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Metaphase chromosomes from figure 4 are arranged according to the chromosome nomenclature of the gray whale. Heteromorphic chromosome pairs are denoted by asterisks.
Source publication
Cetacean karyotypes possess exceptionally stable diploid numbers and highly conserved chromosomes. To date, only toothed whales (Odontoceti) have been analyzed by comparative chromosome painting. Here, we studied the karyotype of a representative of baleen whales, the gray whale (Eschrichtius robustus, Mysticeti), by Zoo-FISH with dromedary camel a...
Contexts in source publication
Context 1
... heterochromatic blocks in the karyotype of the gray whale appear to be composed of both common repeat and heavy satellite repeat se- quences (with several notable exceptions). The subtelo- meric block of heterochromatin on the X chromosome hybridizes only with the heavy satellite repeat ( fig.5 ). In- terstitial blocks in the acrocentric chromosomes 18-21 are represented by the common cetacean repeat sequenc- es, whose amplification could cause the observed hetero- morphism in some of these chromosome pairs (18). ...
Context 2
... analysis also uncovered a higher copy number of the common repeat in one of the homologs in autosome pairs 1 and 5. The rest of the heteromorphic pairs (2, 8, 10, 12 and 15) had heterochromatic blocks that were likely formed via co-amplification of common repeat and heavy satellite repeat ( fig.5 ). ...
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Citations
... Order Artiodactyla, or even-toed ungulates, is a large mammalian order that includes whales, pigs, hippos, camels, and other ruminants. Studies utilizing routine and differential staining techniques have highlighted remarkable karyotype uniformity among cetaceans, with a consistent diploid chromosome number of 2n = 44 across most species [157][158][159][160][161]. Chromosome maps for Odontoceti (toothed) species, such as the Atlantic bottlenose dolphin, pilot whale, and Yangtze finless porpoise, revealed identical karyotypes among these species, emphasizing the stability and low rates of karyotype evolution in cetaceans [162]. ...
Chromosome reshuffling events are often a foundational mechanism by which speciation can occur, giving rise to highly derivative karyotypes even amongst closely related species. Yet, the features that distinguish lineages prone to such rapid chromosome evolution from those that maintain stable karyotypes across evolutionary time are still to be defined. In this review, we summarize lineages prone to rapid karyotypic evolution in the context of Simpson’s rates of evolution—tachytelic, horotelic, and bradytelic—and outline the mechanisms proposed to contribute to chromosome rearrangements, their fixation, and their potential impact on speciation events. Furthermore, we discuss relevant genomic features that underpin chromosome variation, including patterns of fusions/fissions, centromere positioning, and epigenetic marks such as DNA methylation. Finally, in the era of telomere-to-telomere genomics, we discuss the value of gapless genome resources to the future of research focused on the plasticity of highly rearranged karyotypes.
... Cervidae karyotypes are characterized by diversity in the diploid chromosome number (2n = 6-70) 7, 8 and have evolved by tandem and Robertsonian translocations of acrocentric chromosomes 9 , also involving sex chromosomes. Comparative chromosome painting with whole chromosome painting probes has been employed in several studies [10][11][12][13][14][15][16] . These studies showed that artiodactyl autosomes evolved through fissions, fusions, and OPEN www.nature.com/scientificreports/ ...
... According to our data an increase in the rate of X chromosome evolution is observed within the Cervidae family. In ruminants the speed of X chromosome evolution is 1 rearrangement per 15 million years 14 . In the family Cervidae, we find an average rate, including X-autosome translocations, of 2 rearrangements per 10 million years. ...
The family Cervidae is the second most diverse in the infraorder Pecora and is characterized by variability in the diploid chromosome numbers among species. X chromosomes in Cervidae evolved through complex chromosomal rearrangements of conserved segments within the chromosome, changes in centromere position, heterochromatic variation, and X-autosomal translocations. The family Cervidae consists of two subfamilies: Cervinae and Capreolinae. Here we build a detailed X chromosome map with 29 cattle bacterial artificial chromosomes of representatives of both subfamilies: reindeer (Rangifer tarandus), gray brocket deer (Mazama gouazoubira), Chinese water deer (Hydropotes inermis) (Capreolinae); black muntjac (Muntiacus crinifrons), tufted deer (Elaphodus cephalophus), sika deer (Cervus nippon) and red deer (Cervus elaphus) (Cervinae). To track chromosomal rearrangements during Cervidae evolution, we summarized new data, and compared them with available X chromosomal maps and chromosome level assemblies of other species. We demonstrate the types of rearrangements that may have underlined the variability of Cervidae X chromosomes. We detected two types of cervine X chromosome—acrocentric and submetacentric. The acrocentric type is found in three independent deer lineages (subfamily Cervinae and in two Capreolinae tribes—Odocoileini and Capreolini). We show that chromosomal rearrangements on the X-chromosome in Cervidae occur at a higher frequency than in the entire Ruminantia lineage: the rate of rearrangements is 2 per 10 million years.
... The characteristics of the set of dromedary chromosome-specific probes were also reported previously [Balmus et al., 2007]. Probes containing ribosomal DNA and telomere repeated sequences were described earlier [Kulemzina et al., 2016;Proskuryakova et al., 2018]. The protocol of selection of BAC clones was reported in previous research [Proskuryakova et al., 2017]. ...
The family Cervidae is the second most diverse family in the infraorder Pecora and is characterized by a striking variability in the diploid chromosome numbers among species, ranging from 6 to 70. Chromosomal rearrangements in Cervidae have been studied in detail by chromosome painting. There are many comparative cytogenetic data for both subfamilies (Cervinae and Capreolinae) based on homologies with chromosomes of cattle and Chinese muntjac. Previously it was found that interchromosomal rearrangements are the major type of rearrangements occurring in the Cervidae family. Here, we build a detailed chromosome map of a female reindeer ( Rangifer tarandus , 2n = 70, Capreolinae) and a female black muntjac ( Muntiacus crinifrons , 2n = 8, Cervinae) with dromedary homologies to find out what other types of rearrangements may have underlined the variability of Cervidae karyotypes. To track chromosomal rearrangements and the distribution of nucleolus organizer regions not only during Cervidae but also Pecora evolution, we summarized new data and compared them with chromosomal maps of other already studied species. We discuss changes in the pecoran ancestral karyotype in the light of new painting data. We show that intrachromosomal rearrangements in autosomes of Cervidae are more frequent than previously thought: at least 13 inversions in evolutionary breakpoint regions were detected.
... When a chromosome translocation occurs involving a single chromosome, it is referred to as a shift. The similar inversion breakpoint in EAS1, orthologous to ECA31, did not exist in the orthologous regions of EBU8, TIN20, BMU21, and HAS6 but was present in CSI37 (Figs. 4 and 5) [6,13,32]. We also detected an inversion and a shift in EAS1, CSI2, BMU19, and HAS7, orthologous to ECA4 (Figs. 4 and 5). ...
Background
It is important to resolve the evolutionary history of species genomes as it has affected both genome organization and chromosomal architecture. The rapid innovation in sequencing technologies and the improvement in assembly algorithms have enabled the creation of highly contiguous genomes. DNA Zoo, a global organization dedicated to animal conservation, offers more than 150 chromosome-length genome assemblies. This database has great potential in the comparative genomics field.
Results
Using the donkey (Equus asinus asinus, EAS) genome provided by DNA Zoo as an example, the scaffold N50 length and Benchmarking Universal Single-Copy Ortholog score reached 95.5 Mb and 91.6%, respectively. We identified the cytogenetic nomenclature, corrected the direction of the chromosome-length sequence of the donkey genome, analyzed the genome-wide chromosomal rearrangements between the donkey and horse, and illustrated the evolution of the donkey chromosome 1 and horse chromosome 5 in perissodactyls.
Conclusions
The donkey genome provided by DNA Zoo has relatively good continuity and integrity. Sequence-based comparative genomic analyses are useful for chromosome evolution research. Several previously published chromosome painting results can be used to identify the cytogenetic nomenclature and correct the direction of the chromosome-length sequence of new assemblies. Compared with the horse genome, the donkey chromosomes 1, 4, 20, and X have several obvious inversions, consistent with the results of previous studies. A 4.8 Mb inverted structure was first discovered in the donkey chromosome 25 and plains zebra chromosome 11. We speculate that the inverted structure and the tandem fusion of horse chromosome 31 and 4 are common features of non-caballine equids, which supports the correctness of the existing Equus phylogeny to an extent.
... Heterochromatin can appear as dark, intermediate, or light areas by G-banding; in this individual the heterochromatic regions appear mainly as pale staining. The size variation of heterochromatin in cetaceans has been shown to be due to amplification of a small number of specific types of heterochromatin, as detailed by Widegren [1984, 1989] and Kulemzina et al. [2016]. ...
The karyotype of the Odontocete whale, Mesoplodon densirostris, has not been previously reported. The chromosome number is determined to be 2n = 42, and the karyotype is presented using G-, C-, and nucleolar organizer region (NOR) banding. The findings include NOR regions on 2 chromosomes, regions of heterochromatic variation, a large block of heterochromatin on the X chromosome, and a relatively large Y chromosome. The karyotype is compared to published karyograms of 2 other species of Mesoplodon.
... The observed karyotype uniformity is hypothesized to derive from characteristics of the habitat and physiology. Comparative chromosome painting has uncovered an identical order of syntenic segments in toothed and baleen whales [32,73,74] as well as in delphinids [75], just as among the pinnipeds in the present study. The low numbers of interchromosomal rearrangements giving rise to high conservatism of syntenic segments in cetacean and pinniped marine mammals seem well established. ...
Pinnipedia karyotype evolution was studied here using human, domestic dog, and stone marten whole-chromosome painting probes to obtain comparative chromosome maps among species of Odobenidae (Odobenus rosmarus), Phocidae (Phoca vitulina, Phoca largha, Phoca hispida, Pusa sibirica, Erignathus barbatus), and Otariidae (Eumetopias jubatus, Callorhinus ursinus, Phocarctos hookeri, and Arctocephalus forsteri). Structural and functional chromosomal features were assessed with telomere repeat and ribosomal-DNA probes and by CBG (C-bands revealed by barium hydroxide treatment followed by Giemsa staining) and CDAG (Chromomycin A3-DAPI after G-banding) methods. We demonstrated diversity of heterochromatin among pinniped karyotypes in terms of localization, size, and nucleotide composition. For the first time, an intrachromosomal rearrangement common for Otariidae and Odobenidae was revealed. We postulate that the order of evolutionarily conserved segments in the analyzed pinnipeds is the same as the order proposed for the ancestral Carnivora karyotype (2n = 38). The evolution of conserved genomes of pinnipeds has been accompanied by few fusion events (less than one rearrangement per 10 million years) and by novel intrachromosomal changes including the emergence of new centromeres and pericentric inversion/centromere repositioning. The observed interspecific diversity of pinniped karyotypes driven by constitutive heterochromatin variation likely has played an important role in karyotype evolution of pinnipeds, thereby contributing to the differences of pinnipeds’ chromosome sets.
... Additional investigation is required to verify if this inversion occurred in the same region, with an in-depth analysis of the DNA sequence surrounding this region needed to elucidate the genomic elements causing repeated rearrangements. Contrary to what has been previously suggested [5], this ancestral PAK chromosome C2 was composed of HSA 12/22, and not of HSA 12/22/12/22, because the outgroup and many species from basal lineages have the HSA 12/22 association (whales, Java mouse deer, giraffe, okapi, saola, hirola) [5,11,30,43]. Similarly, the independent inversions in PAK chromosome E (CDR 22/3/22/3/22/3) in BTA 7 (Bovina), OAR 5, OMO 8 (Caprini) (CDR 22/3/22/3), and giraffe (Giraffidae) [30], while ancestral conditions were retained in Java mouse deer, pronghorn, Siberian musk deer and saola, mark another hot spot of chromosome evolution that requires further study. ...
Bovidae, the largest family in Pecora infraorder, are characterized by a striking variability in diploid number of chromosomes between species and among individuals within a species. The bovid X chromosome is also remarkably variable, with several morphological types in the family. Here we built a detailed chromosome map of musk ox (Ovibos moschatus), a relic species originating from Pleistocene megafauna, with dromedary and human probes using chromosome painting. We trace chromosomal rearrangements during Bovidae evolution by comparing species already studied by chromosome painting. The musk ox karyotype differs from the ancestral pecoran karyotype by six fusions, one fission, and three inversions. We discuss changes in pecoran ancestral karyotype in the light of new painting data. Variations in the X chromosome structure of four bovid species nilgai bull (Boselaphus tragocamelus), saola (Pseudoryx nghetinhensis), gaur (Bos gaurus), and Kirk’s Dikdik (Madoqua kirkii) were further analyzed using 26 cattle BAC-clones. We found the duplication on the X in saola. We show main rearrangements leading to the formation of four types of bovid X: Bovinae type with derived cattle subtype formed by centromere reposition and Antilopinae type with Caprini subtype formed by inversion in XSB3.
... Molecular probes are another tool that allows the detection of heterochromatin. Cloned repeats (Shevchenko et al. 2002;Liu et al. 2011;Kulemzina et al. 2016) and repeat-containing chromosome or region-specific painting probes (Li et al. 2004) can clearly identify chromosomes with heterochromatin blocks in some cases. However, these probes are usually limited to narrow species group due to fast divergence rate of the heterochromatin repeats. ...
... Interestingly, many of the additional heterochromatin blocks such as in moose, fur seal, hedgehog, polecat, and Arctic fox are mostly GC-rich (Fig. 5, Table 1). However, there are also extended AT-rich heterochromatin areas like in a field vole and a whale (Kulemzina et al. 2016). Thus, evolutionary flexible repeat units forming heterochromatin areas may vary greatly in the nucleotide composition depending on the genome. ...
Сonstitutive heterochromatin areas are revealed by differential staining as C-positive chromosomal regions. These C-positive bands may greatly vary by location, size, and nucleotide composition. CBG-banding is the most commonly used method to detect structural heterochromatin in animals. The difficulty in identification of individual chromosomes represents an unresolved problem of this method as the body of the chromosome is stained uniformly and does not have banding pattern beyond C-bands. Here, we present the method that we called CDAG for sequential heterochromatin staining after differential GTG-banding. The method uses G-banding followed by heat denaturation in the presence of formamide with consecutive fluorochrome staining. The new technique is valid for the concurrent revealing of heterochromatin position due to differential banding of chromosomes and heterochromatin composition (AT-/GC-rich) in animal karyotyping.
... The variation in the number of transcriptionally active NORs can occur even between the cells and tissues of one individual [8]. NORs are predominantly located in telomere regions, colocalizing with telomeric repeats [9], in the short arms or near centromeric regions of acrocentric chromosomes [10][11][12][13] and more rarely interstitially [14,15]. The quantity of ribosomal genes at telomeric sites is variable [16,17]. ...
... There are data about NOR variation in the number and chromosomal location in closely related species, suggesting that rDNA clusters are highly mobile components of the genome [4,36]. In species related to Javan mouse deer, such as gray whale [13] and giraffe [37] NORs are situated on non-homologous chromosomes representing different syntenic groups. Such interspecies lability of NORs is generated either by chromosomal rearrangements or transposition events [38]. ...
There are differences in number and localization of nucleolus organizer regions (NORs) in genomes. In mammalian genomes, NORs are located on autosomes, which are often situated on short arms of acrocentric chromosomes and more rarely in telomeric, pericentromeric, or interstitial regions. In this work, we report the unique case of active NORs located on gonоsomes of a eutherian mammal, the Javan mouse-deer (Tragulus javanicus). We have investigated the position of NORs by FISH experiments with ribosomal DNA (rDNA) sequences (18S, 5.8S, and 28S) and show the presence of a single NOR site on the X and Y chromosomes. The NOR is localized interstitially on the p-arm of the X chromosome in close proximity with prominent C-positive heterochromatin blocks and in the pericentromeric area of mostly heterochromatic Y. The NOR sites are active on both the X and Y chromosomes in the studied individual and surrounded by GC enriched heterochromatin. We hypothesize that the surrounding heterochromatin might have played a role in the transfer of NORs from autosomes to sex chromosomes during the karyotype evolution of the Javan mouse-deer.
... For example, the maximum recorded dive duration for a gray whale clocked in San Ignacio Lagoon was 25.9 min [13]. Chromosomal peculiarities of gray whale and these specimens, including the whole ZooFISH data with human and camel chromosomal painting probes, description and localization of repeated and satellite DNAs were previously reported [14]. ...
Background: Gray whale, Eschrichtius robustus (E. robustus), is a single member of the family Eschrichtiidae, which is considered to be the most primitive in the class Cetacea. Gray whale is often described as a “living fossil”. It is adapted to extreme marine conditions and has a high life expectancy (77 years). The assembly of a gray whale genome and transcriptome will allow to carry out further studies of whale evolution, longevity, and
resistance to extreme environment.
Results: In this work, we report the first de novo assembly and primary analysis of the E. robustus genome and transcriptome based on kidney and liver samples. The presented draft genome assembly is complete by 55% in terms of a total genome length, but only by 24% in terms of the BUSCO complete gene groups, although 10,895 genes were identified. Transcriptome annotation and comparison with other whale species revealed robust expression of DNA repair and hypoxia-response genes, which is expected for whales.
Conclusions: This preliminary study of the gray whale genome and transcriptome provides new data to better
understand the whale evolution and the mechanisms of their adaptation to the hypoxic conditions.
