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Adaptive Variation and Genetic Processes

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In his immortal work “On the Origin of Species, by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life”, Chapter V, Charles Darwin summarized that though variation is essential in generation of the morphological innovations either in domestic or in wild creatures, “our ignorance of the laws of variation is profound”. After 150 years, this situation was undoubtedly improved.

The development of modern genetics and genomics has demonstrated that evolution is a two-step process: initially mutations and recombination in nucleic acid sequences occurred and led to phenotypic changes, and then if these genetic alterations have selective superiority or are subject to genetic drift, they would be eventually fixed in populations and contributed to the origin of species. Needless to say, understanding “the law of (genetic) variation” governing phenotypic adaptation of organisms has been and will be one of the central topics in evolutionary biology as well as in genetics. During the past three decades, the study on molecular basis of evolution has proposed that it is the regulatory genes, rather than the structural genes, that play more important roles during the origin and adaptation of species.

Albeit remaining in debate, the interdisciplinary field of evolution-development (so-called “Evo-Devo”) was initiated under this “regulatory thinking”, aiming at a new synthesis of biology to answer the fundamental question on how adaptive variation is determined by genetic processes. In this area, the evolution of transcription regulation received more attention because the RNA polymerase (RNAP) directed RNA biosynthesis is essential to all kinds of organisms. Studies have revealed that evolution in transcription regulation can give rise to new phenotypes. Taking advantage from the recent development of high-throughput methodologies, such as ChIP-seq, ChIP-chip, massively parallel sequencing and two-dimension gel electrophoresis, a global view of the evolution of transcription regulation has been established, especially in animal and yeast, as being elegantly reviewed elsewhere. Recent experiments revealed large-scale differences in the transcription regulons of related species, yet little is known about the genetic basis underlying the evolution of gene expression and its contribution to phenotypic diversity. The hemiascomycete lineage emerged as a central paradigm for studying the genetic basis of phenotypic diversity. Despite a strong conservation of gene content, yeast species exhibit major phenotypic differences. For example, lets consider the requirements for oxygen in hemiascomycete. Growth of most yeast species requires oxygen; S. cerevisiae grows rapidly in its absence and prefers to ferment glucose anaerobically even when oxygen is present. Many reports have suggested that rewiring in transcriptional factor leads to such conflict adaptations in different species and gives them a unique character. Some studies also suggest that these rewiring events are random.

Although previous studies have revealed many mysteries of rewiring for instant Mallick and Whiteway showed how regulatory connections local to rewired TFs could change to preserve gene target expression patterns (for example, recruitment of IFH1-FHL1 to ribosomal gene targets is maintained in both systems). Yet, there are several aspects of regulatory rewiring that are poorly understood. For instance, (i) How widespread is a wholesale shift in transcriptional regulation of a regulon? (ii) What are the features of target genes that make them amenable to rewiring? (iii) What characterizes rewired TFs? Etc. We can potentially answer some of these questions and gain further insights into conditions conducive to rewiring, as well as enable discovery of clade/species-specific instances of regulatory innovation. Our results might shed new light on the genetic mechanisms underlying the large-scale evolution of transcriptional networks.

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