Circadian clock regulates photoperiodic responses governed by distinct output pathways in the bean bug,<i>Riptortus pedestris</i>

Omura, Shigeki; Numata, Hideharu; Goto, Shin G.

doi:10.1080/09291016.2016.1212515

Cited by 22 publications

(20 citation statements)

References 32 publications

(42 reference statements)

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“…Although the cues that stimulate NSCs to secrete PTTH are known in some insect species (Richter et al, 2000;Mohamed et al, 2014;Wang et al, 2013Wang et al, , 2015, it is not known what factors at the molecular level control the decision to activate or to stop PTTH synthesis and/or release (Vafopoulou & Steel, 1996;Steel & Vafopoulou, 2006;Vafopoulou et al, 2007). Similar to what is known in vertebrates (Dardente et al, 2010), a role for the circadian clock in insect photoperiodic responses has been proposed by several groups (Ikeno et al, 2010;Pegoraro et al, 2014;Denlinger & Armbruster, 2016;Omura et al, 2016;Reppert et al, 2016). In this respect, it was shown long ago that, in larvae of M. sexta, interaction of the circadian clock with environmental photoperiod restricts PTTH release to a specific portion of the day-night cycle (Truman & Riddiford, 1974).…”

Section: Introductionmentioning

confidence: 99%

Identification of the prothoracicotropic hormone (Ptth) coding gene and localization of its site of expression in the pea aphid Acyrthosiphon pisum

Barberà

Martínez‐Torres

2017

Insect Molecular Biology

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Insect hormones control essential aspects of physiology, behaviour and development in insects. The majority of insect hormones are peptide hormones that perform a highly diverse catalogue of functions. Prothoracicotropic hormone (PTTH) is a brain neuropeptide hormone whose main function is to stimulate the secretion of ecdysone (the moulting hormone) by the prothoracic glands in insect larvae thus playing a key role in the control of moulting and metamorphosis. Moreover, both PTTH release or blockade have been reported to act as a switch to terminate or initiate larval and pupal diapauses. In insects, diapause is a prevalent response often regulated by the photoperiod. It has been shown that PTTH participates as an output of the circadian clock and a role in photoperiodic processes is suggested in some insect species. Aphids (Hemiptera: Aphididae) reproduce by cyclical parthenogenesis with a sexual phase, induced by short photoperiods, that leads to the production of diapausing eggs. With the availability of the pea aphid (Acyrthosiphon pisum) genome, efforts to identify and characterize genes relevant to essential aspects of aphid biology have multiplied. In spite of its relevance, several genomic and transcriptomic studies on aphid neuropeptides failed to detect aphid PTTH amongst them. Here we report on the first identification of the aphid PTTH coding gene and the neuroanatomical localization of its expression in the aphid brain.

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Section: Introductionmentioning

confidence: 99%

Identification of the prothoracicotropic hormone (Ptth) coding gene and localization of its site of expression in the pea aphid Acyrthosiphon pisum

Barberà

Martínez‐Torres

2017

Insect Molecular Biology

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“…In plants and mammals, the circadian clock and the photoperiodic response have been shown to be linked (Dardente et al, 2010;Imaizumi, 2010). Similar to what is known in vertebrates, a role for the circadian clock in insect photoperiodism has been proposed by several groups (Denlinger and Armbruster, 2016;Ikeno et al, 2010;Omura et al, 2016;Pegoraro et al, 2014;Reppert et al, 2016). However, the implication of the circadian clockwork in the insect photoperiodic response is not yet fully understood and some authors strongly put this proposal into question (Bradshaw and Holzapfel, 2010).…”

Section: Introductionmentioning

confidence: 94%

“…In general, insects have developed more or less complex life cycles in which they synchronise the appropriate phase of their life cycles with the season they are specialised for. Different insects overcome the adverse season following alternative strategies such as a programmed migration (Reppert et al, 2016), diapause (Denlinger and Armbruster, 2014;Omura et al, 2016) or developing specific morphs (Saunders, 2009;Simon et al, 2010;Tagu et al, 2005). In plants and mammals, the circadian clock and the photoperiodic response have been shown to be linked (Dardente et al, 2010;Imaizumi, 2010).…”

Section: Introductionmentioning

confidence: 99%

“…However, in recent years, evidence for the involvement of circadian genes in the seasonal response in different insect species have been accumulating. RNAi experiments on circadian genes have shown to have an effect on both circadian rhythms and seasonal responses in the dipteran Chymomyza costata (Pavelka et al, 2003), the orthopteran Modicogryllus siamensis , the hemipteran Riptortus pedestris (Ikeno et al, 2010;Omura et al, 2016), the lepidopteran Antheraea pernyi (Mohamed et al, 2014) and the dipteran Culex pipiens (Meuti et al, 2015). In addition, mutant alleles of circadian clock genes in Drosophila have been shown to correlate with differential seasonal responses (Pegoraro et al, 2014;Sandrelli et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

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Characterisation, analysis of expression and localisation of circadian clock genes from the perspective of photoperiodism in the aphid Acyrthosiphon pisum

Barberà

Collantes-Alegre

Martínez‐Torres

2017

Insect Biochemistry and Molecular Biology

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Aphids are typical photoperiodic insects that switch from viviparous parthenogenetic reproduction typical of long day seasons to oviparous sexual reproduction triggered by the shortening of photoperiod in autumn yielding an overwintering egg in which an embryonic diapause takes place. While the involvement of the circadian clock genes in photoperiodism in mammals is well established, there is still some controversy on their participation in insects. The availability of the genome of the pea aphid Acyrthosiphon pisum places this species as an excellent model to investigate the involvement of the circadian system in the aphid seasonal response. In the present report, we have advanced in the characterisation of the circadian clock genes and showed that these genes display extensive alternative splicing. Moreover, the expression of circadian clock genes, analysed at different moments of the day, showed a robust cycling of central clock genes period and timeless. Furthermore, the rhythmic expression of these genes was shown to be rapidly dampened under DD (continuous darkness conditions), thus supporting the model of a seasonal response based on a heavily dampened circadian oscillator. Additionally, increased expression of some of the circadian clock genes under short-day conditions suggest their involvement in the induction of the aphid seasonal response. Finally, in situ localisation of transcripts of genes period and timeless in the aphid brain revealed the site of clock neurons for the first time in aphids. Two groups of clock cells were identified: the Dorsal Neurons (DN) and the Lateral Neurons (LN), both in the protocerebrum.

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“…For insects with a facultative diapause, environmental stimuli perceived during the diapause induction phase determine whether an individual will enter the diapause developmental trajectory or not (Sim and Denlinger, 2013; Omura et al, 2016). These environmental stimuli are translated into endocrine signals that regulate developmental arrest, nutrient accumulation, and stress resistance during the diapause preparation phase (Hahn and Denlinger, 2007; MacRae, 2010).…”

Section: Introductionmentioning

confidence: 99%

Describing the Diapause-Preparatory Proteome of the Beetle Colaphellus bowringi and Identifying Candidates Affecting Lipid Accumulation Using Isobaric Tags for Mass Spectrometry-Based Proteome Quantification (iTRAQ)

et al. 2017

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Prior to entering diapause, insects must prepare themselves physiologically to withstand the stresses of arresting their development for a lengthy period. While studies describing the biochemical and cellular milieu of the maintenance phase of diapause are accumulating, few studies have taken an “omics” approach to describing molecular events during the diapause preparatory phase. We used isobaric tags and mass spectrometry (iTRAQ) to quantitatively compare the expression profiles of proteins identified during the onset of diapause preparation phase in the heads of adult female cabbage beetles, Colaphellus bowringi. A total of 3,175 proteins were identified, 297 of which were differentially expressed between diapause-destined and non-diapause-destined female adults and could therefore be involved in diapause preparation in this species. Comparison of identified proteins with protein function databases shows that many of these differentially expressed proteins enhanced in diapause destined beetles are involved in energy production and conversion, carbohydrate metabolism and transport, and lipid metabolism. Further hand annotation of differentially abundant peptides nominates several associated with stress hardiness, including HSPs and antioxidants, as well as neural development. In contrast, non-diapause destined beetles show substantial increases in cuticle proteins, suggesting additional post-emergence growth. Using RNA interference to silence a fatty acid-binding protein (FABP) that was highly abundant in the head of diapause-destined females prevented the accumulation of lipids in the fat body, a common product of diapause preparation in this species and others. Surprisingly, RNAi against the FABP also affected the transcript abundance of several heat shock proteins. These results suggest that the identified differentially expressed proteins that play vital roles in lipid metabolism may also contribute somehow to enhanced hardiness to environmental stress that is characteristic of diapause.

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Circadian clock regulates photoperiodic responses governed by distinct output pathways in the bean bug,Riptortus pedestris

Cited by 22 publications

References 32 publications

Identification of the prothoracicotropic hormone (Ptth) coding gene and localization of its site of expression in the pea aphid Acyrthosiphon pisum

Identification of the prothoracicotropic hormone (Ptth) coding gene and localization of its site of expression in the pea aphid Acyrthosiphon pisum

Characterisation, analysis of expression and localisation of circadian clock genes from the perspective of photoperiodism in the aphid Acyrthosiphon pisum

Describing the Diapause-Preparatory Proteome of the Beetle Colaphellus bowringi and Identifying Candidates Affecting Lipid Accumulation Using Isobaric Tags for Mass Spectrometry-Based Proteome Quantification (iTRAQ)

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