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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Main Authors: Yifan Wang, Leo W. Beukeboom, Bregje Wertheim, Roelof A. Hut
Format: Article
Language:English
Published: MDPI AG 2023-09-01
Series:Biology
Subjects:
Online Access:https://www.mdpi.com/2079-7737/12/9/1215
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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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AT bregjewertheim transcriptomicanalysisoflightinducedgenesininasoniavitripennisipossibleimplicationsforcircadianlightentrainmentpathways
AT roelofahut transcriptomicanalysisoflightinducedgenesininasoniavitripennisipossibleimplicationsforcircadianlightentrainmentpathways