Transcriptomic and genomic evolution under constant cold in Antarctic notothenioid fish

Abstract

The antifreeze glycoprotein-fortified Antarctic notothenioid fishes comprise the predominant fish suborder in the isolated frigid Southern Ocean. Their ecological success undoubtedly entailed evolutionary acquisition of a full suite of cold-stable functions besides antifreeze protection. Prior studies of adaptive changes in these teleost fishes generally examined a single genotype or phenotype. We report here the genome-wide investigations of transcriptional and genomic changes associated with Antarctic notothenioid cold adaptation. We sequenced and characterized 33,560 ESTs from four tissues of the Antarctic notothenioid Dissostichus mawsoni and derived 3,114 nonredundant protein gene families and their expression profiles. Through comparative analyses of same-tissue transcriptome profiles of D. mawsoni and temperate/tropical teleost fishes, we identified 177 notothenioid protein families that were expressed many fold over the latter, indicating cold-related up-regulation. These up-regulated gene families operate in protein biosynthesis, protein folding and degradation, lipid metabolism, antioxidation, antiapoptosis, innate immunity, choriongenesis, and others, all of recognizable functional importance in mitigating stresses in freezing temperatures during notothenioid life histories. We further examined the genomic and evolutionary bases for this expressional up-regulation by comparative genomic hybridization of DNA from four pairs of Antarctic and basal non-Antarctic notothenioids to 10,700 D. mawsoni cDNA probes and discovered significant to astounding (3-to >300-fold, P < 0.05) Antarctic-specific duplications of 118 protein-coding genes, many of which correspond to the up-regulated gene families. Results of our integrative tripartite study strongly suggest that evolution under constant cold has resulted in dramatic genomic expansions of specific protein gene families, augmenting gene expression and gene functions contributing to physiological fitness of Antarctic notothenioids in freezing polar conditions. cold adaptation ͉ comparative genomics ͉ gene duplication ͉ genome evolution ͉ retrotransposon

Molecular basis and genetic improvement of economically important traits in aquaculture animals

“…To identify candidate cold tolerance-related and cold change-related genes, a large-scale EST sequencing of multi-tissues including brain, liver, head kidney, and ovary had been performed in Antarctic notothenioid (Dissostichus mawsoni), and some important cold-specific expressed genes had been identified by comparative transcriptome analyses between D. mawsoni and non-notothenioid warm-water teleost fishes [133,134]. Moreover, the molecular origination of antifreeze protein III (AFP III) was demonstrated to come from a duplicate copy of sialic acid synthase (SAS) gene, supporting the evolutionary mechanism by neofunctionalization under escape from adaptive conflict [135].…”

Copious copies keep out the cold

“…They employed array comparative genomic hybridizations (aCGH) to compare gene copy number at 10 700 loci in three Antarctic and two non-Antarctic notothenioid fishes. Using a hybridization threshold ratio set for a single, known, gene duplication event between two of these species, Chen et al (2008) identified 101 protein-coding genes for which the average hybridization ratio across the cold-adapted species was above this threshold-indicating likely gene duplication. These candidate loci include 15 with potential activity in cold response, and many that were also among those upregulated in D. mawsoni relative to temperate species according to the EST analysis ( Figure 1).…”

“…These candidate loci include 15 with potential activity in cold response, and many that were also among those upregulated in D. mawsoni relative to temperate species according to the EST analysis ( Figure 1). It is perhaps unusual to apply a threshold analysis technique to this experiment, as Chen et al (2008) do, rather than a statistical analysis that is more appropriate to the hybridization design. A more rigorous statistical analysis of aCGH results would help to quantify hybridization variation within and between species and ecotypes (for example, Emerson et al, 2008).…”

“…Previous studies have typically investigated single genes or phenotypes, such as antifreeze proteins, but in an exciting new survey, Chen et al (2008) take a novel approach to characterizing the genome-wide changes in gene duplication and transcription, relating these to adaptation to the cold Antarctic waters. The broad implications and excitement generated by this research are because of its tripartite approach.…”

“…Chen et al (2008) used unnormalized libraries in order to quantify EST (expressed sequence tag) abundance, and this revealed a highly biased transcription pattern, beyond ordinary expectations for simple tissue specificity. They identified a small number of dominant transcripts in each tissue, and a transcriptional shift towards a functional theme that suggests an elevated stress response.…”