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 94 publications

(181 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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“…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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“…Indeed, even in species with divergent germ line segregation strategies, conserved functional interactions at the post-translational level are required for primordial germ cell specification 55,56 . The observation that metazoan chromosomes have deeply conserved gene linkages, some stretching as far back as unicellular organisms, provides a plausible mechanistic basis for the persistence of ancient transcriptional programs 57 . Accordingly, one can speculate that chromatin interactions have been preserved throughout metazoan evolution to ensure both gene regulation and chromosome pairing during meiosis.…”

Section: Discussionmentioning

confidence: 99%

The conserved genetic program of male germ cells uncovers ancient regulators of human spermatogenesis

Correia

Almeida

Wyrwoll

et al. 2022

Preprint

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Germ cells provide the cellular basis for sexual reproduction in multicellular animals. In males, germ cells differentiate into sperm, one of the most morphologically diverse eukaryotic cell types. Owing both to this remarkable diversity and to the rapid evolution of reproduction-related genes, the transcriptional program of male germ cells is widely regarded as divergent across species1,2. However, the possibility that these cells retain a distinctive evolutionarily-conserved genetic basis remains largely unexplored. Here we show, using phylostratigraphy, that the complex male germ cell transcriptome has an old evolutionary origin shared between vertebrate and invertebrate species. Through network analysis of the human, mouse and fruit fly meiotic transcriptome, we establish that old genes serve as a genetic scaffold from which complexity has evolved, and identify a core set of 79 ancient functional interactions at the heart of male germ cell identity. By silencing a cohort of 920 candidate genes likely to affect the acquisition and maintenance of this identity, we uncover 164 previously unknown spermatogenesis genes. Integrating this information with whole-exome sequencing data from azoospermic men reveals three novel genetic causes of human male infertility associated with germ cell defects shared across more than 600 million years of evolution. Our results demonstrate the central role of old genes in germ cell function and illustrate how comparative biology can be an important tool in medical genetics. We anticipate that our open-access and easily-adaptable interdisciplinary research platform will be harnessed in the context of other cell types and diseases.

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Deeply conserved synteny and the evolution of metazoan chromosomes

Cited by 94 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

Early diversification and karyotype evolution of flowering plants

The conserved genetic program of male germ cells uncovers ancient regulators of human spermatogenesis

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