Amplification and adaptation of centromeric repeats in polyploid switchgrass species

Yang, Xueming; Zhao, Hainan; Zhang, Tao; Zeng, Zixian; Zhang, Pingdong; Zhu, Bo; Han, Yonghua; Braz, Guilherme Tomaz; Casler, Michael D.; Schmutz, Jeremy; Jiang, Jiming

doi:10.1111/nph.15098

Cited by 32 publications

(35 citation statements)

References 60 publications

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“…2014 ). Based on these findings, along with the presence of partially homogenized centromeric satellites in switchgrass species ( Yang et al. 2018 ), it was hypothesized that evolutionarily young centromeres may be repeat-free and only later accumulate random satellites that are subsequently homogenized across different chromosomes, resulting in the selection of a single, structurally favorable repeat to dominate all centromeres ( Gong et al.…”

Section: Discussionmentioning

confidence: 99%

Extraordinary Sequence Diversity and Promiscuity of Centromeric Satellites in the Legume Tribe Fabeae

Robledillo

Neumann

Koblížková

et al. 2020

Molecular Biology and Evolution

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Satellite repeats are major sequence constituents of centromeres in many plant and animal species. Within a species, a single family of satellite sequences typically occupies centromeres of all chromosomes and is absent from other parts of the genome. Due to their common origin, sequence similarities exist among the centromere-specific satellites in related species. Here, we report a remarkably different pattern of centromere evolution in the plant tribe Fabeae, which includes genera Pisum, Lathyrus, Vicia, and Lens. By immunoprecipitation of centromeric chromatin with CENH3 antibodies, we identified and characterized a large and diverse set of 64 families of centromeric satellites in 14 species. These families differed in their nucleotide sequence, monomer length (33–2,979 bp), and abundance in individual species. Most families were species-specific, and most species possessed multiple (2–12) satellites in their centromeres. Some of the repeats that were shared by several species exhibited promiscuous patterns of centromere association, being located within CENH3 chromatin in some species, but apart from the centromeres in others. Moreover, FISH experiments revealed that the same family could assume centromeric and noncentromeric positions even within a single species. Taken together, these findings suggest that Fabeae centromeres are not shaped by the coevolution of a single centromeric satellite with its interacting CENH3 proteins, as proposed by the centromere drive model. This conclusion is also supported by the absence of pervasive adaptive evolution of CENH3 sequences retrieved from Fabeae species.

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Section: Discussionmentioning

confidence: 99%

Extraordinary Sequence Diversity and Promiscuity of Centromeric Satellites in the Legume Tribe Fabeae

Robledillo

Neumann

Koblížková

et al. 2020

Molecular Biology and Evolution

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“…In addition, Robicheau et al [ 61 ] report rDNA sequences appearing at multiple sites on chromosomes without forming rDNA arrays, presence of centromere-associated rDNA hits, and divergence of these sequences to pseudogenes. Yang et al [ 62 ] even demonstrated that a 5S ribosomal RNA gene array was recruited to be the functional centromere for one of the switchgrass chromosomes, making Pv156 repeat the most enriched centromeric repeat. Thereafter, association of rDNA sequences with the centromeric region of C. gigas ( Table S2 ) is not unexpected.…”

Section: Discussionmentioning

confidence: 99%

Sequence Composition Underlying Centromeric and Heterochromatic Genome Compartments of the Pacific Oyster Crassostrea gigas

Cvitanić

Zeljko

Pasantes

et al. 2020

Genes

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Segments of the genome enriched in repetitive sequences still present a challenge and are omitted in genome assemblies. For that reason, the exact composition of DNA sequences underlying the heterochromatic regions and the active centromeres are still unexplored for many organisms. The centromere is a crucial region of eukaryotic chromosomes responsible for the accurate segregation of genetic material. The typical landmark of centromere chromatin is the rapidly-evolving variant of the histone H3, CenH3, while DNA sequences packed in constitutive heterochromatin are associated with H3K9me3-modified histones. In the Pacific oyster Crassostrea gigas we identified its centromere histone variant, Cg-CenH3, that shows stage-specific distribution in gonadal cells. In order to investigate the DNA composition of genomic regions associated with the two specific chromatin types, we employed chromatin immunoprecipitation followed by high-throughput next-generation sequencing of the Cg-CenH3- and H3K9me3-associated sequences. CenH3-associated sequences were assigned to six groups of repetitive elements, while H3K9me3-associated-ones were assigned only to three. Those associated with CenH3 indicate the lack of uniformity in the chromosomal distribution of sequences building the centromeres, being also in the same time dispersed throughout the genome. The heterochromatin of C. gigas exhibited general paucity and limited chromosomal localization as predicted, with H3K9me3-associated sequences being predominantly constituted of DNA transposons.

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“…rDNA tracts can serve as an origin of satellite repeats [ 50 , 51 ], and centromerically located satellite DNA partially derived from 5S rDNA was described, for instance, in the frog Physalaemus cuvieri [ 52 ]. Remarkably, in the switchgrass Panicum virgatum it was recently shown that one of its centromeres propagated the exact 5S rDNA unit with its completely conserved 5S rRNA gene sequence and NTS region into functional centromeric DNA, without obstructing the fundamental function of the 5S rRNA genes [ 53 ]. We believe a similar scenario could be assumed in T .…”

Section: Discussionmentioning

confidence: 99%

CenH3 distribution reveals extended centromeres in the model beetle Tribolium castaneum

et al. 2020

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Centromeres are chromosomal domains essential for kinetochore assembly and correct chromosome segregation. Inconsistent in their underlying DNA sequences, centromeres are defined epigenetically by the presence of the centromere-specific histone H3 variant CenH3. Most of the analyzed eukaryotes have monocentric chromosomes in which CenH3 proteins deposit into a single, primary constriction visible at metaphase chromosomes. Contrary to monocentrics, evolutionary sporadic holocentric chromosomes lack a primary constriction and have kinetochore activity distributed along the entire chromosome length. In this work, we identified cCENH3 protein, the centromeric H3 histone of the coleopteran model beetle Tribolium castaneum . By ChIP-seq analysis we disclosed that cCENH3 chromatin assembles upon a repertoire of repetitive DNAs. cCENH3 in situ mapping revealed unusually elongated T . castaneum centromeres that comprise approximately 40% of the chromosome length. Being the longest insect regional centromeres evidenced so far, T . castaneum centromeres are characterized by metapolycentric structure composed of several individual cCENH3-containing domains. We suggest that the model beetle T . castaneum with its metapolycentromeres could represent an excellent model for further studies of non-canonical centromeres in insects.

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Amplification and adaptation of centromeric repeats in polyploid switchgrass species

Cited by 32 publications

References 60 publications

Extraordinary Sequence Diversity and Promiscuity of Centromeric Satellites in the Legume Tribe Fabeae

Extraordinary Sequence Diversity and Promiscuity of Centromeric Satellites in the Legume Tribe Fabeae

Sequence Composition Underlying Centromeric and Heterochromatic Genome Compartments of the Pacific Oyster Crassostrea gigas

CenH3 distribution reveals extended centromeres in the model beetle Tribolium castaneum

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