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Genome-wide profiling of 24 hr diel rhythmicity in the water flea, Daphnia pulex: network analysis reveals rhythmic gene expression and enhances functional gene annotation

BACKGROUND: Marine and freshwater zooplankton exhibit daily rhythmic patterns of behavior and physiology which may be regulated directly by the light:dark (LD) cycle and/or a molecular circadian clock. One of the best-studied zooplankton taxa, the freshwater crustacean Daphnia, has a 24 h diel verti...

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Autores principales: Rund, Samuel S. C., Yoo, Boyoung, Alam, Camille, Green, Taryn, Stephens, Melissa T., Zeng, Erliang, George, Gary F., Sheppard, Aaron D., Duffield, Giles E., Milenković, Tijana, Pfrender, Michael E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4991082/
https://www.ncbi.nlm.nih.gov/pubmed/27538446
http://dx.doi.org/10.1186/s12864-016-2998-2
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author Rund, Samuel S. C.
Yoo, Boyoung
Alam, Camille
Green, Taryn
Stephens, Melissa T.
Zeng, Erliang
George, Gary F.
Sheppard, Aaron D.
Duffield, Giles E.
Milenković, Tijana
Pfrender, Michael E.
author_facet Rund, Samuel S. C.
Yoo, Boyoung
Alam, Camille
Green, Taryn
Stephens, Melissa T.
Zeng, Erliang
George, Gary F.
Sheppard, Aaron D.
Duffield, Giles E.
Milenković, Tijana
Pfrender, Michael E.
author_sort Rund, Samuel S. C.
collection PubMed
description BACKGROUND: Marine and freshwater zooplankton exhibit daily rhythmic patterns of behavior and physiology which may be regulated directly by the light:dark (LD) cycle and/or a molecular circadian clock. One of the best-studied zooplankton taxa, the freshwater crustacean Daphnia, has a 24 h diel vertical migration (DVM) behavior whereby the organism travels up and down through the water column daily. DVM plays a critical role in resource tracking and the behavioral avoidance of predators and damaging ultraviolet radiation. However, there is little information at the transcriptional level linking the expression patterns of genes to the rhythmic physiology/behavior of Daphnia. RESULTS: Here we analyzed genome-wide temporal transcriptional patterns from Daphnia pulex collected over a 44 h time period under a 12:12 LD cycle (diel) conditions using a cosine-fitting algorithm. We used a comprehensive network modeling and analysis approach to identify novel co-regulated rhythmic genes that have similar network topological properties and functional annotations as rhythmic genes identified by the cosine-fitting analyses. Furthermore, we used the network approach to predict with high accuracy novel gene-function associations, thus enhancing current functional annotations available for genes in this ecologically relevant model species. Our results reveal that genes in many functional groupings exhibit 24 h rhythms in their expression patterns under diel conditions. We highlight the rhythmic expression of immunity, oxidative detoxification, and sensory process genes. We discuss differences in the chronobiology of D. pulex from other well-characterized terrestrial arthropods. CONCLUSIONS: This research adds to a growing body of literature suggesting the genetic mechanisms governing rhythmicity in crustaceans may be divergent from other arthropod lineages including insects. Lastly, these results highlight the power of using a network analysis approach to identify differential gene expression and provide novel functional annotation. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-016-2998-2) contains supplementary material, which is available to authorized users.
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spelling pubmed-49910822016-08-20 Genome-wide profiling of 24 hr diel rhythmicity in the water flea, Daphnia pulex: network analysis reveals rhythmic gene expression and enhances functional gene annotation Rund, Samuel S. C. Yoo, Boyoung Alam, Camille Green, Taryn Stephens, Melissa T. Zeng, Erliang George, Gary F. Sheppard, Aaron D. Duffield, Giles E. Milenković, Tijana Pfrender, Michael E. BMC Genomics Research Article BACKGROUND: Marine and freshwater zooplankton exhibit daily rhythmic patterns of behavior and physiology which may be regulated directly by the light:dark (LD) cycle and/or a molecular circadian clock. One of the best-studied zooplankton taxa, the freshwater crustacean Daphnia, has a 24 h diel vertical migration (DVM) behavior whereby the organism travels up and down through the water column daily. DVM plays a critical role in resource tracking and the behavioral avoidance of predators and damaging ultraviolet radiation. However, there is little information at the transcriptional level linking the expression patterns of genes to the rhythmic physiology/behavior of Daphnia. RESULTS: Here we analyzed genome-wide temporal transcriptional patterns from Daphnia pulex collected over a 44 h time period under a 12:12 LD cycle (diel) conditions using a cosine-fitting algorithm. We used a comprehensive network modeling and analysis approach to identify novel co-regulated rhythmic genes that have similar network topological properties and functional annotations as rhythmic genes identified by the cosine-fitting analyses. Furthermore, we used the network approach to predict with high accuracy novel gene-function associations, thus enhancing current functional annotations available for genes in this ecologically relevant model species. Our results reveal that genes in many functional groupings exhibit 24 h rhythms in their expression patterns under diel conditions. We highlight the rhythmic expression of immunity, oxidative detoxification, and sensory process genes. We discuss differences in the chronobiology of D. pulex from other well-characterized terrestrial arthropods. CONCLUSIONS: This research adds to a growing body of literature suggesting the genetic mechanisms governing rhythmicity in crustaceans may be divergent from other arthropod lineages including insects. Lastly, these results highlight the power of using a network analysis approach to identify differential gene expression and provide novel functional annotation. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-016-2998-2) contains supplementary material, which is available to authorized users. BioMed Central 2016-08-18 /pmc/articles/PMC4991082/ /pubmed/27538446 http://dx.doi.org/10.1186/s12864-016-2998-2 Text en © The Author(s). 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Rund, Samuel S. C.
Yoo, Boyoung
Alam, Camille
Green, Taryn
Stephens, Melissa T.
Zeng, Erliang
George, Gary F.
Sheppard, Aaron D.
Duffield, Giles E.
Milenković, Tijana
Pfrender, Michael E.
Genome-wide profiling of 24 hr diel rhythmicity in the water flea, Daphnia pulex: network analysis reveals rhythmic gene expression and enhances functional gene annotation
title Genome-wide profiling of 24 hr diel rhythmicity in the water flea, Daphnia pulex: network analysis reveals rhythmic gene expression and enhances functional gene annotation
title_full Genome-wide profiling of 24 hr diel rhythmicity in the water flea, Daphnia pulex: network analysis reveals rhythmic gene expression and enhances functional gene annotation
title_fullStr Genome-wide profiling of 24 hr diel rhythmicity in the water flea, Daphnia pulex: network analysis reveals rhythmic gene expression and enhances functional gene annotation
title_full_unstemmed Genome-wide profiling of 24 hr diel rhythmicity in the water flea, Daphnia pulex: network analysis reveals rhythmic gene expression and enhances functional gene annotation
title_short Genome-wide profiling of 24 hr diel rhythmicity in the water flea, Daphnia pulex: network analysis reveals rhythmic gene expression and enhances functional gene annotation
title_sort genome-wide profiling of 24 hr diel rhythmicity in the water flea, daphnia pulex: network analysis reveals rhythmic gene expression and enhances functional gene annotation
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4991082/
https://www.ncbi.nlm.nih.gov/pubmed/27538446
http://dx.doi.org/10.1186/s12864-016-2998-2
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