Dataset Information

Genome-wide discovery of the daily transcriptome, DNA regulatory elements and transcription factor occupancy in the monarch butterfly brain.

ABSTRACT: The Eastern North American monarch butterfly, Danaus plexippus, is famous for its spectacular seasonal long-distance migration. In recent years, it has also emerged as a novel system to study how animal circadian clocks keep track of time and regulate ecologically relevant daily rhythmic activities and seasonal behavioral outputs. However, unlike in Drosophila and the mouse, little work has been undertaken in the monarch to identify rhythmic genes at the genome-wide level and elucidate the regulation of their diurnal expression. Here, we used RNA-sequencing and Assay for Transposase-Accessible Chromatin (ATAC)-sequencing to profile the diurnal transcriptome, open chromatin regions, and transcription factor (TF) footprints in the brain of wild-type monarchs and of monarchs with impaired clock function, including Cryptochrome 2 (Cry2), Clock (Clk), and Cycle-like loss-of-function mutants. We identified 217 rhythmically expressed genes in the monarch brain; many of them were involved in the regulation of biological processes key to brain function, such as glucose metabolism and neurotransmission. Surprisingly, we found no significant time-of-day and genotype-dependent changes in chromatin accessibility in the brain. Instead, we found the existence of a temporal regulation of TF occupancy within open chromatin regions in the vicinity of rhythmic genes in the brains of wild-type monarchs, which is disrupted in clock deficient mutants. Together, this work identifies for the first time the rhythmic genes and modes of regulation by which diurnal transcription rhythms are regulated in the monarch brain. It also illustrates the power of ATAC-sequencing to profile genome-wide regulatory elements and TF binding in a non-model organism for which TF-specific antibodies are not yet available.

SUBMITTER: Lugena AB

PROVIDER: S-EPMC6677324 | biostudies-literature | 2019 Jul

REPOSITORIES: biostudies-literature

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Genome-wide discovery of the daily transcriptome, DNA regulatory elements and transcription factor occupancy in the monarch butterfly brain.

Lugena Aldrin B AB Zhang Ying Y Menet Jerome S JS Merlin Christine C

PLoS genetics 20190723 7

The Eastern North American monarch butterfly, Danaus plexippus, is famous for its spectacular seasonal long-distance migration. In recent years, it has also emerged as a novel system to study how animal circadian clocks keep track of time and regulate ecologically relevant daily rhythmic activities and seasonal behavioral outputs. However, unlike in Drosophila and the mouse, little work has been undertaken in the monarch to identify rhythmic genes at the genome-wide level and elucidate the regul ...[more]

PMID: 31335862

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Project description:The Eastern North American monarch butterfly, Danaus plexippus, is notorious for its spectacular seasonal long-distance migration. In recent years, it has also emerged as a novel system to study how animal circadian clocks keep track of time and regulate ecologically relevant daily rhythmic activities and seasonal behavioral outputs. However, unlike Drosophila and the mouse, little work has been undertaken in the monarch to identify clock-controlled output genes and elucidate the regulation of their rhythmic expression. Here, we used RNA-sequencing and Assay for Transposase-Accessible Chromatin (ATAC)-sequencing to profile the diurnal transcriptome, open chromatin regions, and transcription factor (TF) footprints in the brain of wild-type monarchs and Cryptochrome 2 (Cry2), Clock (Clk), and Bmal1 (named DCyc-like) butterfly mutants with impaired clock function. We identified 366 rhythmic transcripts under circadian clock control belonging to biological processes key to brain function, such as neurotransmission, neuropeptide signaling, and glucose metabolism. Surprisingly, we found no significant time of day and genotype-dependent changes in chromatin accessibility (i.e., cis-regulatory elements) in the brain. Instead, we found the existence of a temporal regulation of TFs occupancy within open chromatin regions in the vicinity of rhythmic genes in the brains of wild-type monarchs, which is abolished in clock deficient mutants. Our data suggest that TFs binding specifically in the middle of the day display pioneer-like activity by increasing the accessibility of the surrounding chromatin, while TFs binding specifically in the middle of the night would bind DNA with a longer residency time without affecting accessibility of the surrounding chromatin. Together, this work identifies for the first time the clock-controlled genes and modes of regulation by which diurnal transcription rhythms are regulated in the monarch brain. It also illustrates the power of ATAC-seq to profile genome-wide regulatory elements and TF binding in unconventional organisms.

Project description:BackgroundWith the sequence of the Plasmodium falciparum genome and several global mRNA and protein life cycle expression profiling projects now completed, elucidating the underlying networks of transcriptional control important for the progression of the parasite life cycle is highly pertinent to the development of new anti-malarials. To date, relatively little is known regarding the specific mechanisms the parasite employs to regulate gene expression at the mRNA level, with studies of the P. falciparum genome sequence having revealed few cis-regulatory elements and associated transcription factors. Although it is possible the parasite may evoke mechanisms of transcriptional control drastically different from those used by other eukaryotic organisms, the extreme AT-rich nature of P. falciparum intergenic regions (approximately 90% AT) presents significant challenges to in silico cis-regulatory element discovery.ResultsWe have developed an algorithm called Gene Enrichment Motif Searching (GEMS) that uses a hypergeometric-based scoring function and a position-weight matrix optimization routine to identify with high-confidence regulatory elements in the nucleotide-biased and repeat sequence-rich P. falciparum genome. When applied to promoter regions of genes contained within 21 co-expression gene clusters generated from P. falciparum life cycle microarray data using the semi-supervised clustering algorithm Ontology-based Pattern Identification, GEMS identified 34 putative cis-regulatory elements associated with a variety of parasite processes including sexual development, cell invasion, antigenic variation and protein biosynthesis. Among these candidates were novel motifs, as well as many of the elements for which biological experimental evidence already exists in the Plasmodium literature. To provide evidence for the biological relevance of a cell invasion-related element predicted by GEMS, reporter gene and electrophoretic mobility shift assays were conducted.ConclusionThis GEMS analysis demonstrates that in silico regulatory element discovery can be successfully applied to challenging repeat-sequence-rich, base-biased genomes such as that of P. falciparum. The fact that regulatory elements were predicted from a diverse range of functional gene clusters supports the hypothesis that cis-regulatory elements play a role in the transcriptional control of many P. falciparum biological processes. The putative regulatory elements described represent promising candidates for future biological investigation into the underlying transcriptional control mechanisms of gene regulation in malaria parasites.

Dataset Information

Genome-wide discovery of the daily transcriptome, DNA regulatory elements and transcription factor occupancy in the monarch butterfly brain.

Publications

Genome-wide discovery of the daily transcriptome, DNA regulatory elements and transcription factor occupancy in the monarch butterfly brain.

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