Light and Temperature Synchronizes Locomotor Activity in the Linden Bug, Pyrrhocoris apterus

Kaniewska, Magdalena Maria; Vaněčková, Hana; Doležel, David; Kotwica‐Rolinska, Joanna

doi:10.3389/fphys.2020.00242

Cited by 16 publications

(11 citation statements)

References 58 publications

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“…RNAi silencing of tim-m supports its role in the clock, which is consistent with its oscillatory role in the rat neuronal cells ( Barnes et al 2003 ). Nevertheless, relatively low P. apterus activity levels and their broad peaks (see Kaniewska et al 2020 ) make it difficult to determine whether alterations of clock gene expression cause phase shifts in behavioral outputs. Thus, the role of TIM-m in circadian photoreception, proposed by the fruit fly experiments ( Benna et al 2010 ) and suggested by the altered activity phase in mammals ( Kurien et al 2019 ), could only be addressed in P. apterus with great difficulties.…”

Section: Discussionmentioning

confidence: 99%

Loss of Timeless Underlies an Evolutionary Transition within the Circadian Clock

Kotwica‐Rolinska

Chodáková

Smýkal

et al. 2021

Molecular Biology and Evolution

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Most organisms possess time-keeping devices called circadian clocks. At the molecular level, circadian clocks consist of transcription-translation feedback loops. Although some components of the negative transcription-translation feedback loop are conserved across the animals, important differences exist between typical models, such as mouse and the fruit fly. In Drosophila, the key components are PERIOD (PER) and TIMELESS (TIM-d) proteins, whereas the mammalian clock relies on PER and CRYPTOCHROME (CRY-m). Importantly, how the clock has maintained functionality during evolutionary transitions between different states remains elusive. Therefore, we systematically described the circadian clock gene setup in major bilaterian lineages and identified marked lineage-specific differences in their clock constitution. Then we performed a thorough functional analysis of the linden bug Pyrrhocoris apterus, an insect species comprising features characteristic of both the Drosophila and the mammalian clocks. Unexpectedly, the knockout of timeless-d, a gene essential for the clock ticking in Drosophila, did not compromise rhythmicity in P. apterus, it only accelerated its pace. Furthermore, silencing timeless-m, the ancestral timeless type ubiquitously present across animals, resulted in a mild gradual loss of rhythmicity, supporting its possible participation in the linden bug clock, which is consistent with timeless-m role suggested by research on mammalian models. The dispensability of timeless-d in P. apterus allows drawing a scenario in which the clock has remained functional at each step of transition from an ancestral state to the TIM-d-independent PER+CRY-mammalian system operating in extant vertebrates, including humans.

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Section: Discussionmentioning

confidence: 99%

Loss of Timeless Underlies an Evolutionary Transition within the Circadian Clock

Kotwica‐Rolinska

Chodáková

Smýkal

et al. 2021

Molecular Biology and Evolution

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“…The linden bug P. apterus is a long-established model for studies concerning diapause and photoperiodism (reviewed in (Socha, 1993;Saunders, 2021) and references therein), and recently also the circadian clock in this species was addressed in more detail (Pivarciova et al, 2016;Kaniewska et al, 2020;Kotwica-Rolinska et al, 2021). Linden bugs are typical diurnal animals showing the peak of the activity around the middle of the day.…”

Section: Introductionmentioning

confidence: 99%

Pigment Dispersing Factor Is a Circadian Clock Output and Regulates Photoperiodic Response in the Linden Bug, Pyrrhocoris apterus

et al. 2022

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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.

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“…No studies have yet investigated thermal entrainment in non-bilaterian animals, and few studies have measured circadian behavior during simultaneous light and temperature cycles in any animal. Since the late 1950's, there have been studies of conflicting light and temperature cycles in insects [4,[18][19][20][21][22][23][24], vertebrates [25][26][27][28], protists [29], and cyanobacteria [30]. There have also been studies of light in conjunction with time-restricted feeding in vertebrates [31][32][33][34].…”

Section: Introductionmentioning

confidence: 99%

“…Current research of sensory conflict is limited by a dearth of comprehensive behavioral experiments. The small literature of sensory conflict studies has examined conflicting light and temperature cycles in insects ( Miyasako et al, 2007; Currie et al, 2009; Watari and Tanaka, 2010; Yoshii et al, 2010; Nikhil et al, 2014; Harper et al, 2016, 2017; Rivas et al, 2018; Kaniewska et al, 2020 ), vertebrates ( Firth and Kennaway, 1989; Valenciano et al, 1997; Moyer et al, 1997; Firth et al, 1999 ), protists ( Bruce, 1960 ), and cyanobacteria ( Lin et al, 1999 ). There have also been studies of light and time-restricted feeding in vertebrates ( Javier Sánchez-Vázquez et al, 1995; Challet et al, 1998; Reierth and Stokkan, 1998; Lague and Reebs, 2000 ).…”

Section: Introductionmentioning

confidence: 99%

Sensory conflict disrupts circadian rhythms in the sea anemone Nematostella vectensis

Berger

Tarrant

2022

Preprint

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Circadian clocks allow organisms to optimize their phenotypes in relation to rhythmic environmental conditions. Clocks must synchronize, or entrain, to environmental signals called zeitgebers (such as light and temperature) while maintaining internal rhythms that are robust to environmental noise. We know surprisingly little about how clocks function in the presence of multiple zeitgebers, although these are the conditions that exist in nature. Misalignment between zeitgeber cycles (here, "sensory conflict") can disrupt circadian rhythms in behavior and gene expression, but it is not clear whether this is generally true across animals. In order to understand general rules about animal clocks, and how clocks have evolved throughout Metazoa, it is necessary to study non-bilaterian animals such as cnidarians, which include corals, jellies, and sea anemones. The sea anemone Nematostella vectensis has emerged as the principal model system for cnidarian circadian biology. In this study, we show that temperature cycles entrain circadian locomotor rhythms in Nematostella, and then conduct extensive behavioral experiments across a range of light and temperature cycles to show that Nematostella's circadian behavior is disrupted by sensory conflict. Chronic exposure to conflicting light and temperature cycles also causes substantial changes to the rhythmic transcriptome, including the breakdown of rhythmic expression of various metabolic processes. These results have important implications for our understanding of cnidarian circadian clocks at both the molecular and organismal levels, and for how sensory information is processed by clocks in the absence of a central nervous system.

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Light and Temperature Synchronizes Locomotor Activity in the Linden Bug, Pyrrhocoris apterus

Cited by 16 publications

References 58 publications

Loss of Timeless Underlies an Evolutionary Transition within the Circadian Clock

Loss of Timeless Underlies an Evolutionary Transition within the Circadian Clock

Pigment Dispersing Factor Is a Circadian Clock Output and Regulates Photoperiodic Response in the Linden Bug, Pyrrhocoris apterus

Sensory conflict disrupts circadian rhythms in the sea anemone Nematostella vectensis

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