An official website of the United States government
Abstract BackgroundAntarctic fishes of the Notothenioidei suborder constitutively upregulate multiple inducible chaperones, a highly derived adaptation that preserves proteostasis in extreme cold, and represent a system for studying the evolution of gene frontloading. We screened forHsf1-binding sites, asHsf1is a master transcription factor of the heat shock response, and highly-conserved non-coding elements within proximal promoters of chaperone genes across 10 Antarctic notothens, 2 subpolar notothens, and 17 perciform fishes. We employed phylogenetic models of molecular evolution to determine whether (i) changes in motifs associated withHsf1-binding and/or (ii) relaxed purifying selection or exaptation at ancestralcis-regulatory elements coincided with the evolution of chaperone frontloading in Antarctic notothens. ResultsAntarctic notothens exhibited significantly fewerHsf1-binding sites per bp at chaperone promoters than subpolar notothens and Serranoidei, the most closely-related suborder to Notothenioidei included in this study. 90% of chaperone promoters exhibited accelerated substitution rates among Antarctic notothens relative to other perciformes. The proportion of bases undergoing accelerated evolution (i) was significantly greater in Antarctic notothens than in subpolar notothens and Perciformes in 70% of chaperone genes and (ii) increased among bases that were more conserved among perciformes. Lastly, we detected evidence of relaxed purifying selection and exaptation acting on ancestrally conservedcis-regulatory elements in the Antarctic notothen lineage and its major branches. ConclusionA large degree of turnover has occurred in Notothenioidei at chaperone promoter regions that are conserved among perciform fishes following adaptation to the cooling of the Southern Ocean. Additionally, derived reductions inHsf1-binding site frequency suggestcis-regulatory modifications to the classical heat shock response. Of note, turnover events within chaperone promoters were less frequent in the ancestral node of Antarctic notothens relative to younger Antarctic lineages. This suggests thatcis-regulatory divergence at chaperone promoters may be greater between Antarctic notothen lineages than between subpolar and Antarctic clades. These findings demonstrate that strong selective forces have acted uponcis-regulatory elements of chaperone genes among Antarctic notothens.
more »
« less
Characterizing Gene Copy Number of Heat Shock Protein Gene Families in the Emerald Rockcod, Trematomus bernacchii
The suborder Notothenioidae is comprised of Antarctic fishes, several of which have lost their ability to rapidly upregulate heat shock proteins in response to thermal stress, instead adopting a pattern of expression resembling constitutive genes. Given the cold-denaturing effect that sub-zero waters have on proteins, evolution in the Southern Ocean has likely selected for increased expression of molecular chaperones. These selective pressures may have also enabled retention of gene duplicates, bolstering quantitative output of cytosolic heat shock proteins (HSPs). Given that newly duplicated genes are under more relaxed selection, it is plausible that gene duplication enabled altered regulation of such highly conserved genes. To test for evidence of gene duplication, copy number of various isoforms within major heat shock gene families were characterized via qPCR and compared between the Antarctic notothen, Trematomus bernacchii, which lost the inducible heat shock response, and the non-Antarctic notothen, Notothenia angustata, which maintains an inducible heat shock response. The results indicate duplication of isoforms within the hsp70 and hsp40 super families have occurred in the genome of T. bernacchii. The findings suggest gene duplications may have been critical in maintaining protein folding efficiency in the sub-zero waters and provided an evolutionary mechanism of alternative regulation of these conserved gene families.
more »
« less
- Award ID(s):
- 1543419
- PAR ID:
- 10604017
- Publisher / Repository:
- MDP
- Date Published:
- Journal Name:
- Genes
- Volume:
- 11
- Issue:
- 8
- ISSN:
- 2073-4425
- Page Range / eLocation ID:
- 867
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Antarctic notothenioid fishes are noteworthy for their history of isolation and indications they lack the heat shock response. The mechanistic basis for stenothermy has not been fully elucidated, and some aspects of stenothermy could arise post-transcriptionally. Antarctic emerald rockcod (Trematomus bernacchii) were sampled after exposure to chronic and/or acute high temperatures, followed by assessment of proteomic responses in brain, gill, and kidney using tissue-specific DIA assay libraries. Few cellular stress response proteins were induced, and overall responses were modest in terms of numbers of differentially expressed proteins and their fold changes. Inconsistencies in protein induction across treatments and tissues are suggestive of dysregulation, rather than an adaptive response. Changes in regulation of translation in Antarctic notothenioids could explain these patterns. Some components of the “integrative stress response” that regulates translation are highly conserved (e.g., Ser-52 of eIF2α), but the eIF2α kinases GCN2 and PERK may have evolved along different trajectories in Antarctic fishes. Together, these observations suggest a novel hypothesis for stenothermy and the absence of a coordinated cellular stress response in Antarctic fishes.more » « less
-
Abstract Gene duplication is a source of evolutionary novelty. DNA methylation may play a role in the evolution of duplicate genes (paralogs) through its association with gene expression. While this relationship has been examined to varying extents in a few individual species, the generalizability of these results at either a broad phylogenetic scale with species of differing duplication histories or across a population remains unknown. We applied a comparative epigenomic approach to 43 angiosperm species across the phylogeny and a population of 928 Arabidopsis (Arabidopsis thaliana) accessions, examining the association of DNA methylation with paralog evolution. Genic DNA methylation was differentially associated with duplication type, the age of duplication, sequence evolution, and gene expression. Whole-genome duplicates were typically enriched for CG-only gene body methylated or unmethylated genes, while single-gene duplications were typically enriched for non-CG methylated or unmethylated genes. Non-CG methylation, in particular, was a characteristic of more recent single-gene duplicates. Core angiosperm gene families were differentiated into those which preferentially retain paralogs and “duplication-resistant” families, which convergently reverted to singletons following duplication. Duplication-resistant families that still have paralogous copies were, uncharacteristically for core angiosperm genes, enriched for non-CG methylation. Non-CG methylated paralogs had higher rates of sequence evolution, higher frequency of presence–absence variation, and more limited expression. This suggests that silencing by non-CG methylation may be important to maintaining dosage following duplication and be a precursor to fractionation. Our results indicate that genic methylation marks differing evolutionary trajectories and fates between paralogous genes and have a role in maintaining dosage following duplication.more » « less
-
A gene duplication of a septin reveals a developmentally regulated filament length control mechanismSeptins are a family of conserved filament-forming proteins that function in multiple cellular processes. The number of septin genes within an organism varies, and higher eukaryotes express many septin isoforms due to alternative splicing. It is unclear if different combinations of septin proteins in complex alter the polymers’ biophysical properties. We report that a duplication event within the CDC11 locus in Ashbya gossypii gave rise to two similar but distinct Cdc11 proteins: Cdc11a and Cdc1b. CDC11b transcription is developmentally regulated, producing different amounts of Cdc11a- and Cdc11b-complexes in the lifecycle of Ashbya gossypii. Deletion of either gene results in distinct cell polarity defects, suggesting non-overlapping functions. Cdc11a and Cdc11b complexes have differences in filament length and membrane-binding ability. Thus, septin subunit composition has functional consequences on filament properties and cell morphogenesis. Small sequence differences elicit distinct biophysical properties and cell functions of septins, illuminating how gene duplication could be a driving force for septin gene expansions seen throughout the tree of life.more » « less
-
Yang, Guang (Ed.)Abstract Expression of multiple hemoglobin isoforms with differing physiochemical properties likely helps species adapt to different environmental and physiological conditions. Antarctic notothenioid fishes inhabit the icy Southern Ocean and display fewer hemoglobin isoforms, each with less affinity for oxygen than temperate relatives. Reduced hemoglobin multiplicity was proposed to result from relaxed selective pressure in the cold, thermally stable, and highly oxygenated Antarctic waters. These conditions also permitted the survival and diversification of white-blooded icefishes, the only vertebrates living without hemoglobin. To understand hemoglobin evolution during adaptation to freezing water, we analyzed hemoglobin genes from 36 notothenioid genome assemblies. Results showed that adaptation to frigid conditions shaped hemoglobin gene evolution by episodic diversifying selection concomitant with cold adaptation and by pervasive evolution in Antarctic notothenioids compared to temperate relatives, likely a continuing adaptation to Antarctic conditions. Analysis of hemoglobin gene expression in adult hematopoietic organs in various temperate and Antarctic species further revealed a switch in hemoglobin gene expression underlying hemoglobin multiplicity reduction in Antarctic fish, leading to a single hemoglobin isoform in adult plunderfishes and dragonfishes, the sister groups to icefishes. The predicted high hemoglobin multiplicity in Antarctic fish embryos based on transcriptomic data, however, raises questions about the molecular bases and physiological implications of diverse hemoglobin isoforms in embryos compared to adults. This analysis supports the hypothesis that the last common icefish ancestor was vulnerable to detrimental mutations affecting the single ancestral expressed alpha- and beta-globin gene pair, potentially predisposing their subsequent loss.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3390/genes11080867
