Transcriptomic Analysis of Light-Induced Genes in <i>Nasonia vitripennis</i>: Possible Implications for Circadian Light Entrainment Pathways
Circadian entrainment to the environmental day–night cycle is essential for the optimal use of environmental resources. In insects, opsin-based photoreception in the compound eye and ocelli and CRYPTOCHROME1 (CRY1) in circadian clock neurons are thought to be involved in sensing photic information,...
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2023-09-01
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author | Yifan Wang Leo W. Beukeboom Bregje Wertheim Roelof A. Hut |
author_facet | Yifan Wang Leo W. Beukeboom Bregje Wertheim Roelof A. Hut |
author_sort | Yifan Wang |
collection | DOAJ |
description | Circadian entrainment to the environmental day–night cycle is essential for the optimal use of environmental resources. In insects, opsin-based photoreception in the compound eye and ocelli and CRYPTOCHROME1 (CRY1) in circadian clock neurons are thought to be involved in sensing photic information, but the genetic regulation of circadian light entrainment in species without light-sensitive CRY1 remains unclear. To elucidate a possible CRY1-independent light transduction cascade, we analyzed light-induced gene expression through RNA-sequencing in <i>Nasonia vitripennis</i>. Entrained wasps were subjected to a light pulse in the subjective night to reset the circadian clock, and light-induced changes in gene expression were characterized at four different time points in wasp heads. We used co-expression, functional annotation, and transcription factor binding motif analyses to gain insight into the molecular pathways in response to acute light stimulus and to form hypotheses about the circadian light-resetting pathway. Maximal gene induction was found after 2 h of light stimulation (1432 genes), and this included the opsin gene <i>opblue</i> and the core clock genes <i>cry2</i> and <i>npas2</i>. Pathway and cluster analyses revealed light activation of glutamatergic and GABA-ergic neurotransmission, including CREB and AP-1 transcription pathway signaling. This suggests that circadian photic entrainment in <i>Nasonia</i> may require pathways that are similar to those in mammals. We propose a model for hymenopteran circadian light-resetting that involves opsin-based photoreception, glutamatergic neurotransmission, and gene induction of <i>cry2</i> and <i>npas2</i> to reset the circadian clock. |
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spelling | doaj.art-415dce1f9a39425c936baf67b147c65b2023-11-19T09:38:38ZengMDPI AGBiology2079-77372023-09-01129121510.3390/biology12091215Transcriptomic Analysis of Light-Induced Genes in <i>Nasonia vitripennis</i>: Possible Implications for Circadian Light Entrainment PathwaysYifan Wang0Leo W. Beukeboom1Bregje Wertheim2Roelof A. Hut3Groningen Institute for Evolutionary Life Sciences, University of Groningen, 9712 CP Groningen, The NetherlandsGroningen Institute for Evolutionary Life Sciences, University of Groningen, 9712 CP Groningen, The NetherlandsGroningen Institute for Evolutionary Life Sciences, University of Groningen, 9712 CP Groningen, The NetherlandsGroningen Institute for Evolutionary Life Sciences, University of Groningen, 9712 CP Groningen, The NetherlandsCircadian entrainment to the environmental day–night cycle is essential for the optimal use of environmental resources. In insects, opsin-based photoreception in the compound eye and ocelli and CRYPTOCHROME1 (CRY1) in circadian clock neurons are thought to be involved in sensing photic information, but the genetic regulation of circadian light entrainment in species without light-sensitive CRY1 remains unclear. To elucidate a possible CRY1-independent light transduction cascade, we analyzed light-induced gene expression through RNA-sequencing in <i>Nasonia vitripennis</i>. Entrained wasps were subjected to a light pulse in the subjective night to reset the circadian clock, and light-induced changes in gene expression were characterized at four different time points in wasp heads. We used co-expression, functional annotation, and transcription factor binding motif analyses to gain insight into the molecular pathways in response to acute light stimulus and to form hypotheses about the circadian light-resetting pathway. Maximal gene induction was found after 2 h of light stimulation (1432 genes), and this included the opsin gene <i>opblue</i> and the core clock genes <i>cry2</i> and <i>npas2</i>. Pathway and cluster analyses revealed light activation of glutamatergic and GABA-ergic neurotransmission, including CREB and AP-1 transcription pathway signaling. This suggests that circadian photic entrainment in <i>Nasonia</i> may require pathways that are similar to those in mammals. We propose a model for hymenopteran circadian light-resetting that involves opsin-based photoreception, glutamatergic neurotransmission, and gene induction of <i>cry2</i> and <i>npas2</i> to reset the circadian clock.https://www.mdpi.com/2079-7737/12/9/1215biological clocklight sensitivityphotoreceptortransduction pathwayRNAseq |
spellingShingle | Yifan Wang Leo W. Beukeboom Bregje Wertheim Roelof A. Hut Transcriptomic Analysis of Light-Induced Genes in <i>Nasonia vitripennis</i>: Possible Implications for Circadian Light Entrainment Pathways Biology biological clock light sensitivity photoreceptor transduction pathway RNAseq |
title | Transcriptomic Analysis of Light-Induced Genes in <i>Nasonia vitripennis</i>: Possible Implications for Circadian Light Entrainment Pathways |
title_full | Transcriptomic Analysis of Light-Induced Genes in <i>Nasonia vitripennis</i>: Possible Implications for Circadian Light Entrainment Pathways |
title_fullStr | Transcriptomic Analysis of Light-Induced Genes in <i>Nasonia vitripennis</i>: Possible Implications for Circadian Light Entrainment Pathways |
title_full_unstemmed | Transcriptomic Analysis of Light-Induced Genes in <i>Nasonia vitripennis</i>: Possible Implications for Circadian Light Entrainment Pathways |
title_short | Transcriptomic Analysis of Light-Induced Genes in <i>Nasonia vitripennis</i>: Possible Implications for Circadian Light Entrainment Pathways |
title_sort | transcriptomic analysis of light induced genes in i nasonia vitripennis i possible implications for circadian light entrainment pathways |
topic | biological clock light sensitivity photoreceptor transduction pathway RNAseq |
url | https://www.mdpi.com/2079-7737/12/9/1215 |
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