Abstract
Centromeres are chromosomal regions that serve as platforms for kinetochore assembly and spindle attachments, ensuring accurate chromosome segregation during cell division. Despite functional conservation, centromere DNA sequences are diverse and often repetitive, making them challenging to assemble and identify. Here, we describe centromeres in an oomycete Phytophthora sojae by combining long-read sequencing-based genome assembly and chromatin immunoprecipitation for the centromeric histone CENP-A followed by high-throughput sequencing (ChIP-seq). P. sojae centromeres cluster at a single focus at different life stages and during nuclear division. We report an improved genome assembly of the P. sojae reference strain, which enabled identification of 15 enriched CENP-A binding regions as putative centromeres. By focusing on a subset of these regions, we demonstrate that centromeres in P. sojae are regional, spanning 211 to 356 kb. Most of these regions are transposon-rich, poorly transcribed, and lack the histone modification H3K4me2 but are embedded within regions with the heterochromatin marks H3K9me3 and H3K27me3. Strikingly, we discovered a Copia-like transposon (CoLT) that is highly enriched in the CENP-A chromatin. Similar clustered elements are also found in oomycete relatives of P. sojae, and may be applied as a criterion for prediction of oomycete centromeres. This work reveals a divergence of centromere features in oomycetes as compared to other organisms in the Stramenopila-Alveolata-Rhizaria (SAR) supergroup including diatoms and Plasmodium falciparum that have relatively short and simple regional centromeres. Identification of P. sojae centromeres in turn also advances the genome assembly.
Highlights
Accurate segregation of chromosomes during mitosis and meiosis is critical for the development and reproduction of all eukaryotic organisms
Oomycetes are fungal-like microorganisms that belong to the stramenopiles within the Stramenopila-Alveolata-Rhizaria (SAR) supergroup
We report long-read sequencing-based genome assembly of the Phytophthora sojae reference strain, which facilitated the discovery of centromeres
Summary
Accurate segregation of chromosomes during mitosis and meiosis is critical for the development and reproduction of all eukaryotic organisms. Point centromeres have been only reported in the budding yeast Saccharomyces cerevisiae and its close relatives, holocentromeres have been identified in some insects, plants and nematodes, represented by Caenorhabditis elegans, while regional centromeres are the most common type and found in most eukaryotic phyla [1, 3]. Most animals and plants have large regional centromeres composed of satellite sequences that are organized into a variety of different higher order repeats [4, 8, 9]. The centromeric sequences of fungal regional centromeres can be composed of active or inactive clusters of transposable elements and very repetitive, such as in Cryptococcus spp. and N. crassa [13, 14], or can be nonrepetitive and very short, such as in the wheat pathogen Zymoseptoria tritici [15] and C. albicans [16]. The malaria pathogen Plasmodium falciparum and the diatom Phaeodactylum tricornutum CENP-A binding regions are Centromeres in the oomycete Phytophthora sojae characterized by short simple AT-rich sequences [17, 18], while the parasite Toxoplasma gondii has a simple centromere without nucleotide bias [19]
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