Pigment Dispersing Factor Is a Circadian Clock Output and Regulates Photoperiodic Response in the Linden Bug, Pyrrhocoris apterus
Daily and annually cycling conditions manifested on the Earth have forced organisms to develop time-measuring devices. Circadian clocks are responsible for adjusting physiology to the daily cycles in the environment, while the anticipation of seasonal changes is governed by the photoperiodic clock....
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-04-01
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| Series: | Frontiers in Physiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fphys.2022.884909/full |
| _version_ | 1811302874110492672 |
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| author | Joanna Kotwica-Rolinska Milena Damulewicz Lenka Chodakova Lenka Chodakova Lucie Kristofova David Dolezel David Dolezel |
| author_facet | Joanna Kotwica-Rolinska Milena Damulewicz Lenka Chodakova Lenka Chodakova Lucie Kristofova David Dolezel David Dolezel |
| author_sort | Joanna Kotwica-Rolinska |
| collection | DOAJ |
| description | Daily and annually cycling conditions manifested on the Earth have forced organisms to develop time-measuring devices. Circadian clocks are responsible for adjusting physiology to the daily cycles in the environment, while the anticipation of seasonal changes is governed by the photoperiodic clock. Circadian clocks are cell-autonomous and depend on the transcriptional/translational feedback loops of the conserved clock genes. The synchronization among clock centers in the brain is achieved by the modulatory function of the clock-dependent neuropeptides. In insects, the most prominent clock neuropeptide is Pigment Dispersing Factor (PDF). Photoperiodic clock measures and computes the day and/or night length and adjusts physiology accordingly to the upcoming season. The exact mechanism of the photoperiodic clock and its direct signaling molecules are unknown but, in many insects, circadian clock genes are involved in the seasonal responses. While in Drosophila, PDF signaling participates both in the circadian clock output and in diapause regulation, the weak photoperiodic response curve of D. melanogaster is a major limitation in revealing the full role of PDF in the photoperiodic clock. Here we provide the first description of PDF in the linden bug, Pyrrhocoris apterus, an organism with a robust photoperiodic response. We characterize in detail the circadian and photoperiodic phenotype of several CRISPR/Cas9-generated pdf mutants, including three null mutants and two mutants with modified PDF. Our results show that PDF acts downstream of CRY and plays a key role as a circadian clock output. Surprisingly, in contrast to the diurnal activity of wild-type bugs, pdf null mutants show predominantly nocturnal activity, which is caused by the clock-independent direct response to the light/dark switch. Moreover, we show that together with CRY, PDF is involved in the photoperiod-dependent diapause induction, however, its lack does not disrupt the photoperiodic response completely, suggesting the presence of additional clock-regulated factors. Taken together our data provide new insight into the role of PDF in the insect’s circadian and photoperiodic systems. |
| first_indexed | 2024-04-13T07:37:12Z |
| format | Article |
| id | doaj.art-9864bbc1859c489e9a6924005a72cf89 |
| institution | Directory Open Access Journal |
| issn | 1664-042X |
| language | English |
| last_indexed | 2024-04-13T07:37:12Z |
| publishDate | 2022-04-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Physiology |
| spelling | doaj.art-9864bbc1859c489e9a6924005a72cf892022-12-22T02:56:07ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2022-04-011310.3389/fphys.2022.884909884909Pigment Dispersing Factor Is a Circadian Clock Output and Regulates Photoperiodic Response in the Linden Bug, Pyrrhocoris apterusJoanna Kotwica-Rolinska0Milena Damulewicz1Lenka Chodakova2Lenka Chodakova3Lucie Kristofova4David Dolezel5David Dolezel6Institute of Entomology, Biology Centre of the Czech Academy of Sciences, České Budějovice, Czech RepublicInstitute of Zoology and Biomedical Research, Jagiellonian University, Kraków, PolandInstitute of Entomology, Biology Centre of the Czech Academy of Sciences, České Budějovice, Czech RepublicFaculty of Science, University of South Bohemia, České Budějovice, Czech RepublicInstitute of Entomology, Biology Centre of the Czech Academy of Sciences, České Budějovice, Czech RepublicInstitute of Entomology, Biology Centre of the Czech Academy of Sciences, České Budějovice, Czech RepublicFaculty of Science, University of South Bohemia, České Budějovice, Czech RepublicDaily and annually cycling conditions manifested on the Earth have forced organisms to develop time-measuring devices. Circadian clocks are responsible for adjusting physiology to the daily cycles in the environment, while the anticipation of seasonal changes is governed by the photoperiodic clock. Circadian clocks are cell-autonomous and depend on the transcriptional/translational feedback loops of the conserved clock genes. The synchronization among clock centers in the brain is achieved by the modulatory function of the clock-dependent neuropeptides. In insects, the most prominent clock neuropeptide is Pigment Dispersing Factor (PDF). Photoperiodic clock measures and computes the day and/or night length and adjusts physiology accordingly to the upcoming season. The exact mechanism of the photoperiodic clock and its direct signaling molecules are unknown but, in many insects, circadian clock genes are involved in the seasonal responses. While in Drosophila, PDF signaling participates both in the circadian clock output and in diapause regulation, the weak photoperiodic response curve of D. melanogaster is a major limitation in revealing the full role of PDF in the photoperiodic clock. Here we provide the first description of PDF in the linden bug, Pyrrhocoris apterus, an organism with a robust photoperiodic response. We characterize in detail the circadian and photoperiodic phenotype of several CRISPR/Cas9-generated pdf mutants, including three null mutants and two mutants with modified PDF. Our results show that PDF acts downstream of CRY and plays a key role as a circadian clock output. Surprisingly, in contrast to the diurnal activity of wild-type bugs, pdf null mutants show predominantly nocturnal activity, which is caused by the clock-independent direct response to the light/dark switch. Moreover, we show that together with CRY, PDF is involved in the photoperiod-dependent diapause induction, however, its lack does not disrupt the photoperiodic response completely, suggesting the presence of additional clock-regulated factors. Taken together our data provide new insight into the role of PDF in the insect’s circadian and photoperiodic systems.https://www.frontiersin.org/articles/10.3389/fphys.2022.884909/fullpigment dispersing factorcryptochrome-mcircadian clockphotoperiodic clockdiapauseCRISPR/Cas9 |
| spellingShingle | Joanna Kotwica-Rolinska Milena Damulewicz Lenka Chodakova Lenka Chodakova Lucie Kristofova David Dolezel David Dolezel Pigment Dispersing Factor Is a Circadian Clock Output and Regulates Photoperiodic Response in the Linden Bug, Pyrrhocoris apterus Frontiers in Physiology pigment dispersing factor cryptochrome-m circadian clock photoperiodic clock diapause CRISPR/Cas9 |
| title | Pigment Dispersing Factor Is a Circadian Clock Output and Regulates Photoperiodic Response in the Linden Bug, Pyrrhocoris apterus |
| title_full | Pigment Dispersing Factor Is a Circadian Clock Output and Regulates Photoperiodic Response in the Linden Bug, Pyrrhocoris apterus |
| title_fullStr | Pigment Dispersing Factor Is a Circadian Clock Output and Regulates Photoperiodic Response in the Linden Bug, Pyrrhocoris apterus |
| title_full_unstemmed | Pigment Dispersing Factor Is a Circadian Clock Output and Regulates Photoperiodic Response in the Linden Bug, Pyrrhocoris apterus |
| title_short | Pigment Dispersing Factor Is a Circadian Clock Output and Regulates Photoperiodic Response in the Linden Bug, Pyrrhocoris apterus |
| title_sort | pigment dispersing factor is a circadian clock output and regulates photoperiodic response in the linden bug pyrrhocoris apterus |
| topic | pigment dispersing factor cryptochrome-m circadian clock photoperiodic clock diapause CRISPR/Cas9 |
| url | https://www.frontiersin.org/articles/10.3389/fphys.2022.884909/full |
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