Evolution of histone 2A for chromatin compaction in eukaryotes

Author:

Macadangdang Benjamin R12,Oberai Amit1,Spektor Tanya1,Campos Oscar A12,Sheng Fang1,Carey Michael F12,Vogelauer Maria1,Kurdistani Siavash K1234

Affiliation:

1. Department of Biological Chemistry, University of California, Los Angeles, Los Angeles, United States

2. Molecular Biology Institute, University of California, Los Angeles, Los Angeles, United States

3. Department of Pathology and Laboratory Medicine, University of California, Los Angeles, Los Angeles, United States

4. Eli and Edythe Broad Center of Regenerative Medicine and Stem Cell Research, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, United States

Abstract

During eukaryotic evolution, genome size has increased disproportionately to nuclear volume, necessitating greater degrees of chromatin compaction in higher eukaryotes, which have evolved several mechanisms for genome compaction. However, it is unknown whether histones themselves have evolved to regulate chromatin compaction. Analysis of histone sequences from 160 eukaryotes revealed that the H2A N-terminus has systematically acquired arginines as genomes expanded. Insertion of arginines into their evolutionarily conserved position in H2A of a small-genome organism increased linear compaction by as much as 40%, while their absence markedly diminished compaction in cells with large genomes. This effect was recapitulated in vitro with nucleosomal arrays using unmodified histones, indicating that the H2A N-terminus directly modulates the chromatin fiber likely through intra- and inter-nucleosomal arginine–DNA contacts to enable tighter nucleosomal packing. Our findings reveal a novel evolutionary mechanism for regulation of chromatin compaction and may explain the frequent mutations of the H2A N-terminus in cancer.

Funder

National Institutes of Health

Howard Hughes Medical Institute

University of California

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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