Deeply conserved synteny and the evolution of metazoan chromosomes

Simakov, Oleg; Bredeson, Jessen V.; Berkoff, Kodiak C.; Marlétaz, Ferdinand; Mitros, Therese; Schultz, Darrin T.; O’Connell, Brendan; Dear, Paul H.; Martínez, Daniel E.; Steele, Robert E.; Green, Edward; David, Charles N.; Rokhsar, Daniel S.

doi:10.1126/sciadv.abi5884

Cited by 131 publications

(273 citation statements)

References 99 publications

(178 reference statements)

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“…Evolutionary comparisons will shed new light on the origin of cell nuclei 92 and the evolution of metazoan chromosomes 93 . Based on the emerging evidence that physical compaction and decompaction of chromatin nanodomains play a major role in gene regulation not only in eukaryotes but also in prokaryotes 94 , it is interesting to explore to which extent differences between high-resolution DNA density maps of different cell types 90 correlate with and may predict global transcriptional differences.…”

Section: Discussionmentioning

confidence: 99%

True-to-scale DNA-density maps correlate with major accessibility differences between active and inactive chromatin

Gelléri

Chen

Szczurek

et al. 2022

Preprint

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Chromatin compaction differences may have a strong impact on accessibility of individual macromolecules and macromolecular assemblies to their DNA target sites. Estimates based on fluorescence microscopy with conventional resolution, however, suggested only modest compaction differences (~2-10x) between active and inactive nuclear compartments (ANC and INC). Here, we present maps of nuclear landscapes with true-to-scale DNA-densities, ranging from <5 Mbp/μm3 to >300 Mbp/μm3. Maps were generated from individual human and mouse cell nuclei with single-molecule localization microscopy at ~20 nm lateral and ~100 nm axial resolution and supplemented by electron spectroscopic imaging. Live cell microinjection experiments with 20 nm and 40 nm sized fluorescent beads, corresponding to macromolecular assemblies for transcription and replication, indicated movements within the ANC, but exclusion from the INC. In line with previous studies of transcription, pulse-chase labeling experiments of DNA demonstrated replication within the ANC, followed by re-location of replicated, inactive chromatin into the INC.

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Section: Discussionmentioning

confidence: 99%

True-to-scale DNA-density maps correlate with major accessibility differences between active and inactive chromatin

Gelléri

Chen

Szczurek

et al. 2022

Preprint

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“…Many vertebrate evolutionary innovations were influenced by the drastic genomic reorganizations caused by two rounds of whole genome duplication (WGD). The ancestral 18 chordate chromosomes were duplicated, reshuffled and rearranged to give rise to the diversity of existing karyotypes in vertebrates 4 . Concomitantly, the pervasive loss of paralogous genes after the WGD produced gene deserts enriched in regulatory elements 5 .…”

Section: Mainmentioning

confidence: 99%

The little skate genome and the evolutionary emergence of wing-like fin appendages

Marlétaz

Calle‐Mustienes

Acemel

et al. 2022

Preprint

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Skates are cartilaginous fish whose novel body plan features remarkably enlarged wing-like pectoral fins that allow them to thrive in benthic environments. The molecular underpinnings of this unique trait, however, remain elusive. Here we investigate the origin of this phenotypic innovation by developing the little skate Leucoraja erinacea as a genomically enabled model. Analysis of a high-quality chromosome-scale genome sequence for the little skate shows that it preserves many ancestral jawed vertebrate features compared with other sequenced genomes, including numerous ancient microchromosomes. Combining genome comparisons with extensive regulatory datasets in developing fins (gene expression, chromatin occupancy and three-dimensional (3D) conformation) we find skate-specific genomic rearrangements that alter the 3D regulatory landscape of genes involved in the planar cell polarity (PCP) pathway. Functional inhibition of PCP signaling resulted in marked reduction of anterior fin size, confirming this pathway as a major contributor of batoid fin morphology. We also identified a fin-specific enhancer that interacts with 3' HOX genes, consistent with the redeployment of Hox gene expression in anterior pectoral fins, and confirmed the potential of this element to activate transcription in the anterior fin using zebrafish reporter assays. Our findings underscore the central role of genome reorganizations and regulatory variation in the evolution of phenotypes, shedding light on the molecular origin of an enigmatic trait.

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“…It is interesting that we identi ed a shared chromosomal fusion event by Amborellales and Nymphaeales, which may further support their sister relationship. Chromosomal fusions, as the major macrostructural genomic changes, may be homoplasious or reversed during the long evolutionary history of diverse plants and animals 34,35 . However, the rapid radiation of only three early angiosperm lineages within a very short timescale, as indicated by various analyses, seems to reduce such a probability for the recovered shared NCF event by Amborellales and Nymphaeales having occurred although we could not exclude it totally.…”

Section: Discussionmentioning

confidence: 99%

Early diversification and karyotype evolution of flowering plants

Sun

Yang

Liu³

et al. 2022

Preprint

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Flowering plants (angiosperms) dominate our planet and sustain all life on Earth. However, evolutionary relationships among the angiosperm lineages that diverged early – Amborellales, Nymphaeales, Austrobaileyales and Mesangiospermae, which further comprises monocots and other four clades – have remained highly disputed likely because of their rapid diversification promoted by an ancestral polyploidization event. Here, we present high-quality chromosomal-level genome assemblies of two species – star anise (Illicium verum: 12.5 Gb with a large size) in the Austrobaileyales and calamus (Acorus gramineus) representing the sister lineage to all other extant monocots. These two genomes filled the final gaps of all genomic representatives for major angiosperm lineages. Our phylogenetic analyses of collinear genes support Amborellales and Nymphaeales as sister lineages and they, together with Austrobaileyales and monocots are successively sister to other Mesangiospermae clades. Based on chromosome-like synteny blocks shared between extant genomes, we constructed the ancestral angiosperm karyotype to be x=16. We independently established evolutionary relationships for all sampled species based on shared polyploidizations and chromosomal fusions from the common ancestral karyotype. This phylogenetic relationship is congruent with that from collinear genes, especially the finding that Amborellales and Nymphaeales shared a rare chromosomal fusion not seen in other angiosperms. These results advance our understanding and shed new lights on early diversification and karyotype evolution of flowering plants.

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Deeply conserved synteny and the evolution of metazoan chromosomes

Cited by 131 publications

References 99 publications

True-to-scale DNA-density maps correlate with major accessibility differences between active and inactive chromatin

True-to-scale DNA-density maps correlate with major accessibility differences between active and inactive chromatin

The little skate genome and the evolutionary emergence of wing-like fin appendages

Early diversification and karyotype evolution of flowering plants

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