Highly conserved Z and molecularly diverged W chromosomes in the fish genus Triportheus (Characiformes, Triportheidae)

Yano, Cassia Fernanda; Bertollo, Luis Antônio Carlos; Ezaz, Tariq; Trifonov, Vladimir A.; Sember, Alexandr; Liehr, Thomas; Cioffi, Marcelo de Bello

doi:10.1038/hdy.2016.83

Cited by 41 publications

(49 citation statements)

References 58 publications

(73 reference statements)

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“…Chromosomal mapping of rDNA clusters has repeatedly helped to unveil diverse evolutionary issues (e.g., [82,83]). Particularly in fishes, it provided valuable clues about the incidence of cryptic, morphologically indistinguishable sibling species [5,6,8,10,84], polyploidization and interspecific hybridization events [85,86], a geographical gradient of genomic and morphological change [87], patterns of sex chromosome differentiation [80,[88][89][90], and the correlation of genome dynamics in response to environmental cues [91,92]. 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.…”

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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“…For example, in the characid genus Triportheus (Triportheidae), the W chromosome harbors an 18S rDNA cistron in the terminal region of the q arms, which is missing in the Z chromosome in the majority of the species [Yano et al, 2016a]. In this case, it is likely that these sequences could have been deleted from the Z chromosome after acquisition of a sex-specific allele by the W and the restriction of recombination in the sex chromosome pair [Yano et al, 2016b]. In Hoplias malabaricus (Erythrinidae), which corresponds to a species complex having a conspicuous XX/XY sex chromosome system in one of its karyomorphs, the X chromosome also shows an exclusive heterochromatic segment associated with a NOR region [Cioffi et al, 2010].…”

Section: Discussionmentioning

confidence: 99%

Genomic Organization of Repetitive DNAs and Differentiation of an XX/XY Sex Chromosome System in the Amazonian Puffer Fish, <b><i>Colomesus asellus </i></b>(Tetraodontiformes)

Viana

Ezaz²,

Marajó

et al. 2017

Cytogenet Genome Res

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The genus Colomesus is the sole representative of the family Tetraodontidae in the Amazon region. Here, Colomesus asellus was analyzed using conventional and molecular cytogenetic protocols. Its diploid chromosome number is 2n = 46 with 12 meta-, 10 submeta-, 16 subtelo-, and 8 acrocentric chromosomes and a fundamental number of FN = 84. An XX/XY sex chromosome system was identified. Mapping of 18S rDNA correlated with the nucleolus organizer regions (Ag-NORs) in the short arms of the 2 X chromosomes in females and in the Y chromosome in males. C-banding revealed heterochromatin in the centromeric regions of all chromosomes, except for pair 3. Prominent sex chromosome-specific heterochromatin amplification was observed, covering the short arms of the Y chromosome almost entirely. FISH with telomeric and tropomyosin (tpm1) sequences, respectively, revealed terminal signals in all chromosomes. The analysis of extended DNA fibers confirmed the colocalization and the interspersed pattern of the telomeric and tpm1 sequences. Thus, this study highlights the remarkable evolutionary dynamism presented by the Amazonian puffer fish regarding the differentiation of a heteromorphic XY sex chromosome system and a particular sex-specific amplification of rDNA sites. This is the first record of such an association in the Tetraodontidae family.

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“…This way, the significative role of several classes of repetitive DNAs in the differentiation path of the sex pair, both at its inicial stage (Cioffi and Bertollo 2010; Freitas et al in press) or more advanced ones (Cioffi et al 2010, 2011a, b, 2012b; Yano et al 2014a, b), was clearly highlighted. Notably, whole chromosome painting (WCP) and comparative genomic hybridization (CGH) were able to demonstrate that fish sex chromosomes can have an independent origin even among closely related species (Cioffi et al 2011c, d; 2013) or, alternatively, a common origin within particular monophyletic groups (Yano et al 2016). …”

Section: Catalogue Of Msc Dissertations and Phd Thesesmentioning

confidence: 99%

Contributions to the cytogenetics of the Neotropical fish fauna

Bertollo

Cioffi

Galetti

et al. 2017

CCG

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Brazilian fish cytogenetics started as early as the seventies in three pioneering research groups, located at the Universidade Estadual Paulista (UNESP, Botucatu, SP), Universidade Federal de São Carlos (UFSCar, São Carlos, SP) and Universidade de São Paulo (USP, São Paulo, SP). Investigations that have been conducted in these groups led to the discovery of a huge chromosomal and genomic biodiversity among Neotropical fishes. Besides, they also provided the expansion of this research area, with the genesis of several other South American research groups, in view of a number of dissertations and doctoral theses developed over years. The current authors were encouraged to make their thesis catalog accessible from a public source, in order to share informations on the taxa and subject matter analyzed. Some of the key contributions to evolutionary fish cytogenetics are also being highligthed.

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“…Oreochromis (Baroiller and D'Cotta, 2019). Nonetheless, a remarkable conservation of SD has also been reported in other groups, such as the genus Seriola (Koyama et al, 2019) or the order Salmoniformes (Yano et al, 2016). It has been hypothesized that intraspecific variability might facilitate the high SD evolutionary turnover of fish and accordingly, these authors suggested focusing not only on the master SDg, but also on the genetic variation within species to obtain a more comprehensive picture of the SD genetic architecture.…”

Section: Introductionmentioning

confidence: 99%

Multiple evidences suggest sox2 as the main driver of a young and complex sex determining ZW/ZZ system in turbot (Scophthalmus maximus)

Martínez

Robledo

Taboada

et al. 2019

Preprint

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A major challenge in evolutionary biology is to find an explanation for the variation in sex-determining (SD) systems across taxa and to understand the mechanisms driving sex chromosome differentiation. We studied the turbot, holding a ZW/ZZ SD system and no sex chromosome heteromorphism, by combining classical genetics and genomics approaches to disentangle the genetic architecture of this trait. RAD-Seq was used to genotype 18,214 SNPs on 1,135 fish from 36 families and a genome wide association study (GWAS) identified a ~ 6 Mb region on LG5 associated with sex (P < 0.05). The most significant associated markers were located close to sox2, dnajc19 and fxr1 genes. A segregation analysis enabled narrowing down the associated region and evidenced recombination suppression in a region overlapping the candidate genes. A Nanopore/Illumina assembly of the SD region using ZZ and WW individuals identified a single SNP fully associated with Z and W chromosomes. RNA-seq from 5-90 day-old fish detected the expression along the gonad differentiation period of a short non-coding splicing variant (ncRNA) included in a vertebrate-conserved long non-coding RNA overlapping sox2. qPCR showed that sox2 was the only differentially expressed gene between males and females at 50-55 days post fertilization, just prior the beginning of gonad differentiation. More refined information on the involvement of secondary genetic and environmental factors and their interactions on SD was gathered after the analysis of a broad sample of families. Our results confirm the complex nature of SD in turbot and support sox2 as its main driver.

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“…According to a recent phylogenetic study established for this genus, Triportheus originated at 26.2 ± 6.5 Myr and represents a monophyletic group in which T. auritus is the oldest living species within the genus (Mariguela et al, 2016). Triportheus has stood out in many cytogenetics studies, mainly because all species studied so far have a ZW sex chromosomes system well characterized (Artoni et al, 2001;Diniz et al, 2009;Yano et al, 2016Yano et al, , 2017a. In addition, the rDNAs (Diniz et al, 2009;Marquioni et al, 2013;Yano et al, 2017b) and the U2 snRNA genes (Yano et al, 2017b) have been also investigated, highlighting the variability in the syntenic configuration as well as in the number of sites of these multigene families, mainly regarding the 5S rDNAs (Yano et al, 2017b).…”

Section: Introductionmentioning

confidence: 99%

Evolutionary Dynamics of Multigene Families in Triportheus (Characiformes, Triportheidae): A Transposon Mediated Mechanism?

Yano¹,

Torres

Bens

et al. 2020

Front. Mar. Sci.

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Triportheus (Characiformes, Triportheidae) is a freshwater fish genus with 18 valid species. These fishes are widely distributed in the major river drainages of South America, having commercial importance in the fishing market, mainly in the Amazon basin. This genus has diverged recently in a complex process of speciation carried out in different river basins. The use of repetitive sequences is suitable to trace the genomic reorganizations occured along the speciation process. In this work, the 5S rDNA multigene family has been characterized at molecular and phylogenetic level. The results showed that other multigene family has been found within the non-transcribed spacer (NTS): the U1 snRNA gene. Double-FISH with 5S and U1 probes were also performed, confirming the close linkage between these two multigene families. Moreover, evidences of different transposable elements (TE) were detected within the spacer, thus suggesting a transposon-mediated mechanism of 5S-U1 evolutionary pathway in this genus. Phylogenetic analysis demonstrated a species-specific grouping, except for Triportheus pantanensis, Triportheus aff. rotundatus and Triportheus trifurcatus. The evolutionary model of the 5S rDNA in Triportheus species has been discussed. In addition, the results suggest new clues for the speciation and evolutionary trend in these species, which could be suitable to use in other Characiformes species.

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Highly conserved Z and molecularly diverged W chromosomes in the fish genus Triportheus (Characiformes, Triportheidae)

Cited by 41 publications

References 58 publications

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

Genomic Organization of Repetitive DNAs and Differentiation of an XX/XY Sex Chromosome System in the Amazonian Puffer Fish, <b><i>Colomesus asellus </i></b>(Tetraodontiformes)

Contributions to the cytogenetics of the Neotropical fish fauna

Multiple evidences suggest sox2 as the main driver of a young and complex sex determining ZW/ZZ system in turbot (Scophthalmus maximus)

Evolutionary Dynamics of Multigene Families in Triportheus (Characiformes, Triportheidae): A Transposon Mediated Mechanism?

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