosse-Wilde, E., Gohl, T., Dewer, Y.M., Raming, K. & Breer, H. (2004) Genes encoding candidate pheromone receptors in a moth (Heliothis virescens). Proc. Natl. Acad. Sci. USA, 101, 11845-11850. – reference: Nakagawa, T., Sakurai, T., Nishioka, T. & Touhara, K. (2005) Insect sex-pheromone signals mediated by specific combinations of olfactory receptors. Science, 307, 1638-1642. – reference: Quero, C., Lucas, P., Renou, M. & Guerrero, A. (1996) Behavioral responses of Spodoptera littoralis males to sex pheromone components and virgin females in wind tunnel. J. Chem. Ecol., 22, 1087-1102. – reference: Benton, R., Sachse, S., Michnick, S.W. & Vosshall, L.B. (2006) Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol., 4, e20. – reference: Garczynski, S.F., Wanner, K.W. & Unruh, T.R. (2011) Identification and initial characterization of the 3′ end of gene transcripts encoding putative members of the pheromone receptor sub-family in Lepidoptera. Insect Science, 19, 64-74. – reference: Wang, G., Vasquez, G.M., Schal, C., Zwiebel, L.J. & Gould, F. (2010) Functional characterization of pheromone receptors in the tobacco budworm Heliothis virescens. Insect Mol. Biol., 20, 125-133. – reference: Legeai, F., Malpel, S., Montagné, N., Monsempes, C., Cousserans, F., Merlin, C., Francois, M.C., Maibèche-Coisne, M., Gavory, F., Poulain, J. & Jacquin-Joly, E. (2011) An expressed sequence tag collection from the male antennae of the Noctuid moth Spodoptera littoralis: a resource for olfactory and pheromone detection research. BMC Genomics, 12, 86. – reference: Dunkelblum, E., Kehat, M., Gothilf, S., Greenberg, S. & Sklarsz, B. (1982) Optimized mixture of sex pheromonal components for trapping of male Spodoptera littoralis in Israel. Phytoparasitica, 10, 21-26. – reference: Syed, Z., Ishida, Y., Taylor, K., Kimbrell, D.A. & Leal, W.S. (2006) Pheromone reception in fruit flies expressing a moth's odorant receptor. Proc. Natl. Acad. Sci. USA, 103, 16538-16543. – reference: Grosse-Wilde, E., Svatos, A. & Krieger, J. (2006) A pheromone-binding protein mediates the bombykol-induced activation of a pheromone receptor in vitro. Chem. Senses, 31, 547-555. – reference: Wanner, K.W., Nichols, A.S., Allen, J.E., Bunger, P.L., Garczynski, S.F., Linn, C.E., Robertson, H.M. & Luetje, C.W. (2010) Sex pheromone receptor specificity in the European corn borer moth, Ostrinia nubilalis. PLoS ONE, 5, e8685. – reference: Krieger, J., Grosse-Wilde, E., Gohl, T. & Breer, H. (2005) Candidate pheromone receptors of the silkmoth Bombyx mori. Eur. J. Neurosci., 21, 2167-2176. – reference: Kreher, S.A., Kwon, J.Y. & Carlson, J.R. 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| Snippet | Moth sex pheromone communication is recognised as a long‐standing model for insect olfaction studies, and a widespread knowledge has been accumulated on this... Moth sex pheromone communication is recognised as a long-standing model for insect olfaction studies, and a widespread knowledge has been accumulated on this... |
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| SubjectTerms | Action Potentials Agricultural sciences Amino Acid Sequence Animals Arthropod Antennae - metabolism Arthropod Antennae - physiology Biochemistry and Molecular Biology Biokemi och molekylärbiologi Diptera Drosophila Drosophila - genetics Drosophila - metabolism Drosophila - physiology electroantennography Gene Expression Insect Proteins - genetics Insect Proteins - metabolism Insect Proteins - physiology insects Life Sciences Molecular Sequence Data Noctuidae odorant receptor olfaction Olfactory Receptor Neurons - physiology pheromone Receptors, Pheromone - genetics Receptors, Pheromone - metabolism Receptors, Pheromone - physiology Sensilla - physiology Sex Attractants - pharmacology single sensillum recordings Spodoptera Spodoptera littoralis Zoologi Zoology |
| Title | Functional characterization of a sex pheromone receptor in the pest moth Spodoptera littoralis by heterologous expression in Drosophila |
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