Conservation of core gene expression in vertebrate tissues

Abstract

C Co on ns se er rv va at ti io on n o of f c co or re e g ge en ne e e ex xp pr re es ss si io on n i in n v ve er rt te eb br ra at te e t ti is ss su ue es s Esther T Chan* ¶ , Gerald T Quon † ¶ , Gordon Chua ‡ ¶¥ , Tomas Babak ¶# , Miles Trochesset † ‡ , Ralph A Zirngibl*, Jane Aubin*, Michael JH Ratcliffe § , Andrew Wilde*, Michael Brudno † ‡ ¶ , Quaid D Morris* † ‡ ¶ and Timothy R Hughes* ‡ ¶ A Ab bs st tr ra ac ct t B Ba ac ck kg gr ro ou un nd d Vertebrates share the same general body plan and organs, possess related sets of genes, and rely on similar physiological mechanisms, yet show great diversity in morphology, habitat and behavior. Alteration of gene regulation is thought to be a major mechanism in phenotypic variation and evolution, but relatively little is known about the broad patterns of conservation in gene expression in non-mammalian vertebrates.R Re es su ul lt ts s We measured expression of all known and predicted genes across twenty tissues in chicken, frog and pufferfish. By combining the results with human and mouse data and considering only ten common tissues, we have found evidence of conserved expression for more than a third of unique orthologous genes. We find that, on average, transcription factor gene expression is neither more nor less conserved than that of other genes. Strikingly, conservation of expression correlates poorly with the amount of conserved nonexonic sequence, even using a sequence alignment technique that accounts for non-collinearity in conserved elements. Many genes show conserved human/fish expression despite having almost no nonexonic conserved primary sequence.C Co on nc cl lu us si io on ns s There are clearly strong evolutionary constraints on tissue-specific gene expression. A major challenge will be to understand the precise mechanisms by which many gene expression patterns remain similar despite extensive cis-regulatory restructuring. [5] initially posited that phenotypic differences among primates are mainly due to adaptive changes in gene regulation, rather than to changes in protein-coding sequence or function, and this idea has accumulated supporting evidence in recent years [6][7][8][9][10][11][12]. Recent work has indicated that gene expression evolves in a fashion similar to other traits, where in the absence of selection, random mutations introduce variants within a population [11,[13][14][15][16][17][18][19]. Changes negatively affecting fitness are probably eliminated by purifying selection: core cellular processes seem to be coexpressed from yeast to human [20], and conservation of the expression of individual genes in specific tissues has been observed across distantly related vertebrates [21][22][23][24], perhaps reflecting requirements for patterning and development as well as conserved functions of organs, tissues and cell types. Conversely, changes that benefit fitness (for example, under new ecological pressures) may become fixed: changes in gene expression are believed to underlie many differences in morphology, physiology and behavior...

Contrasting genetic paths to morphological and physiological evolution

“…4D). These caveats being said, it is interesting to note that our finding of faster expression evolution but slower cis-regulatory evolution of morphogenes than physiogenes is consistent with the observation of poor correlation between cis-element changes and expression divergence in yeasts and vertebrates (32,33). The relative contributions of cis-and trans-changes to gene expression evolution have been examined in yeast at the genomic scale (34).…”

Beyond the ENCODE project: using genomics and epigenomics strategies to study enhancer evolution

“…The other important aspect of the correlation between regulatory divergence and gene expression is that the latter has been shown to be largely conserved across vertebrates [59][60][61]. Although it is possible that the small fraction of conserved binding events is responsible for conserved expression patterns, with the majority of non-conserved events providing species-specific regulation, the observation of small numbers of conserved targets [17,19] challenges this hypothesis.…”

Comparative Network Analysis Reveals That Tissue Specificity and Gene Function Are Important Factors Influencing the Mode of Expression Evolution in Arabidopsis and Rice

“…As in vertebrates (Chan et al, 2009), in Arabidopsis and rice many genes show tissue specificity as well as expression conservation (e.g. AT3G04700, AT3G17060, GATL4, AMS, and AG in flower; AT4G31830, AT2G28420, AT1G05510, AT3G12960, and ATOEP16-2 in seed; AT1G30870 in root).…”