Chromatin binding by HORMAD proteins regulates meiotic recombination initiation

Milano, Carolyn R.; Ur, Sarah N.; Gu, Yajie; Zhang, Jessie; Allison, Rachal; Brown, George; Neale, Matthew J.; Tromer, Eelco C.; Corbett, Kevin D.; Hochwagen, Andreas

doi:10.1038/s44318-024-00034-3

Title: Chromatin binding by HORMAD proteins regulates meiotic recombination initiation

Journal Article · 08 February 2024 · The EMBO Journal (Online)

DOI: https://doi.org/10.1038/s44318-024-00034-3 · OSTI ID:2471065

Milano, Carolyn R. ^[1]; Ur, Sarah N. ^[2];

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New York Univ. (NYU), NY (United States)
Univ. of California, San Diego, La Jolla, CA (United States); Vividion Therapeutics, San Diego, CA (United States)
Univ. of California, San Diego, La Jolla, CA (United States)
Univ. of Sussex, Brighton (United Kingdom)
Univ. of Groningen (Netherlands)

The meiotic chromosome axis coordinates chromosome organization and interhomolog recombination in meiotic prophase and is essential for fertility. In S. cerevisiae, the HORMAD protein Hop1 mediates the enrichment of axis proteins at nucleosome-rich islands through a central chromatin-binding region (CBR). Here, we use cryoelectron microscopy to show that the Hop1 CBR directly recognizes bent nucleosomal DNA through a composite interface in its PHD and winged helix–turn–helix domains. Targeted disruption of the Hop1 CBR-nucleosome interface causes a localized reduction of axis protein binding and meiotic DNA double-strand breaks (DSBs) in axis islands and leads to defects in chromosome synapsis. Synthetic effects with mutants of the Hop1 regulator Pch2 suggest that nucleosome binding delays a conformational switch in Hop1 from a DSB-promoting, Pch2-inaccessible state to a DSB-inactive, Pch2-accessible state to regulate the extent of meiotic DSB formation. Phylogenetic analyses of meiotic HORMADs reveal an ancient origin of the CBR, suggesting that the mechanisms we uncover are broadly conserved.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). Advanced Light Source (ALS)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2471065

Journal Information:: The EMBO Journal (Online), Journal Name: The EMBO Journal (Online) Journal Issue: 5 Vol. 43; ISSN 1460-2075

Publisher:: EMBO PressCopyright Statement

Country of Publication:: United States

Language:: English

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59 BASIC BIOLOGICAL SCIENCES
Budding Yeast
Chromatin
Chromosome Segregation
HORMA
Meiosis

Title: Chromatin binding by HORMAD proteins regulates meiotic recombination initiation

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