The H3 histone chaperone NASP^SIM3 escorts CenH3 in Arabidopsis

Abstract

SummaryCentromeres define the chromosomal position where kinetochores form to link the chromosome to microtubules during mitosis and meiosis. Centromere identity is determined by incorporation of a specific histone H3 variant termed CenH3. As for other histones, escort and deposition of CenH3 must be ensured by histone chaperones, which handle the non‐nucleosomal CenH3 pool and replenish CenH3 chromatin in dividing cells. Here, we show that the Arabidopsis orthologue of the mammalian NUCLEAR AUTOANTIGENIC SPERM PROTEIN (NASP) and Schizosaccharomyces pombe histone chaperone Sim3 is a soluble nuclear protein that binds the histone variant CenH3 and affects its abundance at the centromeres. NASPSIM3 is co‐expressed with Arabidopsis CenH3 in dividing cells and binds directly to both the N‐terminal tail and the histone fold domain of non‐nucleosomal CenH3. Reduced NASPSIM3 expression negatively affects CenH3 deposition, identifying NASPSIM3 as a CenH3 histone chaperone.

Centromeric Transcription: A Conserved Swiss-Army Knife

“…In many species, a dedicated CENP-A chaperone has been identified that performs this function. Human cells use HJURP [ 107 , 108 ] and RbAp48 [ 109 ], fruit flies use CAL1 [ 110 ], fission and budding yeast uses SCM3 [ 111 , 112 , 113 , 114 ], the holocentric roundworm Caenorhabditis elegans uses RbAp46/48 LIN-53 [ 115 ], and Arabidopsis thaliana uses NASP SIM3 [ 116 ]. Although knock-down of fruit fly 359-bp satellite RNA resulted in reduced levels of CAL1 at the centromere [ 51 ], HJURP has been shown to directly interact with α-satellite lncRNAs [ 21 ].…”

Conservation of centromeric histone 3 interaction partners in plants

“…Evidence in plants is largely missing, and only indirect indications for a role in CENH3 chaperone function are available. For instance, the interaction of NASP with both CENH3 and H3.1/H3.3 has been demonstrated ( Le Goff et al , 2020 ). HFDs of H3s and CENH3 show 50–60% sequence similarity within the same species ( Talbert and Henikoff, 2010 ).…”

“…An ortholog of NASP identified in A. thaliana shows H3 chaperone activity ( Maksimov et al , 2016 ). NASP also binds CENH3, and NASP down-regulation impairs the loading of CENH3 at the centromeres ( Le Goff et al , 2020 ). An HJURP-like CENH3-selective chaperone has hitherto not been identified in plants.…”

Looking At the Past and Heading to the Future: Meeting Summary of the 6th European Workshop on Plant Chromatin 2019 in Cologne, Germany

“…Inna Lermontova (Gatersleben, Germany) reported on the collaborative effort to search for histone CenH3 interactors and the identification of the plant homologue of NUCLEAR AUTOANTIGENIC SPERM PROTEIN (NASP) as a CenH3 binding protein. Previously shown to bind histone H3 monomers or H3-H4 dimers (Maksimov et al, 2016), the nuclear NASP protein interacts both with the N-terminal tail as well as with the histone fold domain of CenH3 and reduced NASP expression negatively affects CenH3 levels, suggesting that NASP functions as a CenH3 escort protein (Le Goff et al, 2019).…”