The evolution of the temporal program of genome replication

• Published in: Nature communications Vol. 9; no. 1; pp. 2199 - 12
• Main Authors: Agier, Nicolas, Delmas, Stéphane, Zhang, Qing, Fleiss, Aubin, Jaszczyszyn, Yan, van Dijk, Erwin, Thermes, Claude, Weigt, Martin, Cosentino-Lagomarsino, Marco, Fischer, Gilles
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 06.06.2018; Nature Publishing Group; Nature Portfolio
• Subjects: 45; 45/23; 45/77; 49; 49/22; 49/23; 49/31; 631/114/2785; 631/181/2474; 631/208/191; 64; Biological evolution; Chromosomes; Chromosomes, Fungal - genetics; Divergence; DNA Replication - genetics; DNA Replication Timing - genetics; Evolution; Evolution, Molecular; Genome, Fungal - genetics; Genomes; Humanities and Social Sciences; Life Sciences; Models, Genetic; multidisciplinary; Origins; Phylogeny; Replication; Replication Origin - genetics; Replication origins; Saccharomycetales - classification; Saccharomycetales - genetics; Science; Science (multidisciplinary); Species Specificity; Yeasts
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-018-04628-4

Genome replication is highly regulated in time and space, but the rules governing the remodeling of these programs during evolution remain largely unknown. We generated genome-wide replication timing profiles for ten Lachancea yeasts, covering a continuous evolutionary range from closely related to more divergent species. We show that replication programs primarily evolve through a highly dynamic evolutionary renewal of the cohort of active replication origins. We found that gained origins appear with low activity yet become more efficient and fire earlier as they evolutionarily age. By contrast, origins that are lost comprise the complete range of firing strength. Additionally, they preferentially occur in close vicinity to strong origins. Interestingly, despite high evolutionary turnover, active replication origins remain regularly spaced along chromosomes in all species, suggesting that origin distribution is optimized to limit large inter-origin intervals. We propose a model on the evolutionary birth, death, and conservation of active replication origins. Temporal programs of genome replication show different levels of conservation between closely or distantly related species. Here, the authors generate genome-wide replication timing profiles for ten yeast species, and analyze their evolutionary dynamics.