How diverse a monocentric chromosome can be? Repeatome and centromeric organization of Juncus effusus (Juncaceae)

Abstract

SUMMARYJuncus is the largest genus of Juncaceae and was considered holocentric for a long time. Recent findings, however, indicated that 11 species from different clades of the genus have monocentric chromosomes. Thus, the Juncus centromere organization and evolution need to be reassessed. We aimed to investigate the major repetitive DNA sequences of two accessions of Juncus effusus and its centromeric structure by employing whole‐genome analyses, fluorescent in situ hybridization, CENH3 immunodetection, and chromatin immunoprecipitation sequencing. We showed that the repetitive fraction of the small J. effusus genome (~270 Mbp/1C) is mainly composed of Class I and Class II transposable elements (TEs) and satellite DNAs. Three identified satellite DNA families were mainly (peri)centromeric, with two being associated with the centromeric protein CENH3, but not strictly centromeric. Two types of centromere organization were discerned in J. effusus: type 1 was characterized by a single CENH3 domain enriched with JefSAT1‐155 or JefSAT2‐180, whereas type 2 showed multiple CENH3 domains interrupted by other satellites, TEs or genes. Furthermore, while type 1 centromeres showed a higher degree of satellite identity along the array, type 2 centromeres had less homogenized arrays along the multiple CENH3 domains per chromosome. Although the analyses confirmed the monocentric organization of J. effusus chromosomes, our data indicate a more dynamic arrangement of J. effusus centromeres than observed for other plant species, suggesting it may constitute a transient state between mono‐ and holocentricity.

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

“…However, an origin via a stepwise, distally proceeding insertion of clustered centromere units, starting from the original monocentromeres (with metapolycentromeres as an intermediate stage) cannot be excluded. Intriguingly, in monocentric Juncus effuses, [11] a close relative of the holocentric genus Luzula, two types of centromeres have been found after detailed CENH3-ChIPseq analysis. Type 1 centromeres resemble canonical monocentromeres with a single CENH3 domain, but type 2 shows few additional CENH3 domains embedded within a restricted centromere region.…”

“…The "regional centromeres", representing the majority of centromeres studied so far, are often assembled on repetitive DNAs and flanked by heterochromatin domains. [7] Also, ChIP-seq experiments in different species, such as soybean, [8] Arabidopsis, [9] maize, [10] and Juncus effusus [11] demonstrated that regional monocentromeres consist of multiple neighbouring CENH3-enriched subdomains forming centromere units. The most direct proof that monocentric regional centromeres are composed of repeated centromere units is the observation of telocentric chromosomes, formed by centromere fission of a (sub)metacentric chromosome (e.g., ref.…”

Repeat-based holocentromeres of the woodrushLuzula sylvaticareveal new insights into the evolutionary transition from mono- to holocentricity

“…2024). Recent chromatin immunoprecipitation sequencing revealed that J. effusus has repeat-based and CENH3-associated monocentromeres, consisting mainly of two tandem repeat families underlying one or up to three spaced cores of CENH3-enriched regions per chromosome (Dias et al . 2024).…”

“…An interesting feature of this family is its variation in centromeric organization and chromosomal structure, making it an ideal model to address hypotheses about evolutionary processes during centromere development. Although historically the entire Juncaceae family was thought to be holocentric, cytogenetic and genomic studies revealed that six different Juncus species are monocentric (Guerra et al 2019;Hofstatter et al 2022;Mata-Sucre et al 2023;Dias et al 2024). Recent chromatin immunoprecipitation sequencing revealed that J. effusus has repeat-based and CENH3-associated monocentromeres, consisting mainly of two tandem repeat families underlying one or up to three spaced cores of CENH3-enriched regions per chromosome (Dias et al 2024).…”

“…Although historically the entire Juncaceae family was thought to be holocentric, cytogenetic and genomic studies revealed that six different Juncus species are monocentric (Guerra et al 2019;Hofstatter et al 2022;Mata-Sucre et al 2023;Dias et al 2024). Recent chromatin immunoprecipitation sequencing revealed that J. effusus has repeat-based and CENH3-associated monocentromeres, consisting mainly of two tandem repeat families underlying one or up to three spaced cores of CENH3-enriched regions per chromosome (Dias et al 2024). On the other hand, Luzula species have been up till now characterized as holocentric without specific centromeric repeats (Kuta et al 2004;Nagaki et al 2005;Heckmann et al 2011Heckmann et al , 2013Bozek et al 2012).…”