Evolution of Stress-Regulated Gene Expression in Duplicate Genes of Arabidopsis thaliana

Abstract

Due to the selection pressure imposed by highly variable environmental conditions, stress sensing and regulatory response mechanisms in plants are expected to evolve rapidly. One potential source of innovation in plant stress response mechanisms is gene duplication. In this study, we examined the evolution of stress-regulated gene expression among duplicated genes in the model plant Arabidopsis thaliana. Key to this analysis was reconstructing the putative ancestral stress regulation pattern. By comparing the expression patterns of duplicated genes with the patterns of their ancestors, duplicated genes likely lost and gained stress responses at a rapid rate initially, but the rate is close to zero when the synonymous substitution rate (a proxy for time) is >∼0.8. When considering duplicated gene pairs, we found that partitioning of putative ancestral stress responses occurred more frequently compared to cases of parallel retention and loss. Furthermore, the pattern of stress response partitioning was extremely asymmetric. An analysis of putative cis-acting DNA regulatory elements in the promoters of the duplicated stress-regulated genes indicated that the asymmetric partitioning of ancestral stress responses are likely due, at least in part, to differential loss of DNA regulatory elements; the duplicated genes losing most of their stress responses were those that had lost more of the putative cis-acting elements. Finally, duplicate genes that lost most or all of the ancestral responses are more likely to have gained responses to other stresses. Therefore, the retention of duplicates that inherit few or no functions seems to be coupled to neofunctionalization. Taken together, our findings provide new insight into the patterns of evolutionary changes in gene stress responses after duplication and lay the foundation for testing the adaptive significance of stress regulatory changes under highly variable biotic and abiotic environments.

The developmental transcriptome of contrasting Arctic charr (Salvelinus alpinus) morphs

“…The downside is that paralog-specific expression patterns are masked, as our qPCR results of the natterin like gene family show ( Figure 3 and S1 Figure). Recent rainbow trout data shows most paralogs from the latest whole genome duplication event retain the same expression pattern 32 indicating that this scenario is probably uncommon; hence it is of considerable interest when two paralogs show distinct expression patterns 82 . In their analysis of the Arctic charr gill transcriptome, Norman et al (2014) 16 also used Illumina sequencing technology to evaluate expression.…”

Adaptive evolution of duplicated hsp17 genes in wild barley from microclimatically divergent sites of Israel

“…An evolutionary consequence for duplicated loci was referred to as subfunctionalization (Moore and Purugganan, 2005). Recently, the models involving epigenetic silencing of duplicate genes or purifying selection for gene balance have also been proposed (Zou et al 2009). …”

“…The generation of new evolutionary novelties will lead to environmental adaptations. Most studies on the evolution of gene duplications focus on examining whole-genome duplications of model organisms (Zou et al, 2009) and the macroevolutionary patterns of gene diversification (Hanada et al, 2008). In contrast, we know very little about the relative importance of the two evolutionary forces, neutral genetic drift and positive selection, which shape the ultimate functional fate of the duplicate gene pair (Moore and Purugganan, 2005).…”

Life at the extreme: lessons from the genome

“…Tandem duplications seem to have a more important role in shaping genomes for stress adaptations than polyploidy, segmental transposition-duplications, or ectopic duplication and translocation [40]; recombination and tandem duplication events may both become accelerated by environmental challenges [29]. As the result of unequal crossing-over during recombination, tandem duplications vary in their 'genetic neighborhoods', with copies receiving different regulatory motifs that can lead to drastic changes in expression [40].…”

“…As the result of unequal crossing-over during recombination, tandem duplications vary in their 'genetic neighborhoods', with copies receiving different regulatory motifs that can lead to drastic changes in expression [40]. A comparative study on plant genomes ranging from Arabidopsis to Physcomitrella showed genes associated with defense, transport functions, or abiotic stress responses enriched in tandem duplicates, whereas duplicates due to other mechanisms included genes enriched in other intracellular regulatory roles [41].…”