Repeat-based holocentromeres influence genome architecture and karyotype evolution

Hofstatter, Paulo G.; Thangavel, Gokilavani; Lux, Thomas; Neumann, Pavel; Vondrak, Tihana; Novák, Petr; Zhang, Meng; Costa, Lucas; Castellani, Marco; Scott, Alison Dawn; Fuchs, Joerg; Mata-Sucre, Yennifer; Dias, Yhanndra; Vanzela, André Luís Laforga; Huettel, Bruno; Šimková, Hana; Souza, Gustavo; Pedrosa‐Harand, Andrea; Macas, Jiří; Mayer, Klaus; Houben, Andreas; Marques, André

doi:10.1016/j.cell.2022.06.045

Cited by 73 publications

(194 citation statements)

References 99 publications

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“…This pattern of centromere definition via transcriptional inactivity is seen in both C. elegans and in the CenH3-devoid Bombyx mori ( Gassmann et al 2012 ; Steiner and Henikoff 2014 ; Senaratne et al 2021 ). In contrast, some holocentric species like Meloidogyne nematodes and Rhynchospora plants localize their CenH3 proteins to specific repeats found distributed over the genome ( Marques et al 2015 ; Despot-Slade et al 2021 ; Hofstatter et al 2022 ).…”

Section: Discussionmentioning

confidence: 99%

Recurrent but Short-Lived Duplications of Centromeric Proteins in HolocentricCaenorhabditisSpecies

Caro

Raman

Steiner

et al. 2022

Molecular Biology and Evolution

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Centromeric histones (CenH3s) are essential for chromosome inheritance during cell division in most eukaryotes. CenH3 genes have rapidly evolved and undergone repeated gene duplications and diversification in many plant and animal species. In Caenorhabditis species, two independent duplications of CenH3 (named hcp-3 for HoloCentric chromosome-binding Protein 3) were previously identified in C. elegans and C. remanei. Using phylogenomic analyses in thirty-two Caenorhabditis species, we find strict retention of the ancestral hcp-3 gene and ten independent duplications. Most hcp-3L (hcp-3-like) paralogs are only found in 1-2 species, are expressed in both males and females/hermaphrodites, and encode histone fold domains with 69-100% identity to ancestral hcp-3. We identified novel N-terminal protein motifs, including putative kinetochore protein-interacting motifs and a potential separase cleavage site, which are well conserved across Caenorhabditis HCP-3 proteins. Other N-terminal motifs vary in their retention across paralogs or species, revealing potential sub-functionalization or functional loss following duplication. An N-terminal extension in the hcp-3L gene of C. afra revealed an unprecedented protein fusion, where hcp-3L fused to duplicated segments from hcp-4 (nematode CENP-C). By extending our analyses beyond CenH3, we found gene duplications of six inner and outer kinetochore genes in Caenorhabditis, which appear to have been retained independent of hcp-3 duplications. Our findings suggest that centromeric protein duplications occur frequently in Caenorhabditis nematodes, are selectively retained for short evolutionary periods, then degenerate or are lost entirely. We hypothesize that unique challenges associated with holocentricity in Caenorhabditis may lead to this rapid ‘revolving door’ of kinetochore protein paralogs.

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Section: Discussionmentioning

confidence: 99%

Recurrent but Short-Lived Duplications of Centromeric Proteins in HolocentricCaenorhabditisSpecies

Caro

Raman

Steiner

et al. 2022

Molecular Biology and Evolution

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“…On the other hand, several satDNA families accumulate in CEN6, forming long arrays, some of which are associated with CENH3. Arrays of centromeric satellites up to several megabasepairs in length are typical of monocentric chromosomes, whereas holocentric chromosomes either lack CENH3-associated satellites (Heckmann et al 2013) or have them distributed as multiple short arrays across their length (Hofstatter et al 2022).…”

Section: Discussionmentioning

confidence: 99%

“…In plants, complete centromere assemblies have been constructed only for monocentric species to date, including maize (Liu et al 2020; Hufford et al 2021), rice (Song et al 2021) and Arabidopsis thaliana (Naish et al 2021; Wang et al 2022). In addition, high-quality assemblies of three holocentric species belonging to the Rhynchospora genus recently became available (Hofstatter et al 2022). Here, we report the assembly of a genomic region representing yet another type of centromere organization, namely metapolycentromere, in the pea cultivar Cameor.…”

Section: Discussionmentioning

confidence: 99%

“…Monocentric chromosomes are generally characterized by an uneven distribution of genomic features along their length, with centromeric and pericentromeric regions showing greater repetitive DNA accumulation, lower gene density, and different epigenetic profiles than the chromosome arms. By contrast, holocentric chromosomes show a more homogeneous distribution of repeats, genes, and histone modifications (Hofstatter et al 2022). For example, during mitosis, histone H2A phosphorylation at Thr120 (H2AT120ph) is detected across almost the entire length of holocentric chromosomes but is restricted to the (peri)centromeres in monocentric chromosomes (Schubert et al 2020).…”

Section: Discussionmentioning

confidence: 99%

“…However, compared with rice, the CENH3 domains in the pea CEN6 metapolycentromere are much more widely spaced and are all confined to satDNA arrays. Another mechanism, based on the mobilization of CENH3-associated centromeric satellite Tyba by Helitron elements, has been proposed to facilitate the spread of centromeric chromatin in holocentric Rhynchospora species (Hofstatter et al 2022). However, this is unlikely to occur in pea centromeres because CENH3-associated satellites in the pea genome are organized in a few large arrays, unlike the centromeric satellites of Rhynchospora , which exist as a large number of scattered and much shorter loci that may be embedded in functional Helitron elements.…”

Section: Discussionmentioning

confidence: 99%

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Assembly of the 81.6 Mb centromere of pea chromosome 6 elucidates the structure and evolution of metapolycentric chromosomes

Macas

Robledillo

Kreplak

et al. 2022

Preprint

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Centromeres in the legume genera Pisum and Lathyrus exhibit unique morphological characteristics, including extended primary constrictions and multiple separate domains of centromeric chromatin. These so-called metapolycentromeres resemble an intermediate form between monocentric and holocentric types, and therefore provide a great opportunity for studying the transitions between different types of centromere organizations. However, because of the exceedingly large and highly repetitive nature of metapolycentromeres, highly contiguous assemblies needed for these studies are lacking. Here, we report on the assembly and analysis of a 177.6 Mb region of pea (Pisum sativum) chromosome 6, including the 81.6 Mb centromere region (CEN6) and adjacent chromosome arms. Genes, DNA methylation profiles, and most of the repeats were uniformly distributed within the centromere, and their densities in CEN6 and chromosome arms were similar. The exception was an accumulation of satellite DNA in CEN6, where it formed multiple arrays up to 2 Mb in length. Centromeric chromatin, characterized by the presence of the CENH3 protein, was predominantly associated with arrays of three different satellite repeats; however, five other satellites present in CEN6 lacked CENH3. The presence of CENH3 chromatin was found to determine the spatial distribution of the respective satellites during the cell cycle. Finally, oligo-FISH painting experiments, performed using probes specifically designed to label the genomic regions corresponding to CEN6 in Pisum, Lathyrus, and Vicia species, revealed that metapolycentromeres evolved via the expansion of centromeric chromatin into neighboring chromosomal regions and the accumulation of novel satellite repeats. However, in some of these species, centromere evolution also involved chromosomal translocations and centromere repositioning.

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Centromere diversity: How different repeat‐based holocentromeres may have evolved

Kuo,

Schubert,

Marques

et al. 2024

BioEssays

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In addition to monocentric eukaryotes, which have a single localized centromere on each chromosome, there are holocentric species, with extended repeat‐based or repeat‐less centromeres distributed over the entire chromosome length. At least two types of repeat‐based holocentromeres exist, one composed of many small repeat‐based centromere units (small unit‐type), and another one characterized by a few large centromere units (large unit‐type). We hypothesize that the transposable element‐mediated dispersal of hundreds of short satellite arrays formed the small centromere unit‐type holocentromere in Rhynchospora pubera. The large centromere unit‐type of the plant Chionographis japonica is likely a product of simultaneous DNA double‐strand breaks (DSBs), which initiated the de novo formation of repeat‐based holocentromeres via insertion of satellite DNA, derived from extra‐chromosomal circular DNAs (eccDNAs). The number of initial DSBs along the chromosomes must be higher than the number of centromere units since only a portion of the breaks will have incorporated eccDNA at an appropriate position to serve as future centromere unit sites. Subsequently, preferential incorporation of the centromeric histone H3 variant at these positions is assumed. The identification of repeat‐based holocentromeres across lineages will unveil the centromere plasticity and elucidate the mechanisms underlying the diverse formation of holocentromeres.

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Repeat-based holocentromeres influence genome architecture and karyotype evolution

Cited by 73 publications

References 99 publications

Recurrent but Short-Lived Duplications of Centromeric Proteins in HolocentricCaenorhabditisSpecies

Recurrent but Short-Lived Duplications of Centromeric Proteins in HolocentricCaenorhabditisSpecies

Assembly of the 81.6 Mb centromere of pea chromosome 6 elucidates the structure and evolution of metapolycentric chromosomes

Centromere diversity: How different repeat‐based holocentromeres may have evolved

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