Synthetic maize centromeres transmit chromosomes across generations

Dawe, R. Kelly; Gent, Jonathan I.; Zeng, Yibing; Zhang, Han; Fu, Fangfang; Wang, Na; Kim, Dong Won; Swentowsky, Kyle W.; Liu, Jianing; Piri, Rebecca D.

doi:10.1101/2022.09.19.508542

Cited by 5 publications

(9 citation statements)

References 61 publications

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“…Some centromeres do not appear to be composed of one or many clear tandem repeats and their harmonics; instead, they are made up of clusters of retrotransposons. Zea mays (Dawe et al ., 2023) and Triticum monococcum (bread wheat and einkorn wheat (Ahmed et al ., 2023)) are examples of such centromeres (Figure 5E and F). The blur in the Fourier transform implies that the repetitive sequences vary considerably in length.…”

Section: Resultsmentioning

confidence: 99%

RepeatOBserver: tandem repeat visualization and centromere detection

Elphinstone,

Todesco

et al. 2023

Preprint

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Tandem repeats can play an important role in centromere structure, subtelomeric regions, DNA methylation, recombination, and the regulation of gene activity. There is a growing need for bioinformatics tools that can visualize and explore chromosome-scale repeats. Here we present RepeatOBserver, a new tool for visualizing tandem repeats and clustered transposable elements and for identifying potential natural centromere locations, using a Fourier transform of DNA walks: https://github.com/celphin/RepeatOBserverV1. RepeatOBserver can identify a broad range of repeats (3-20,000bp long) in genome assemblies without any a priori knowledge of repeat sequences or the need for optimizing parameters. RepeatOBserver allows for easy visualization of the positions of both perfect and imperfect repeating sequences across each chromosome. We use RepeatOBserver to compare DNA walks, repeat patterns and centromere positions across genome assemblies in a wide range of well-studied species (e.g., human, mouse-ear cress), crops, and non-model organisms (e.g., fern, yew). Analyzing 107 chromosomes with known centromere positions, we find that centromeres consistently occur in regions that have the least diversity in repeat types (i.e. one or a few repeated sequences are present in very high numbers). Taking advantage of this information, we use a genomic Shannon diversity index to predict centromere locations in several other chromosome-scale genome assemblies. The Fourier spectra produced by RepeatOBserver can help visualize historic centromere positions, potential neocentromeres, retrotransposon clusters and gene copy variation. Identification of patterns of split and inverted tandem repeats at inversion boundaries suggests that at least some chromosomal inversions can be predicted with RepeatOBserver. RepeatOBserver is therefore a flexible tool for comprehensive characterization of tandem repeat patterns that can be used to visualize and identify a variety of regions of interest in genome assemblies.

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Section: Resultsmentioning

confidence: 99%

RepeatOBserver: tandem repeat visualization and centromere detection

Elphinstone,

Todesco

et al. 2023

Preprint

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“…Analysis of B Chromosome-derived mini-chromosomes in maize showed that many can also pair and recombine during meiosis, although smaller variants showed precocious separation during anaphase and, in other cases, did not pair (Han et al 2008). In maize, tethering CENH3 using a LexA fusion to an array of LexO repeats causes formation of dicentric chromosomes that show instability and chromosome breakage, with the resulting mini-chromosomes being maintained through subsequent generations (Dawe et al 2023). As these mini-chromosomes can autonomously propagate, they have the potential to form chassis or blueprints for artificial chromosomes capable of delivering complex pathways within and between species (Dawe et al 2023).…”

Section: Cenh3 Genome Elimination and Mini-chromosomesmentioning

confidence: 99%

The structure, function, and evolution of plant centromeres

Naish,

Henderson

2024

Genome Res.

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Centromeres are essential regions of eukaryotic chromosomes responsible for the formation of kinetochore complexes, which connect to spindle microtubules during cell division. Notably, although centromeres maintain a conserved function in chromosome segregation, the underlying DNA sequences are diverse both within and between species and are predominantly repetitive in nature. The repeat content of centromeres includes high-copy tandem repeats (satellites), and/or specific families of transposons. The functional region of the centromere is defined by loading of a specific histone 3 variant (CENH3), which nucleates the kinetochore and shows dynamic regulation. In many plants, the centromeres are composed of satellite repeat arrays that are densely DNA methylated and invaded by centrophilic retrotransposons. In some cases, the retrotransposons become the sites of CENH3 loading. We review the structure of plant centromeres, including monocentric, holocentric, and metapolycentric architectures, which vary in the number and distribution of kinetochore attachment sites along chromosomes. We discuss how variation in CENH3 loading can drive genome elimination during early cell divisions of plant embryogenesis. We review how epigenetic state may influence centromere identity and discuss evolutionary models that seek to explain the paradoxically rapid change of centromere sequences observed across species, including the potential roles of recombination. We outline putative modes of selection that could act within the centromeres, as well as the role of repeats in driving cycles of centromere evolution. Although our primary focus is on plant genomes, we draw comparisons with animal and fungal centromeres to derive a eukaryote-wide perspective of centromere structure and function.

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“…Root tissues were collected from tissue culture-grown 717 plantlets. Fluorescent in situ hybridization and slides preparation were performed following published methods (Dawe et al, 2023), using four 6-FAM-labeled PtaM147 oligos (5 0 -ATCGAAGTCGGAATGCCG CGA-3 0 ,5 0 -AGCAGAAGCATACATGCTCAA-3 0 , 5 0 -AAGGCAACTGAA TTTCGGCAA-3 0 , 5 0 -AACTCACCGAGTCAAAGCGTT-3 0 ). The images were captured using a Zeiss Axio Imager.M1 fluorescence microscope with a 639 plan-apo Chromat oil objective.…”

Section: Fluorescent In Situ Hybridizationmentioning

confidence: 99%

Haplotype‐resolved genome assembly of Populus tremula × P. alba reveals aspen‐specific megabase satellite DNA

Zhou,

Jenkins,

Zeng

et al. 2023

The Plant Journal

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SUMMARYPopulus species play a foundational role in diverse ecosystems and are important renewable feedstocks for bioenergy and bioproducts. Hybrid aspen Populus tremula × P. alba INRA 717‐1B4 is a widely used transformation model in tree functional genomics and biotechnology research. As an outcrossing interspecific hybrid, its genome is riddled with sequence polymorphisms which present a challenge for sequence‐sensitive analyses. Here we report a telomere‐to‐telomere genome for this hybrid aspen with two chromosome‐scale, haplotype‐resolved assemblies. We performed a comprehensive analysis of the repetitive landscape and identified both tandem repeat array‐based and array‐less centromeres. Unexpectedly, the most abundant satellite repeats in both haplotypes lie outside of the centromeres, consist of a 147 bp monomer PtaM147, frequently span >1 megabases, and form heterochromatic knobs. PtaM147 repeats are detected exclusively in aspens (section Populus) but PtaM147‐like sequences occur in LTR‐retrotransposons of closely related species, suggesting their origin from the retrotransposons. The genomic resource generated for this transformation model genotype has greatly improved the design and analysis of genome editing experiments that are highly sensitive to sequence polymorphisms. The work should motivate future hypothesis‐driven research to probe into the function of the abundant and aspen‐specific PtaM147 satellite DNA.

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Synthetic maize centromeres transmit chromosomes across generations

Cited by 5 publications

References 61 publications

RepeatOBserver: tandem repeat visualization and centromere detection

RepeatOBserver: tandem repeat visualization and centromere detection

The structure, function, and evolution of plant centromeres

Haplotype‐resolved genome assembly of Populus tremula × P. alba reveals aspen‐specific megabase satellite DNA

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