Evolution of vertebrate gill covers through shifts in an ancient gnathostome Pou3f3 enhancer
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ABSTRACT:
PROVIDER: PRJNA590283 | ENA |
REPOSITORIES: ENA
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Project description:Whereas the gill chambers of extant jawless vertebrates (lampreys and hagfish) open directly into the environment, jawed vertebrates have evolved skeletal appendages that promote the unidirectional flow of oxygenated water over the gills. A major anatomical difference between the two jawed vertebrate lineages is the presence of a single operculum covering a large common gill cavity in bony fishes versus separate covers for each gill chamber in cartilaginous fishes. Here we find that these divergent gill cover patterns correlate with the pharyngeal arch expression of Pou3f3 orthologs, and we identify a deeply conserved Pou3f3 arch enhancer that is present in nearly all jawed vertebrates but undetectable in lampreys. Despite only minor sequence differences, bony fish and cartilaginous fish versions of this enhancer are sufficient to drive the respective single versus multiple gill arch expression. In zebrafish, loss of Pou3f3 gene function or its conserved enhancer disrupts gill cover formation. Conversely, forced expression of Pou3f3b in the gill arches generates ectopic skeletal elements reminiscent of the multiple gill covers of cartilaginous fish. Emergence and modification of this ancient Pou3f3 enhancer may thus have contributed to the acquisition and diversification of gill covers during early gnathostome evolution.
2020-06-17 | GSE140636 | GEO
Project description:Vertebrates have highly methylated genomes at CpG positions while most invertebrates have sparsely methylated genomes. Therefore, hypermethylation is considered a major innovation that shaped the genome and the regulatory roles of DNA methylation in vertebrates. However, here we report that the marine sponge Amphimedon queenslandica, belonging to one of the earliest branching animal lineages, has evolved a hypermethylated genome with remarkable similarities to that of a vertebrate. Despite major differences in genome size and architecture, independent acquisition of hypermethylation reveal common distribution patterns and repercussions for genome regulation between both lineages. Genome wide depletion of CpGs is counterbalanced by CpG enrichment at unmethylated promoters, mirroring CpG islands. Furthermore, a subset of CpG-bearing transcription factor motifs are enriched at Amphimedon unmethylated promoters. We find that the animal-specific transcription factor NRF has conserved methyl-sensitivity over 700 million years, indicating an ancient cross-talk between transcription factors and DNA methylation. Finally, the sponge shows vertebrate-like levels of 5-hydroxymethylcytosine, the oxidative derivative of cytosine methylation involved in active demethylation. Hydroxymethylation is concentrated in regions that are enriched for transcription factor motifs and show developmentally dynamic demethylation. Together, these findings push back the links between DNA methylation and its regulatory roles to the early steps of animal evolution. Thus, the Amphimedon methylome challenges the prior hypotheses about the origins of vertebrate genome hypermethylation and its implications for regulatory complexity.
2019-08-02 | GSE124016 | GEO
Project description:Gills of teleost fish represent a vital multifunctional organ; however, they are subjected to environmental stressors, causing gill damage. Gill damage is associated with significant losses in the Atlantic salmon aquaculture industry. Gill disorders due to environmental stressors are exacerbated by global environmental changes, especially with open-net pen aquaculture (as farmed fish lack the ability to escape those events). The local and systemic response to gill damage, concurrent with several environmental insults, are not well investigated. We performed field sampling to collect gill and liver tissue after several environmental insults. Using a 44K salmonid microarray platform, we aimed to compare the transcriptomes of pristine and moderately damaged gill tissue. The gill damage-associated biomarker genes and associated qPCR assays arising from this study will be valuable in future research aimed at developing therapeutic diets to improve farmed salmon gill health.
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Project description:This SuperSeries is composed of the following subset Series: GSE22171: Pacific salmon gill samples: fate tracking in river, sampled in ocean GSE22177: Pacific salmon gill samples: fate tracking in river GSE22347: Pacific salmon gill samples: fate tracking at spawning grounds Refer to individual Series
2010-12-31 | E-GEOD-22179 | biostudies-arrayexpress
Project description:Bone is an evolutionary novelty of vertebrates, likely to have first emerged as part of ancestral dermal armor that consisted of osteogenic and odontogenic components. Whether these early vertebrate structures arose from mesoderm or neural crest cells has been a matter of considerable debate. To examine the developmental origin of the bony part of the dermal armor, we have performed in vivo lineage tracing in the sterlet sturgeon, a representative of non-teleost ray-finned fish that has retained an extensive postcranial dermal skeleton. The results definitively show that sterlet trunk neural crest cells give rise to osteoblasts of the scutes. Transcriptional profiling further reveals neural crest gene signature in sterlet scutes as well as bichir scales. Finally, histological and microCT analysis of ray-finned fish dermal armor show that their scales and scutes are formed by bone, dentin and hypermineralized covering tissues, in various combinations, that resemble those of the first armored vertebrates. Taken together, our results support a primitive skeletogenic role for the neural crest along the entire body axis, that was later progressively restricted to the cranial region during vertebrate evolution. Thus, the neural crest was a crucial evolutionary innovation driving the origin and diversification of dermal armor along the entire body axis.
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2008-12-01 | E-MEXP-1396 | biostudies-arrayexpress
Project description:The evolutionary origins of the gene network underlying cellular pluripotency, a central theme in developmental biology, have yet to be elucidated. In mammals, Oct4 is a factor crucial in the reprogramming of differentiated cells into induced pluripotent stem cells. The Oct4 and Pou2 genes evolved from a POU class V gene ancestor, but it is unknown whether pluripotency induced by Oct4 gene activity is a feature specific to mammals or was already present in ancestral vertebrates. Here we report that different vertebrate Pou2 and Oct4 homologues can induce pluripotency in mouse and human fibroblasts and that the inability of zebrafish Pou2 to establish pluripotency is not representative of all Pou2 genes, as medaka Pou2 and axolotl Pou2 are able to reprogram somatic cells into pluripotent cells. Therefore, our results indicate that induction of pluripotency is not a feature specific to mammals, but existed in the Oct4/Pou2 common ancestral vertebrate. 16 samples were analyzed Notation: O: stands for OCT4 reprogramming factor from human; o: stands for Oct4 reprogramming factor from Axolotl S: stands for SOX2 reprogramming factor from human; s: stands for SOX2 reprogramming factor from Axolotl K: stands for KLF4 reprogramming factor from human
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Project description:There is a paucity of information on the physiological changes that occur over the course of salmon early marine migration. Here we aim to provide insight on juvenile Coho salmon (Oncorhynchus kisutch) physiology using the changes in gene expression (cGRASP 44K microarray) of four tissues (brain, gill, muscle, and liver) across the parr to smolt transition in freshwater and through the first eight months of ocean residence. We also examined transcriptome changes with body size as a covariate. The strongest shift in the transcriptome for brain, gill, and muscle occurred between summer and fall in the ocean, representing physiological changes that we speculate may be associated with migration preparation to feeding areas. Metabolic processes in the liver were positively associated with body length, generally consistent with enhanced feeding opportunities. However, a notable exception to this metabolic pattern was for spring post-smolts sampled soon after entry into the ocean, which showed a pattern of gene expression more likely associated with depressed feeding or recent fasting. Overall, this study has revealed life stages that may be the most critical developmentally (fall post-smolt) and for survival (spring post-smolt) in the early marine environment. These life stages may warrant further investigation.
2019-12-03 | GSE123305 | GEO
Project description:Suspended animation (e.g. hibernation, diapause) allows organisms to survive extreme environments. But the mechanisms underlying the evolution of suspended animation states are unknown. The African turquoise killifish has evolved diapause as a form of suspended development to survive the complete drought that occurs every summer. Here, we show that gene duplicates – paralogs – exhibit specialized expression in diapause compared to normal development in the African turquoise killifish. Surprisingly, paralogs with specialized expression in diapause are evolutionarily very ancient and are present even in vertebrates that do not exhibit diapause. To determine if evolution of diapause is due to the regulatory landscape rewiring at ancient paralogs, we assessed chromatin accessibility genome-wide in fish species with or without diapause. This analysis revealed an evolutionary recent increase in chromatin accessibility at very ancient paralogs in African turquoise killifish. The increase in chromatin accessibility is linked to the presence of new binding sites for transcription factors, likely due to de novo mutations and transposable element (TE) insertion. Interestingly, accessible chromatin regions in diapause are enriched for lipid metabolism genes, and our lipidomics studies uncover a striking difference in lipid species in African turquoise killifish diapause, which could be critical for long-term survival. Together, our results show that diapause likely originated by repurposing pre-existing gene programs via recent changes in the regulatory landscape. This work raises the possibility that suspended animation programs could be reactivated in other species for long-term preservation via transcription factor remodeling and suggests a mechanism for how complex adaptations evolve in nature.
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