Whole chromosome elimination and chromosome terminus elimination both contribute to somatic differentiation in Taiwanese hagfish Paramyxine sheni

Abstract

Chromosome elimination is a process in which some chromatins are discarded from the presumptive somatic cells during early embryogenesis. Eliminated chromatins in hagfish generally consist of repetitive sequences, and they are highly heterochromatinized in germ cells. In this study, we characterized four novel eliminated DNA families, EEPs1-4, from the Taiwanese hagfish Paramyxine sheni. Sequences of these four elements occupied 20-27% of eliminated DNA in total, and each family was arranged mainly in tandem in the germline genome with high copy numbers. Although most of these elements were eliminated, a minor fraction remained in somatic cells. Some eliminated DNA families are shared as eliminated sequences between Eptatretidae and Myxinidae. Fluorescence in situ hybridization (FISH) of these elements showed that not only heterochromatic chromosomes but also both ends of euchromatic chromosomes in germ cells are absent in somatic cells of P. sheni. It strongly suggests that chromosome terminus elimination, in addition to whole chromosome elimination, contributes to somatic chromosome differentiation. Telomere-FISH further showed that chromosome fragmentation and the subsequent de novo addition of telomeric repeats are the likely mechanisms underlying chromosome terminus elimination. These characteristics make it indispensable to study the evolution and mechanisms underlying chromosome elimination in hagfish.

Comprehensive Chromosome End Remodeling During Programmed DNA Elimination

“…In hagfish, loss of only repetitive sequences has been identified in DNA elimination [9,10]. DNA FISH and cytogenetic analysis indicate the loss of whole hagfish chromosomes and chromosome termini encompassing 21-75% of the germline DNA in different species [9,10]. It is not known whether the loss at hagfish chromosome termini is similar to that observed here in Ascaris or if an excision event (internal deletion and fusion) occurs removing subtelomeric regions without loss of the telomere from the chromosome.…”

“…Programmed DNA elimination in lampreys is associated with decreased chromosome numbers (chromosome loss and/or fusion) and loss of ~20% the germline DNA (500 Mb of DNA) in somatic cells, loss of both repetitive sequences and some germline expressed genes [11,12,14,15]. In hagfish, loss of only repetitive sequences has been identified in DNA elimination [9,10]. DNA FISH and cytogenetic analysis indicate the loss of whole hagfish chromosomes and chromosome termini encompassing 21-75% of the germline DNA in different species [9,10].…”

“…The elimination only occurs in somatic cells and leads to a distinct and reduced somatic cell genome compared to the germline cell genome. This form of DNA elimination occurs in some parasitic nematodes (ascarids), copepods, ratfish, hagfish, and lampreys [4,[8][9][10][11][12][13][14][15][16]. Programmed DNA rearrangements also occur in ciliates distinguishing the germline from somatic nuclei [17][18][19][20][21].…”

Genome Duplication in Early Vertebrates: Insights from Agnathan Cytogenetics

“…Depending on the species, between 2 and 46 chromosomes that account for 21 to over 80% of total chromatin content become eliminated from the presomatic cell line, indicating that chromosome elimination takes place during early cleavage except in germline cells ( table 2 ). Intra-and interindividual differences in chromosome numbers were reported for eptatretine germ cells, due to variation in small chromosomes ('microchromosomes') [Kojima et al, 2010] or in larger paired or odd chromosomes ('B chromosomes') [Nakai et al, 1995]. The eliminated chromatin and chromosomes, with the exception of M. garmani , are heterochromatic and contain repetitive DNA ].…”

“…Twelve families of these repetitive DNA sequences are eliminated elements that have been characterized and named according to the eptatretine species from which they were originally isolated: EEEo1 and EEEo2 (i.e. eliminated element of E. okinoseanus 1 and 2) from E. okinoseanus [Kubota et al, 1993]; EEPa1 from P. atami ; EEEc1, EEEc2 and EEEc3 from E. cirrhatus [Goto et al, 1998]; EEEb1 and EEEb2 from E. burgeri , and EEPs1-4 from P. sheni ( table 3 ) [Kojima et al, 2010]. A minor fraction of these latter sequences remains in somatic cells after chromosome elimination in P. sheni , where various germline repetitive elements accumulate also at all ends of Cband-negative chromosomes and are eliminated together with the whole C-band-positive chromosomes during germline-soma differentiation.…”