Syntenic Associations Research Articles

Karyotypic Reshuffling in the Genus Rhipidomys (Rodentia: Cricetidae: Sigmodontinae) Revealed by Zoo-FISH

Introduction: Rhipidomys is the second most specious and the most widespread genus of the tribe Thomasomyini. Chromosomal data have been an important tool in the taxonomy of the group that presents low variability of diploid number (2n) and highly variable fundamental numbers (FNs). Despite such diversity, the genus has been studied mainly by classical and banding cytogenetic techniques. Methods: This study performed a comparative study between R. emiliae (2n = 44, FN = 52), R. macrurus (2n = 44, FN = 49), R. nitela (2n = 50, FN = 71), and R. mastacalis (2n = 44, FN = 72) using chromosome painting probes of two Oryzomyini species. Results: Our analysis revealed pericentric inversion as the main rearrangement involved in the karyotype evolution of the group, although tandem fusions/fissions were also detected. In addition, we detected eight syntenic associations exclusive of the genus Rhipidomys, and three syntenic associations shared between species of the tribe Thomasomyini and Oryzomyini. Conclusion: Comparative cytogenetic analysis by ZOO-FISH on genus Rhipidomys supports a pattern of chromosomal rearrangement already suggested by comparative G-banding. However, the results suggest that karyotype variability in the genus could also involve the occurrence of an evolutionary new centromere.

Correction to: A large-scale multiomics analysis of wheat stem solidness and the wheat stem sawfly feeding response, and syntenic associations in barley, Brachypodium, and rice.

The original version of this article contained a mistake. The word "RefSeq v.1" was incorrectly inserted on page 7. The correct sentence should be: To identify the differentially regulated transcripts, clean RNA-Seq reads were mapped onto the T. aestivum Chinese Spring chromosome 3B pseudomolecule.

Chromosomal evolution and phylogeny in the Nullicauda group (Chiroptera, Phyllostomidae): evidence from multidirectional chromosome painting

BackgroundThe family Phyllostomidae (Chiroptera) shows wide morphological, molecular and cytogenetic variation; many disagreements regarding its phylogeny and taxonomy remains to be resolved. In this study, we use chromosome painting with whole chromosome probes from the Phyllostomidae Phyllostomus hastatus and Carollia brevicauda to determine the rearrangements among several genera of the Nullicauda group (subfamilies Gliphonycterinae, Carolliinae, Rhinophyllinae and Stenodermatinae).ResultsThese data, when compared with previously published chromosome homology maps, allow the construction of a phylogeny comparable to those previously obtained by morphological and molecular analysis. Our phylogeny is largely in agreement with that proposed with molecular data, both on relationships between the subfamilies and among genera; it confirms, for instance, that Carollia and Rhinophylla, previously considered as part of the same subfamily are, in fact, distant genera.ConclusionsThe occurrence of the karyotype considered ancestral for this family in several different branches suggests that the diversification of Phyllostomidae into many subfamilies has occurred in a short period of time. Finally, the comparison with published maps using human whole chromosome probes allows us to track some syntenic associations prior to the emergence of this family.

A large-scale multiomics analysis of wheat stem solidness and the wheat stem sawfly feeding response, and syntenic associations in barley, Brachypodium, and rice

The wheat stem sawfly (WSS), Cephus cinctus Norton (Hymenoptera: Cephidae), is an important pest of wheat and other cereals, threatening the quality and quantity of grain production. WSS larvae feed and develop inside the stem where they are protected from the external environment; therefore, pest management strategies primarily rely on host plant resistance. A major locus on the long arm of wheat chromosome 3B underlies most of the variation in stem solidness; however, the impact of stem solidness on WSS feeding has not been completely characterized. Here, we used a multiomics approach to examine the response to WSS in both solid- and semi-solid-stemmed wheat varieties. The combined transcriptomic, proteomic, and metabolomic data revealed that two important molecular pathways, phenylpropanoid and phosphate pentose, are involved in plant defense against WSS. We also detected a general downregulation of several key defense transcripts, including those encoding secondary metabolites such as DIMBOA, tricetin, and lignin, which suggested that the WSS larva might interfere with plant defense. We comparatively analyzed the stem solidness genomic region known to be associated with WSS tolerance in wild emmer, durum, and bread wheats, and described syntenic regions in the close relatives barley, Brachypodium, and rice. Additionally, microRNAs identified from the same genomic region revealed potential regulatory pathways associated with the WSS response. We propose a model outlining the molecular responses of the WSS–wheat interactions. These findings provide insight into the link between stem solidness and WSS feeding at the molecular level.

Impact of long-term chromosomal shuffling on the multispecies coalescent analysis of two anthropoid primate lineages.

Multispecies coalescent (MSC) theory assumes that gene trees inferred from individual loci are independent trials of the MSC process. As genes might be physically close in syntenic associations spanning along chromosome regions, these assumptions might be flawed in evolutionary lineages with substantial karyotypic shuffling. Neotropical primates (NP) represent an ideal case for assessing the performance of MSC methods in such scenarios because chromosome diploid number varies significantly in this lineage. To this end, we investigated the effect of sequence length on the theoretical expectations of MSC model, as well as the results of coalescent‐based tree inference methods. This was carried out by comparing NP with hominids, a lineage in which chromosome macrostructure has been stable for at least 15 million years. We found that departure from the MSC model in Neotropical primates decreased with smaller sequence fragments, where sites sharing the same evolutionary history were more frequently found than in longer fragments. This scenario probably resulted from extensive karyotypic rearrangement occurring during the radiation of NP, contrary to the comparatively stable chromosome evolution in hominids.

Distribution of Interstitial Telomeric Sequences in Primates and the Pygmy Tree Shrew (Scandentia)

It has been hypothesized that interstitial telomeric sequences (ITSs), i.e., repeated telomeric DNA sequences found at intrachromosomal sites in many vertebrates, could be correlated to chromosomal rearrangements and plasticity. To test this hypothesis, we hybridized a telomeric PNA probe through FISH on representative species of 2 primate infraorders, Strepsirrhini (Lemur catta, Otolemur garnettii, Nycticebus coucang) and Catarrhini (Erythrocebus patas, Cercopithecus petaurista, Chlorocebus aethiops, Colobus guereza), as well as on 1 species of the order Scandentia, Tupaia minor, used as an outgroup for primates in phylogenetic reconstructions. In almost all primate species analyzed, we found a telomeric pattern only. In Tupaia, the hybridization revealed many bright ITSs on at least 11 chromosome pairs, both biarmed and acrocentric. These ITS signals in Tupaia correspond to fusion points of ancestral human syntenic associations, but are also present in other chromosomes showing synteny to only a single human chromosome. This distribution pattern was compared to that of the heterochromatin regions detected through sequential C-banding performed after FISH. Our results in the analyzed species, compared with literature data on ITSs in primates, allowed us to discuss different mechanisms responsible for the origin and distribution of ITSs, supporting the correlation between rearrangements and ITSs.

Clues on Syntenic Relationship among Some Species of Oryzomyini and Akodontini Tribes (Rodentia: Sigmodontinae).

Sigmodontinae rodents represent one of the most diverse and complex components of the mammalian fauna of South America. Among them most species belongs to Oryzomyini and Akodontini tribes. The highly specific diversification observed in both tribes is characterized by diploid complements, which vary from 2n = 10 to 86. Given this diversity, a consistent hypothesis about the origin and evolution of chromosomes depends on the correct establishment of synteny analyzed in a suitable phylogenetic framework. The chromosome painting technique has been particularly useful for identifying chromosomal synteny. In order to extend our knowledge of the homeological relationships between Akodontini and Oryzomyini species, we analyzed the species Akodon montensis (2n = 24) and Thaptomys nigrita (2n = 52) both from the tribe Akodontini, with chromosome probes of Hylaeamys megacephalus (2n = 54) of the tribe Oryzomyini. The results indicate that at least 12 of the 26 autosomes of H. megacephalus show conserved synteny in A. montensis and 14 in T. nigrita. The karyotype of Akodon montensis, as well as some species of the Akodon cursor species group, results from many chromosomal fusions and therefore the syntenic associations observed probably represent synapomorphies. Our finding of a set of such associations revealed by H. megacephalus chromosome probes (6/21; 3/25; 11/16/17; and, 14/19) provides phylogenetic information for both tribes. An extension of these observations to other members of Akodontini and Oryzomyini tribes should improve our knowledge about chromosome evolution in both these groups.

Genome-wide comparative chromosome maps of Arvicola amphibius, Dicrostonyx torquatus, and Myodes rutilus.

The subfamily Arvicolinae consists of a great number of species with highly diversified karyotypes. In spite of the wide use of arvicolines in biological and medicine studies, the data on their karyotype structures are limited. Here, we made a set of painting probes from flow-sorted chromosomes of a male Palearctic collared lemming (Dicrostonyx torquatus, DTO). Together with the sets of painting probes made previously from the field vole (Microtus agrestis, MAG) and golden hamster (Mesocricetus auratus, MAU), we carried out a reciprocal chromosome painting between these three species. The three sets of probes were further hybridized onto the chromosomes of the Eurasian water vole (Arvicola amphibius) and northern red-backed vole (Myodes rutilus). We defined the diploid chromosome number in D. torquatus karyotype as 2n = 45 + Bs and showed that the system of sex chromosomes is X1X2Y1. The probes developed here provide a genomic tool-kit, which will help to investigate the evolutionary biology of the Arvicolinae rodents. Our results show that the syntenic association MAG1/17 is present not only in Arvicolinae but also in some species of Cricetinae; and thus, should not be considered as a cytogenetic signature for Arvicolinae. Although cytogenetic signature markers for the genera have not yet been found, our data provides insight into the likely ancestral karyotype of Arvicolinae. We conclude that the karyotypes of modern voles could have evolved from a common ancestral arvicoline karyotype (AAK) with 2n = 56 mainly by centric fusions and fissions.

A First Generation Comparative Chromosome Map between Guinea Pig (Cavia porcellus) and Humans.

The domesticated guinea pig, Cavia porcellus (Hystricomorpha, Rodentia), is an important laboratory species and a model for a number of human diseases. Nevertheless, genomic tools for this species are lacking; even its karyotype is poorly characterized. The guinea pig belongs to Hystricomorpha, a widespread and important group of rodents; so far the chromosomes of guinea pigs have not been compared with that of other hystricomorph species or with any other mammals. We generated full sets of chromosome-specific painting probes for the guinea pig by flow sorting and microdissection, and for the first time, mapped the chromosomal homologies between guinea pig and human by reciprocal chromosome painting. Our data demonstrate that the guinea pig karyotype has undergone extensive rearrangements: 78 synteny-conserved human autosomal segments were delimited in the guinea pig genome. The high rate of genome evolution in the guinea pig may explain why the HSA7/16 and HSA16/19 associations presumed ancestral for eutherians and the three syntenic associations (HSA1/10, 3/19, and 9/11) considered ancestral for rodents were not found in C. porcellus. The comparative chromosome map presented here is a starting point for further development of physical and genetic maps of the guinea pig as well as an aid for genome assembly assignment to specific chromosomes. Furthermore, the comparative mapping will allow a transfer of gene map data from other species. The probes developed here provide a genomic toolkit, which will make the guinea pig a key species to unravel the evolutionary biology of the Hystricomorph rodents.

Multiple sex chromosome systems in howler monkeys (Platyrrhini, Alouatta).

In light of the multiple sex chromosome systems observed in howler monkeys (Alouatta Lacépède, 1799) a combined cladistic analysis using chromosomal and molecular characters was applied to discuss the possible origin of these systems. Mesoamerican and South American howlers were karyologically compared. FISH analysis using the chromosome painting probes for the #3 and #15 human chromosomes was applied to corroborate the homeology of the sexual systems. We found that the HSA3/15 syntenic association, present in the sex chromosome systems of South American Howlers, is not present in those of Mesoamerican ones. The autosomes involved in the translocation that formed the sexual systems in the Mesoamerican and South American species are different, thus suggesting an independent origin. Parsimony analysis resolved the phylogenetic relationships among howler species, demonstrating utility of the combined approach. A hypothesis for the origin of the multiple sex chromosome systems for the genus is proposed.

The evolutionary history of HSA7/16 synteny in vertebrates: a critical interpretation of comparative cytogenetic and genome sequence data

The current work is an in silico study of data from previous publications and genome browsers, on the origin of the human synteny HSA7a/16p. The molecular composition of the chromosomal segments identified as HSA7a/16 and 7b (free or differently associated) is not yet clear. This means that a syntenic association 7/16, which can be detected by an in situ hybridization (FISH) method in different taxa, may not necessarily correspond to those of the same association in different lineages. In silico research, together with comparative cytogenetics, have been applied in order to define the composition of the 7/16 syntenic association. These results allow a confident reconstruction of the syntenic associations HSA7/16 in diverse vertebrate lineages, indicating various levels of homology, but also considerable levels of non-homology, which should elicit caution with phylogenetic interpretations. The 7/16 association represents a paradigmatic example of the complexity involved in the interpretation of comparative...

Chromosomal evolution among leaf-nosed nectarivorous bats – evidence from cross-species chromosome painting (Phyllostomidae, Chiroptera)

BackgroundNew World leaf-nosed bats, Phyllostomidae, represent a lineage of Chiroptera marked by unprecedented morphological/ecological diversity and extensive intergeneric chromosomal reorganization. There are still disagreements regarding their systematic relationships due to morphological convergence among some groups. Their history of karyotypic evolution also remains to be documented.ResultsTo better understand the evolutionary relationships within Phyllostomidae, we developed chromosome paints from the bat species Macrotus californicus. We tested the potential of these paints as phylogenetic tools by looking for chromosomal signatures in two lineages of nectarivorous phyllostomids whose independent origins have been statistically supported by molecular phylogenies. By examining the chromosomal homologies defined by chromosome painting among two representatives of the subfamily Glossophaginae (Glossophaga soricina and Anoura cultrata) and one species from the subfamily Lonchophyllinae (Lonchophylla concava), we found chromosomal correspondence in regions not previously detected by other comparative cytogenetic techniques. We proposed the corresponding human chromosomal segments for chromosomes of the investigated species and found two syntenic associations shared by G. soricina and A. cultrata.ConclusionComparative painting with whole chromosome-specific paints of M. californicus demonstrates an extensive chromosomal reorganization within the two lineages of nectarivorous phyllostomids, with a large number of chromosomes shared between M. californicus and G. soricina. We show that the evolution of nectar-feeding bats occurs mainly by reshuffling of chiropteran Evolutionarily Conserved Units (ECUs). Robertsonian fusions/fissions and inversions seem to be important modifiers of phyllostomid karyotypes, and autapomorphic character states are common within species. Macrotus californicus chromosome paints will be a valuable tool for documenting the pattern of karyotypic evolution within Phyllostomidae radiation.

The phylogenetic position of Daubentonia madagascariensis (Gmelin, 1788; primates, Strepsirhini) as revealed by chromosomal analysis

One of the major topics in primate evolution is the phylogenetic position of the bizarre Daubentonia madagascariensis (DMA, aye-aye). The principal points that have been discussed for many decades are whether the aye-aye is: (i) the sister group of primates; (ii) the sister group of strepsirhines; or (iii) the sister group of lemurs. Very little is known about Daubentonia evolution, particularly on the chromosomal background. The present report focuses on the chromosomal history of this species. We used available chromosome painting data as the main source to identify conserved chromosomes, chromosomal segments and syntenic associations that have characterized the aye-aye karyotype. The dataset includes 47 characters that have been subjected to a concatenated analysis using maximum parsimony (MP) and Bayesian inference (BI). Both MP and BI topologies show Daubentonia as an independent monophyletic lineage, sister group of all other Strepsirhini. Further, both trees have weak statistical support as result ...

Chromosome Painting of the Pygmy Tree Shrew Shows that No Derived Cytogenetic Traits Link Primates and Scandentia

We hybridized human chromosome paints on metaphases of the pygmy tree shrew (Tupaia minor, Scandentia). The lack of the ancestral mammalian 4/8 association in both Primates and Scandentia was long considered a cytogenetic landmark that phylogenetically linked these mammalian orders. However, our results show that the association 4/8 is present in Tupaia along with not previously reported associations for 1/18 and 7/10. Altogether there are 11 syntenic associations of human chromosome segments in the pygmy tree shrew karyotype: 1/18, 2/21, 3/21, 4/8, 7/10, 7/16, 11/20, 12/22 (twice), 14/15 and 16/19. Our data remove any cytogenetic evidence that Scandentia has a preferential phylogenetic relationship with Primates.

Molecular cytogenetic and genomic insights into chromosomal evolution

This review summarizes aspects of the extensive literature on the patterns and processes underpinning chromosomal evolution in vertebrates and especially placental mammals. It highlights the growing synergy between molecular cytogenetics and comparative genomics, particularly with respect to fully or partially sequenced genomes, and provides novel insights into changes in chromosome number and structure across deep division of the vertebrate tree of life. The examination of basal numbers in the deeper branches of the vertebrate tree suggest a haploid (n) chromosome number of 10-13 in an ancestral vertebrate, with modest increases in tetrapods and amniotes most probably by chromosomal fissioning. Information drawn largely from cross-species chromosome painting in the data-dense Placentalia permits the confident reconstruction of an ancestral karyotype comprising n=23 chromosomes that is similarly retained in Boreoeutheria. Using in silico genome-wide scans that include the newly released frog genome we show that of the nine ancient syntenies detected in conserved karyotypes of extant placentals (thought likely to reflect the structure of ancestral chromosomes), the human syntenic segmental associations 3p/21, 4pq/8p, 7a/16p, 14/15, 12qt/22q and 12pq/22qt predate the divergence of tetrapods. These findings underscore the enhanced quality of ancestral reconstructions based on the integrative molecular cytogenetic and comparative genomic approaches that collectively highlight a pattern of conserved syntenic associations that extends back ∼360 million years ago.

Karyotype Evolution of Eulipotyphla (Insectivora): The Genome Homology of Seven Sorex Species Revealed by Comparative Chromosome Painting and Banding Data

The genus Sorex is one of the most successful genera of Eulipotyphla. Species of this genus are characterized by a striking chromosome variability including XY1Y2 sex chromosome systems and exceptional chromosomal polymorphisms within and between populations. To study chromosomal evolution of the genus in detail, we performed cross-species chromosome painting of 7 Sorex species with S. granarius and S. araneus whole-chromosome probes and found that the tundra shrew S. tundrensis has the most rearranged karyotype among these. We reconstructed robust phylogeny of the genus Sorex based on revealed conserved chromosomal segments and syntenic associations. About 16 rearrangements led to formation of 2 major Palearctic groups after their divergence from the common ancestor: the S. araneus group (10 fusions and 1 fission) and the S. minutus group (5 fusions). Further chromosomal evolution of the 12 species inside the groups, including 5 previously investigated species, was accompanied by multiple reshuffling events: 39 fusions, 20 centromere shifts and 10 fissions. The rate of chromosomal exchanges upon formation of the genus was close to the average rate for eutherians, but increased during recent (about 6–3 million years ago) speciation within Sorex. We propose that a plausible ancestral Sorex karyotype consists of 56 elements. It underwent 20 chromosome rearrangements from the boreoeutherian ancestor, with 14 chromosomes retaining the conserved state. The set of genus-specific chromosome signatures was drawn from the human (HSA)-shrew comparative map (HSA3/12/22, 8/19/3/21, 2/13, 3/18, 11/17, 12/15 and 1/12/22). The syntenic association HSA4/20, that was previously proposed as a common trait of all Eulipotyphla species, is shown here to be an apomorphic trait of S. araneus.

Comparative Chromosome Maps of Neotropical Rodents Necromys lasiurus and Thaptomys nigrita (Cricetidae) Established by ZOO-FISH

This work presents chromosome homology maps between Mus musculus (MMU) and 2 South American rodent species from the Cricetidae group: Necromys lasiurus (NLA, 2n = 34) and Thaptomys nigrita (TNI, 2n = 52), established by ZOO-FISH using mouse chromosome-specific painting probes. Extending previous molecular cytogenetic studies in Neotropical rodents, the purpose of this work was to delineate evolutionary chromosomal rearrangements in Cricetidae rodents and to reconstruct the phylogenetic relationships among the Akodontini species. Our phylogenetic reconstruction by maximum parsimony analysis of chromosomal characters confirmed one consistent clade of all Neotropical rodents studied so far. In both species analyzed here, we observed the syntenic association of chromosome segments homologous to MMU 8/13, suggesting that this chromosome form is a synapomorphic trait exclusive to Neotropical rodents. Further, the previously described Akodontini-specific syntenic associations MMU 3/18 and MMU 6/12 were observed in N.lasiurus but not in T. nigrita, although the latter species is considered a member of the Akodontini tribe by some authors. Finally, and in agreement with this finding, N.lasiurus and Akodon serrensis share the derived fission of MMU 13, which places them as basal sister clades within Akodontini.

A Phylogenetic Analysis of Human Syntenies Revealed by Chromosome Painting in Euarchontoglires Orders

To search for cytogenetic signatures that can help to clarify evolutionary affinities among the five orders within the Euarchontoglires clade, we focused on associations of conserved syntenic blocks that have been accumulated in the karyotypes of Primates (Strepsirhini and Haplorhini), five families of Rodentia, Scandentia (Tupaia belangeri), Dermoptera (Galeopterus variegatus) and Lagomorpha (Oryctolagus cuniculus). We examined available chromosome painting data to identify conserved chromosomes and chromosomal segments, and syntenic associations likely to have characterized the ancestral eutherian karyotype. The data set includes 161 characters that have been subjected to a concatenated analysis using maximum parsimony (MP) and Bayesian inference (BI). The phylogenetic pattern recovered is generally consistent with reconstructions based on molecular and morphological data (particularly with respect to higher systematic groupings), but there are several anomalies (e.g., in the position of the lagomorphs). Both MP and BI topologies have weak statistical support, as a consequence of the high number of autapomorphic and homoplastic character states that have evolved during the history of the clade. The vast majority of derived associations are located on the terminal portions of the branches, and very few can be identified to support deeper divergences in the tree, indicating that chromosomal structures are far more fluid that was previously recognized. The high levels of homoplasy reflected in our data suggest that the number of possible syntenic character states is limited by chromosomal structures, and the same associations occur repeatedly.

Recapitulating the evolution of Afrotheria: 57 genes and rare genomic changes (RGCs) consolidate their history

The decipherment of higher level relationships among the orders of Afrotheria – an extraordinary assumption in mammalian evolution – constitutes one of the major disputes in the evolutionary history of mammals. Recent comprehensive studies of various genomic data, including mitochondrial and nuclear DNA sequences, chromosomal syntenic associations and retroposon insertions support strongly the monophyly of Afrotheria. However, the relationships within Afrotheria have remained ambiguous and there is a necessity for a more sophisticated analysis (i.e. combination of gene phylogeny and Rare Genomic Changes (RGCs)), which could aid in the comprehension of the evolutionary history of this old group of mammals. The present study investigated the phylogenetic relationships within Afrotheria by analysing a data set of coding and non-coding sequences (∼32 000 bp) comprising 57 orthologous genes and 31 RGCs, such as chromosomal associations and retroposon insertions, and re-evaluated a molecular timescale for afrotherian mammals using a Bayesian relaxed clock approach. The interordinal afrotherians phylogeny presented here contributed to the elucidation of the evolutionary history of this ancient clade of mammals, which is one of the most unorthodox proposals in mammalian biology. This is critical not only for understanding how Afrotheria evolved in Africa, but also to comprehend the early biogeographical history of placental mammals.

Genome-Wide Comparative Chromosome Map between Human and the Forrest’s Pika (Ochotona forresti) Established by Cross-Species Chromosome Painting: Further Support for the Glires Hypothesis

Comparative genomic data for ochotonids (pikas) are important for understanding the karyotype evolution of lagomorphs. Here, we have established the first genome-wide chromosomal homologies between human and the Forrest’s pika (Ochotona forresti, 2n = 54) by cross-species chromosome painting. Integration of our map with the published comparative chromosome map between human and rabbit has enabled the establishment of an indirect homology map between Forrest’s pika and domestic rabbit (Oryctolagus cuniculus, 2n = 44), representing the 2 Lagomorpha families: Leporidae and Ochotonidae. Our results demonstrate that (1) most of the proposed ancestral eutherian syntenies or syntenic associations have been retained in the O. forresti genome; (2) the HSA1/10p association, one of the 2 signature rearrangements that were proposed to support the grouping of the orders Lagomorpha and Rodentia into a monophyletic clade called Glires, is also present in the O. forresti genome; and (3) Robertsonian translocations have contributed to the karyotype differences between O. forresti and O. cuniculus.