Old cogs, new tricks: the evolution of gene expression in a chromatin context

• Published in: Nature reviews. Genetics Vol. 20; no. 5; pp. 283 - 297
• Main Authors: Talbert, Paul B., Meers, Michael P., Henikoff, Steven
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.05.2019; Nature Publishing Group
• Subjects: 631/181/2474; 631/208/176/1988; 631/208/199; 631/208/200; 631/337/100; 631/337/100/101; 631/337/100/102; 631/337/100/1701; 631/337/100/2285; 631/337/100/2286; Agriculture; Animal Genetics and Genomics; Animals; Biological Evolution; Biomedical and Life Sciences; Biomedicine; Cancer Research; Chromatin; Chromatin Assembly and Disassembly; Chromosomal Proteins, Non-Histone - genetics; Chromosomal Proteins, Non-Histone - history; Chromosomal Proteins, Non-Histone - metabolism; Deoxyribonucleic acid; DNA; DNA - genetics; DNA - history; DNA - metabolism; Eukaryotes; Eukaryotic Cells - cytology; Eukaryotic Cells - metabolism; Evolution; Evolutionary genetics; Gene expression; Gene Function; Gene regulation; Genetic aspects; Genetic regulation; Genetic research; Genome; Genomes; Genomics - methods; Histones - genetics; Histones - history; Histones - metabolism; History, 21st Century; History, Ancient; Human Genetics; Humans; Molecular modelling; Nucleosomes; Nucleosomes - chemistry; Nucleosomes - genetics; Nucleosomes - metabolism; Observations; Prokaryotes; Prokaryotic Cells - cytology; Prokaryotic Cells - metabolism; Properties; Review Article; Transcription factors; Transcription Factors - genetics; Transcription Factors - history; Transcription Factors - metabolism; Transcription, Genetic; United States
• ISSN: 1471-0056; 1471-0064; 1471-0064
• DOI: 10.1038/s41576-019-0105-7

Sophisticated gene-regulatory mechanisms probably evolved in prokaryotes billions of years before the emergence of modern eukaryotes, which inherited the same basic enzymatic machineries. However, the epigenomic landscapes of eukaryotes are dominated by nucleosomes, which have acquired roles in genome packaging, mitotic condensation and silencing parasitic genomic elements. Although the molecular mechanisms by which nucleosomes are displaced and modified have been described, just how transcription factors, histone variants and modifications and chromatin regulators act on nucleosomes to regulate transcription is the subject of considerable ongoing study. We explore the extent to which these transcriptional regulatory components function in the context of the evolutionarily ancient role of chromatin as a barrier to processes acting on DNA and how chromatin proteins have diversified to carry out evolutionarily recent functions that accompanied the emergence of differentiation and development in multicellular eukaryotes. Eukaryotes differ substantially from bacteria and archaea owing to their nucleosome-based packaging of DNA. In this Review, Talbert, Meers and Henikoff place gene regulation in an evolutionary context by discussing how the emergence and diversification of eukaryotic chromatin provided both challenges and opportunities for intricate mechanisms of gene regulation in eukaryotes.