Differences in firing efficiency, chromatin and transcription underlie the developmental plasticity of the Arabidopsis originome

Full genome replication in eukaryotes depends on the function of thousands of DNA replication origins (ORIs) that constitute the originome. The identification of ORIs in cultured cells has served to define their basic DNA and chromatin features. However, a major challenge is to learn the biology of ORIs in adult organisms to understand their developmental plasticity. Here, we have determined the originome and chromatin landscape in Arabidopsis thaliana at two stages of vegetative development. We found that ORIs associate with multiple chromatin signatures including the most frequent at TSS but also at proximal and distal gene regulatory regions or repressed Polycomb (PcG) domains. In constitutive heterochromatin, a high fraction of ORIs colocalize with GC-rich retrotransposons. Quantitative analysis of ORI activity led us to conclude that strong ORIs possess high scores of local GC content and clusters of GGN trinucleotides that may form G quadruplexes and other G-rich structures. We also found that development primarily influences ORI firing strength rather than ORI location. Moreover, ORIs that preferentially fire at early vegetative stages colocalize with GC-rich heterochromatin whereas those at later stages associate with transcribed genes. Our study provides the first originome of an adult organism, which is a developmentally and genetically tractable, thus opening new avenues of studying the biology of ORIs in response to developmental cues, transcriptional programs, environmental challenges and mutant backgrounds.