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

• Published in: The Plant journal : for cell and molecular biology 2024-06, Vol.118 (6), p.1832-1847
• Main Authors: Dias, Yhanndra, Mata‐Sucre, Yennifer, Thangavel, Gokilavani, Costa, Lucas, Báez, Mariana, Houben, Andreas, Marques, André, Pedrosa‐Harand, Andrea
• Format: Article
• Language: English
• Subjects: Aquatic plants; Arrays; Centromere - genetics; centromere organization; Centromeres; centromeric sequences; ChIP‐sequencing; Chromatin; chromatin immunoprecipitation; chromosome evolution; Chromosomes; Chromosomes, Plant - genetics; class; Deoxyribonucleic acid; DNA; DNA Transposable Elements - genetics; DNA, Plant - genetics; DNA, Satellite - genetics; domain; evolution; Fluorescence; Fluorescence in situ hybridization; Gene sequencing; genome; Genome, Plant - genetics; Genomes; genus; hybridization; Immunoprecipitation; In Situ Hybridization, Fluorescence; Juncaceae; Juncus effusus; Nucleotide sequence; Plant Proteins - genetics; Plant Proteins - metabolism; Plant species; repetitive elements; Repetitive Sequences, Nucleic Acid - genetics; rushes; Satellite DNA; satellite DNAs; Satellites; species
• ISSN: 0960-7412; 1365-313X; 1365-313X
• DOI: 10.1111/tpj.16712

SUMMARY Juncus 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. Significance Statement Recent studies have challenged the holocentric organization of Juncus centromeres, with several species now demonstrated to be monocentric. However, the annotation of all Juncus effusus centromeres revealed a distinctive centromeric organization, with eventually multiple CENH3 domains along the centromere associated with less homogenized satellite DNA, suggesting a putative transitional state between monocentric and holocentric chromosomes.