Ordered structure of the transcription network inherited from the yeast whole-genome duplication

Abstract

Background: Gene duplication, a major evolutionary path to genomic innovation, can occur at the scale of an entire genome. One such "whole-genome duplication" (WGD) event among the Ascomycota fungi gave rise to genes with distinct biological properties compared to small-scale duplications. Results: We studied the evolution of transcriptional interactions of whole-genome duplicates, to understand how they are wired into the yeast regulatory system. Our work combines network analysis and modeling of the large-scale structure of the interactions stemming from the WGD. Conclusions: The results uncover the WGD as a major source for the evolution of a complex interconnected block of transcriptional pathways. The inheritance of interactions among WGD duplicates follows elementary "duplication subgraphs", relating ancestral interactions with newly formed ones. Duplication subgraphs are correlated with their neighbours and give rise to higher order circuits with two elementary properties: newly formed transcriptional pathways remain connected (paths are not broken), and are preferentially cross-connected with ancestral ones. The result is a coherent and connected "WGD-network", where duplication subgraphs are arranged in an astonishingly ordered configuration.