Are NORs Always Located on Homeologous Chromosomes? A FISH Investigation with rDNA and Whole Chromosome Probes in Gymnotus Fishes (Gymnotiformes)

Milhomem, Susana Suely Rodrigues; Scacchetti, Priscilla Cardim; Pieczarka, Júlio César; Ferguson‐Smith, Malcolm A.; Pansonato-Alves, José Carlos; O’Brien, Patrícia C. M.; Foresti, Fausto; Nagamachi, Cleusa Yoshiko

doi:10.1371/journal.pone.0055608

Cited by 24 publications

(24 citation statements)

References 34 publications

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“…3). Although a discussion of the ancestral condition of nucleolar organizer regions, with simple or multiple marking, has recently been proposed, 41 the great majority of species in which 18S rDNA was mapped, including the species in this study, present a terminal marking in the short arm of a subtelocentric/acrocentric pair, which suggests that they may be homologues.…”

Section: Discussionmentioning

confidence: 71%

New Approach Data in Electric Fish (Teleostei: Gymnotus): Sex Chromosome Evolution and Repetitive DNA

Silva

Matoso²,

Artoni³

et al. 2014

Zebrafish

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Antagonist sexual selection is the driving force behind the origin and diversification of sex chromosomes such as XX/XY and ZZ/ZW. However, chromosome mobility, mainly in fishes, may result in the formation of chromosomes of recent origin, a process known as turnover. The family Gymnotidae, which is composed of the genera Electrophorus+Gymnotus, presents a multiple system of the type X1X1X2X2/X1X2Y, which has been described for Gymnotus pantanal. This article describes the karyotype of three Amazon Gymnotus species, revealing the presence of both simple and multiple systems: Gymnotus carapo "Catalão" 2n=40 XX/XY, Gymnotus coropinae 2n=49♂/50♀ X1X1X2X2/X1X2Y, and Gymnotus sp. "Negro" 2n=50 XX/XY. Our hypothesis is that the simple system present in G. carapo "Catalão" is ancestral in relation to G. pantanal's multiple system and that the diversification of the subsequent multiple system occurred after the final separation of the Amazon and Paraná basins. Moreover, G. coropinae's multiple system may have originated from the simple system present in Gymnotus sp. "Negro." The distant position between the species in the Gymnotidae family's phylogeny in addition to differences in sex chromosome formula and number between Clade G1 G. coropinae and G. sp. "Negro" species and "Carapo" Clade. G. carapo and G. pantanal species suggest that both sequences of sexual systems occurred independently, supporting other proposed models and highlighting the fact that species of the genus Gymnotus may serve as a model for studying sex chromosome turnover.

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Section: Discussionmentioning

confidence: 71%

New Approach Data in Electric Fish (Teleostei: Gymnotus): Sex Chromosome Evolution and Repetitive DNA

Silva

Matoso²,

Artoni³

et al. 2014

Zebrafish

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“…The chromosome pairs GCA6 and 20 of GCA, 2n = 42 correspond to GCA11 and 20 in GCA, 2n = 40 and to GCP8 and 15. Milhomem et al [2013] demonstrated by 2-color FISH, using probes for 18S rDNA together with the WCP GCA20, that the association of rDNA and GCA20 is conserved and shared by all the studied species of Gymnotus of the G. carapo species group. G. jonasi , from the species group G. pantherinus or species group G1 [Lovejoy et al, 2010], has multiple NORs and does not share this association.…”

Section: Discussionmentioning

confidence: 88%

Chromosome Painting Reveals Multiple Rearrangements between Gymnotus capanema and Gymnotus carapo (Gymnotidae, Gymnotiformes)

Nagamachi

Pieczarka²,

Milhomem³

et al. 2013

Cytogenet Genome Res

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The genus Gymnotus (Gymnotiformes) is a group of fishes with karyotypic plasticity, demonstrated by cytogenetic studies using whole chromosome probes of G. carapo (GCA, 2n = 42) that were obtained by flow-sorting from fibroblast cultures. In the present work we undertook comparative mapping of the karyotype of G. capanema (GCP, 2n = 34) with GCA, 2n = 42 painting probes. The results demonstrate that the karyotype of G. capanema is extensively rearranged when compared to G. carapo. From the 12 chromosome pairs of G. carapo that can be individually differentiated (GCA1-3, 6, 7, 9, 14, 16 and 18-21), only 4 pairs (GCA6, 7, 19, and 20) maintained conserved synteny in G. capanema. From these 4, GCA6 and GCA20 correspond to individual chromosomes (GCP8 and GCP15), while the other 2 share homology with parts of GCP1 and GCP2, respectively. The remaining GCP chromosomes showed more complex hybridization patterns with homologies to other GCA pairs. These results demonstrate that the level of reorganization in the genome of G. capanema is much greater than in GCA, 2n = 42 and in karyomorph GCA, 2n = 40 which was previously analyzed by chromosome painting.

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“…Among the Nannostomus species investigated here, chromosomal mapping revealed somewhat uniform patterns of distribution for both rDNA classes, with one to few sites of accumulation, as found in most fishes [93,94], as well as in some other lebiasinids [21,22] investigated to date. While some of these sites may appear to be orthologous among the species under study, the frequently high dynamics of these repetitive DNA classes do not allow us to make certain conclusions without additional data (for an exemplary study, see Milhomem et al [95]). Nonetheless, in addition to the fact that some rDNA sites were clearly involved in Robertsonian fusions (as mentioned above), it may be inferred that like some other related lebiasinids [19], Nannostomus species do not show a substantial level of intrachromosomal dynamics that could be detected by the markers selected by us.…”

Section: Discussionmentioning

confidence: 99%

Centric Fusions behind the Karyotype Evolution of Neotropical Nannostomus Pencilfishes (Characiforme, Lebiasinidae): First Insights from a Molecular Cytogenetic Perspective

Sember

Oliveira

Ráb

et al. 2020

Genes

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Lebiasinidae is a Neotropical freshwater family widely distributed throughout South and Central America. Due to their often very small body size, Lebiasinidae species are cytogenetically challenging and hence largely underexplored. However, the available but limited karyotype data already suggested a high interspecific variability in the diploid chromosome number (2n), which is pronounced in the speciose genus Nannostomus, a popular taxon in ornamental fish trade due to its remarkable body coloration. Aiming to more deeply examine the karyotype diversification in Nannostomus, we combined conventional cytogenetics (Giemsa-staining and C-banding) with the chromosomal mapping of tandemly repeated 5S and 18S rDNA clusters and with interspecific comparative genomic hybridization (CGH) to investigate genomes of four representative Nannostomus species: N. beckfordi, N. eques, N. marginatus, and N. unifasciatus. Our data showed a remarkable variability in 2n, ranging from 2n = 22 in N. unifasciatus (karyotype composed exclusively of metacentrics/submetacentrics) to 2n = 44 in N. beckfordi (karyotype composed entirely of acrocentrics). On the other hand, patterns of 18S and 5S rDNA distribution in the analyzed karyotypes remained rather conservative, with only two 18S and two to four 5S rDNA sites. In view of the mostly unchanged number of chromosome arms (FN = 44) in all but one species (N. eques; FN = 36), and with respect to the current phylogenetic hypothesis, we propose Robertsonian translocations to be a significant contributor to the karyotype differentiation in (at least herein studied) Nannostomus species. Interspecific comparative genome hybridization (CGH) using whole genomic DNAs mapped against the chromosome background of N. beckfordi found a moderate divergence in the repetitive DNA content among the species’ genomes. Collectively, our data suggest that the karyotype differentiation in Nannostomus has been largely driven by major structural rearrangements, accompanied by only low to moderate dynamics of repetitive DNA at the sub-chromosomal level. Possible mechanisms and factors behind the elevated tolerance to such a rate of karyotype change in Nannostomus are discussed.

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Are NORs Always Located on Homeologous Chromosomes? A FISH Investigation with rDNA and Whole Chromosome Probes in Gymnotus Fishes (Gymnotiformes)

Cited by 24 publications

References 34 publications

New Approach Data in Electric Fish (Teleostei: Gymnotus): Sex Chromosome Evolution and Repetitive DNA

New Approach Data in Electric Fish (Teleostei: Gymnotus): Sex Chromosome Evolution and Repetitive DNA

Chromosome Painting Reveals Multiple Rearrangements between <b><i>Gymnotus capanema</i></b> and <b><i>Gymnotus carapo</i></b> (Gymnotidae, Gymnotiformes)

Centric Fusions behind the Karyotype Evolution of Neotropical Nannostomus Pencilfishes (Characiforme, Lebiasinidae): First Insights from a Molecular Cytogenetic Perspective

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