Annelid Comparative Genomics and the Evolution of Massive Lineage-specific Genome Rearrangement in Bilaterians

Molecular Biology and Evolution, Journal Year: 2024, Volume and Issue: 41(9)

Published: Aug. 13, 2024

Abstract The organization of genomes into chromosomes is critical for processes such as genetic recombination, environmental adaptation, and speciation. All animals with bilateral symmetry inherited a genome structure from their last common ancestor that has been highly conserved in some taxa but seemingly unconstrained others. However, the evolutionary forces driving these differences by which they emerge have remained largely uncharacterized. Here, we analyze across phylum Annelida using 23 chromosome-level annelid genomes. We find while many lineages maintained bilaterian structure, Clitellata, group containing leeches earthworms, possesses completely scrambled develop rearrangement index to quantify extent evolution show that, compared bilaterians, earthworms among most rearranged any currently sampled species. further can be classified two distinct categories—high low rearrangement—largely influenced presence or absence, respectively, chromosome fission events. Our findings demonstrate animal variable within reveal occur both gradual, stepwise fashion, rapid, all-encompassing changes over short timescales.

Language: Английский

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​​Fusion, fission, and scrambling of the bilaterian genome in Bryozoa

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2024, Volume and Issue: unknown

Published: Feb. 16, 2024

Abstract Groups of orthologous genes are commonly found together on the same chromosome over vast evolutionary distances. This extensive physical gene linkage, known as macrosynteny, is seen between bilaterian phyla divergent Chordata, Echinodermata, Mollusca, and Nemertea. Here, we report a unique pattern genome evolution in Bryozoa, an understudied phylum colonial invertebrates. Using comparative genomics, reconstruct chromosomal history five bryozoans. Multiple ancient fusions followed by mixing led to near-complete loss linkage groups ancestor extant A second wave rearrangements, including fission, then occurred independently two bryozoan classes, further scrambling genomes. We also discover at least derived fusion events shared bryozoans brachiopods, supporting traditional but highly debated Lophophorata hypothesis. Finally, show that fission processes partitioning from Hox clusters onto multiple chromosomes. Our findings demonstrate canonical structure has been lost across all studied representatives entire phylum; reveal group can occur very frequently specific lineages; provide powerful source phylogenetic information.

Language: Английский

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Multiplex single-cell analysis of serotonergic neuron function in planarians reveals widespread effects in diverse cell types

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2024, Volume and Issue: unknown

Published: March 2, 2024

Abstract Neurons function by interacting with each other and cell types, often exerting organism-wide regulation. Serotonergic neurons play a systemic role in processes such as appetite, sleep motor control. Functional studies the planarian Schmidtea mediterranea have shown that impairment of serotonergic results effects. Studying tissues they interact is challenging using either bulk or single-cell analysis techniques. While methods merge information from all show promise overcoming this limitation. However, current approaches encounter challenges including stress dissociation, high cost, multiplexing capacity, batch effects, replication statistical analysis. Here we used ACME SPLiT-seq to generate multiplex neuron planarians inhibiting pitx lhx1/5-1 , two transcription factors expressed them. We recovered transcriptomic profiles 47,292 cells knockdown control animals, biological technical replicates. Our epidermal, muscular recently described parenchymal types are affected most impairment. By computationally dissecting type, elucidated gene expression changes each, epidermis cilia genes myofiber muscle. Interestingly, downregulate involved neurotransmitter recycling, suggesting glial-like these enigmatic types. will allow disentangling complexity inhibition studying downstream effectors tissues, offer new data on planarians. Ultimately, our pave way for complex phenotypes through transcriptomics.

Language: Английский

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A comparative roadmap of PIWI-interacting RNAs across seven species reveals insights into de novo piRNA-precursor formation in mammals

Cell Reports, Journal Year: 2024, Volume and Issue: 43(10), P. 114777 - 114777

Published: Sept. 19, 2024

Language: Английский

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Annelid comparative genomics and the evolution of massive lineage-specific genome rearrangement in bilaterians

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2024, Volume and Issue: unknown

Published: May 18, 2024

Abstract The organization of genomes into chromosomes is critical for processes such as genetic recombination, environmental adaptation, and speciation. All animals with bilateral symmetry inherited a genome structure from their last common ancestor that has been highly conserved in some taxa but seemingly unconstrained others. However, the evolutionary forces driving these differences by which they emerge have remained largely uncharacterized. Here we analyze across phylum Annelida using 23 chromosome-level annelid genomes. We find while most annelids maintained bilaterian structure, group containing leeches earthworms possesses completely scrambled develop rearrangement index to quantify extent evolution show rearranged any currently sampled bilaterian. further can be classified two distinct categories—high low rearrangement—largely influenced presence or absence, respectively, chromosome fission events. Our findings demonstrate animal variable within reveal occur both gradual, stepwise fashion rapid, all-encompassing changes over short timescales.

Language: Английский

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Conservation of animal genome structure is the exception not the rule

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2024, Volume and Issue: unknown

Published: Aug. 6, 2024

Abstract Species from diverse animal lineages have retained groups of orthologous genes together on the same chromosomes for over half a billion years since their last common ancestor. However, by examining interchromosomal rearrangements across all major bilaterian groups, we show that cases high-fidelity genome structure conservation are unexpectedly rare. Large-scale restructuring events pervasive, correlate with increased rates protein sequence evolution, and may contribute to adaptation diversity.

Language: Английский

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A Comparative Roadmap of PIWI-Interacting RNAs (piRNAs) Across Seven Species Reveals Insights Into de novo piRNA Precursor Formation in Mammals

Published: Jan. 1, 2024

PIWI-interacting RNAs (piRNAs) play a crucial role in safeguarding genome integrity by silencing mobile genetic elements. From flies to human, piRNAs originate from long single-stranded precursors encoded genomic piRNA clusters. How clusters form adapt novel invaders and evolve maintain protection, remain key outstanding questions. Here, we generated roadmap of across seven species that highlights both similarities variations. In mammals, identified transcriptional readthrough as mechanism generate transposon insertions downstream-of-genes (piC-DoGs). Together with the well-known stress-dependent DoG-transcripts, our findings suggest molecular for formation response retroviral invasion. Finally, class dynamic humans, underscoring unique features human germ cell biology. Our results advance understanding conserved principles species-specific variations biology provide tools future studies.

Language: Английский

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Chromatin remodeling protein BPTF regulates transcriptional stability in planarian stem cells

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2024, Volume and Issue: unknown

Published: May 26, 2024

Trimethylation of histone H3 lysine 4 (H3K4me3) correlates strongly with gene expression in many different organisms, yet the question whether it plays a causal role transcriptional activity remains unresolved. Although H3K4me3 does not directly affect chromatin accessibility, can indirectly genome accessibility by recruiting ATP-dependent remodeling complex NuRF (Nucleosome Remodeling Factor). The largest subunit NuRF, BPTF/NURF301, binds specifically and recruits to loci marked this modification. Studies have shown that strength duration BPTF binding likely also depends on additional features at these loci, such as acetylation variant proteins. However, exact details recruitment mechanism vary between studies largely been tested vitro. Here, we use stem cells isolated from live planarian animals investigate regulating vivo. We find operates promoters is most effective facilitating transcription genes Set1-dependent peaks, which are significantly broader than those added methyltransferase MLL1/2. Moreover, essential for cell biology its loss function phenotype mimics Set1 knockdown. Together, data suggest important mediators both vivo function.

Language: Английский

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Axis reset is rate limiting for onset of whole-body regenerative abilities during planarian development

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2024, Volume and Issue: unknown

Published: July 23, 2024

SUMMARY Few studies have investigated whether or how regenerative abilities vary across developmental stages of animal life cycles. Determining mechanisms that promote limit regeneration in certain cycle may pinpoint the most critical factors for successful and suggest strategies reverse-engineering responses therapeutic settings. In contrast to many mammalian systems, which typically show a loss with age, planarian flatworms remain highly throughout adulthood. The robust reproductive capabilities Schmidtea polychroa ( Spol ) make them an ideal model determine when competence is established during development. We report gradually acquires whole body late embryonic early juvenile stages. Posterior (tail) are constitutive, whereas anterior (head) dependent on stage, tissue composition amputated fragment, axial position cut plane. Stem-like cells required, but not sufficient, onset head ability. propose regulation main axis reset, specifically ability remake organizing center, rate-limiting factor establishment whole-body competence. Supporting this hypothesis, knock-down canonical Wnt pathway effector β-catenin-1, posterior determinant, induces precocious under conditions normally incompetent. Our results emerges through interactions between cycling stem-like cells, cellular source new tissue, developing adult tissue(s) harboring patterning information.

Language: Английский

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RNaseH-based ribodepletion of total planarian RNA improves detection of longer and non-polyadenylated transcripts

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2024, Volume and Issue: unknown

Published: July 21, 2024

The overwhelming majority of RNA species isolated from cells or tissues using organic extraction are ribosomal RNAs (rRNA), whereas a relatively small percentage messenger (mRNA). For studies that seek to detect mRNA transcripts and measure changes in their expression, this lopsided ratio desired undesired creates significant challenge obtaining sensitive reproducible results. One method for improving detection is selectively amplify polyadenylated (polyA) molecules when generating RNA-seq libraries, strategy generally very successful many species. However, less effective starting with total some e.g., the planarian

Language: Английский

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