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Gene duplication promotes adaptive evolution in two main ways: allowing one duplicate to evolve a new function and splitting ancestral functions between the duplicates. The second scenario may resolve adaptive conflicts that can rise when one gene performs different functions. In an apparent departure from both scenarios, low-expressing transcription factor (TF) duplicates commonly bind to the same DNA motifs and act in overlapping conditions. To examine for possible benefits of this apparent redundancy, we examined the Msn2 and Msn4 duplicates in budding yeast. We show that Msn2,4 function as one unit by inducing the same set of target genes in overlapping conditions. Yet, the two-factor composition allows this unit’s expression to be both environmentally responsive and with low noise, resolving an adaptive conflict that limits expression of single genes. We propose that duplication can provide adaptive benefit through cooperation rather than functional divergence, allowing two-factor dynamics with beneficial properties that cannot be achieved by a single gene.

No abstract

Transcription factors (TFs) regulate gene expression by binding DNA sequences recognized by their DNA-binding domains (DBDs). DBD-recognized motifs are short and highly abundant in genomes. The ability of TFs to bind a specific subset of motif-containing sites, and to do so rapidly upon activation, is fundamental for gene expression in all eukaryotes. Despite extensive interest, our understanding of the TF-target search process is fragmented; although binding specificity and detection speed are two facets of this same process, trade-offs between them are rarely addressed. In this opinion article, we discuss potential speed-specificity trade-offs in the context of existing models. We further discuss the recently described 'distributed specificity' paradigm, suggesting that intrinsically disordered regions (IDRs) promote specificity while reducing the TF-target search time.

Gene duplication promotes adaptive evolution in two principle ways: allowing one duplicate to evolve a new function and resolving adaptive conflicts by splitting ancestral functions between the duplicates. In an apparent departure from both scenarios, low-expressing transcription factor (TF( duplicates commonly regulate similar sets of genes and act in overlapping conditions. To examine for possible benefits of such apparently redundant duplicates, we examined the budding yeast duplicated stress regulators Msn2 and Msn4. We show that Msn2,4 indeed function as one unit, inducing the same set of target genes in overlapping conditions, yet this two-factor composition allows its expression to be both environmental-responsive and with low-noise, thereby resolving an adaptive conflict that inherently limits expression of single genes. Our study exemplified a new model for evolution by gene duplication whereby duplicates provide adaptive benefit through cooperation, rather than functional divergence: attaining two-factor dynamics with beneficial properties that cannot be achieved by a single gene.