Article

Insect Cryptochromes: Gene Duplication and Loss Define Diverse Ways to Construct Insect Circadian Clocks

University of Massachusetts Amherst, Amherst Center, Massachusetts, United States
Molecular Biology and Evolution (Impact Factor: 9.11). 05/2007; 24(4):948-55. DOI: 10.1093/molbev/msm011
Source: PubMed

ABSTRACT

Cryptochrome (CRY) proteins are components of the central circadian clockwork of metazoans. Phylogenetic analyses show at least 2 rounds of gene duplication at the base of the metazoan radiation, as well as several losses, gave rise to 2 cryptochrome (cry) gene families in insects, a Drosophila-like cry1 gene family and a vertebrate-like cry2 family. Previous studies have shown that insect CRY1 is photosensitive, whereas photo-insensitive CRY2 functions to potently inhibit clock-relevant CLOCK:CYCLE-mediated transcription. Here, we extended the transcriptional repressive function of insect CRY2 to 2 orders--Hymenoptera (the honeybee Apis mellifera and the bumblebee Bombus impatiens) and Coleoptera (the red flour beetle Tribolium castaneum). Importantly, the bee and beetle CRY2 proteins are not light sensitive in culture, in either degradation of protein levels or inhibitory transcriptional response, suggesting novel light input pathways into their circadian clocks as Apis and Tribolium do not have CRY1. By mapping the functional data onto a cryptochrome/6-4 photolyase gene tree, we find that the transcriptional repressive function of insect CRY2 descended from a light-sensitive photolyase-like ancestral gene, probably lacking the ability to repress CLOCK:CYCLE-mediated transcription. These data provide an evolutionary context for proposing novel circadian clock mechanisms in insects.

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    • "All five genes were found in two species of Lepidoptera (Bombyx mori and D. plexippus), in three mosquitoes (Anopheles gambiae, Aedes aegypti and Culex quinquefasciatus) and in the aphid Acyrthosiphon pisum. The form of the circadian clock containing cry2 is regarded as 'ancestral' (Yuan et al., 2007;Sandrelli et al., 2008;Merlin & Reppert, 2010;Tomioka & Matsumoto, 2010), whereas that in D. melanogaster, in which cry2 has been lost, and that in the honey bee A. mellifera (Rubin et al., 2006) and in N. vitripennis, in which both cry1 and tim have been lost, are considered to be 'derived'. If these differences also occur in the photoperiodic mechanism, substantial differences in the way clock genes are involved in photoperiodism may also be expected (Saunders & Bertossa, 2011). "
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    ABSTRACT: In 1936, Erwin Bünning suggested that photoperiodic time measurement was a function of the circadian system. Colin Pittendrigh became an ardent supporter of Bünning's hypothesis, drawing parallels between photoperiodism and his own group's investigations of adult eclosion rhythmicity in the fruit fly Drosophila pseudoobscura. They developed several more modern versions of Bünning's general hypothesis based on the entrainment of circadian oscillations to the light cycle, including ‘external coincidence’, which is a derivation of Bünning's original model, and ‘internal coincidence’, which relied upon seasonal changes in the mutual phase relationship of oscillators within a multi-oscillator circadian system. This review considers the experimental evidence for the central role of the circadian system in photoperiodic timing and, in some species, for both external and internal coincidence. Pittendrigh, however, pursued the idea of internal coincidence further with his analysis of the pacemaker–slave organization of eclosion rhythmicity in D. pseudoobscura and proposed a similar theoretical model for photoperiodism comprising a group of slave oscillators driven by a light-sensitive pacemaker. In this model, the phase relationships of the slaves to the pacemaker were affected by (i) the relative periods of the pacemaker and slave(s); (ii) the strength(s) of the coupling between the two; and (iii) the dampening coefficients of the various slaves. Manipulation of these variables showed that the slaves adopted different internal phase relationships (both to each other and to the pacemaker) under the influence of changes in daily photophase, the period of the Zeitgeber and phase shifts of the entraining light cycle.
    Full-text · Article · Jan 2016 · Physiological Entomology
    • "Although Drosophila and closely related flies have only one cry gene, some insects, such as African malaria mosquito, Anopheles gambiae (Giles), and yellowfever mosquito, Aedes aegypti (L.) (Zhu et al. 2005, Yuan et al. 2007), have two kinds of cryptochrome: cry1, which is orthologous to Drosophila cry, and cry2 more closely related to the mammalian Cry genes. Other insects, such as the honey bee, Apis mellifera (L.), have only cry2 (Rubin et al. 2006, Yuan et al. 2007). Circadian genes have been cloned in species closely related to D. melanogaster such as A. gambiae (Holt et al. 2002) and A. aegypti (Nene et al. 2007). "

    No preview · Article · Mar 2015 · Southwestern Entomologist
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    • "Although Drosophila and closely related flies have only one cry gene, some insects, such as African malaria mosquito, Anopheles gambiae (Giles), and yellowfever mosquito, Aedes aegypti (L.) (Zhu et al. 2005, Yuan et al. 2007), have two kinds of cryptochrome: cry1, which is orthologous to Drosophila cry, and cry2 more closely related to the mammalian Cry genes. Other insects, such as the honey bee, Apis mellifera (L.), have only cry2 (Rubin et al. 2006, Yuan et al. 2007). Circadian genes have been cloned in species closely related to D. melanogaster such as A. gambiae (Holt et al. 2002) and A. aegypti (Nene et al. 2007). "
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    ABSTRACT: In eukaryotes, the timeless (TIM) gene plays a fundamental role in the control of the circadian clock by regulating several biochemical, physiological, and behavioral processes. RT-PCR was used to amplify TIM mRNA from larval southern house mosquito, Culex quinquefasciatus Say, from three locations in the State of Nuevo Leon in northeastern Mexico. The 3062 bp TIM cDNA was assembled from three overlapping PCRs that were cloned and sequenced. DNA sequence analysis used amplified cDNA fragments to complete coding the DNA sequence (2991 bp). Tim ORF consisting of 996 codons was shorter than the orthologous genes from other mosquito species. A series of deletions in the core sequence of TIM were detected. No other amplification products were visualized, and thus, the possibility of alternative spliced mRNA species was discarded. Because TIM is a widely conserved gene in eukaryotes, and maintaining colonies of Cx. quinquefasciatus is easy, determining the sequence of the TIM gene in the mosquito provides the possibility of its use as a model for circadian clock experimentation.
    Full-text · Article · Mar 2015 · Southwestern Entomologist
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