scholarly journals Cross-species incompatibility between a DNA satellite and a chromatin protein poisons germline genome integrity

2021 ◽  
Author(s):  
Cara L Brand ◽  
Mia T Levine
Keyword(s):  
Satellite Dna ◽  
Rapid Evolution ◽  
Genome Integrity ◽  
Dna Repeats ◽  
Chromatin Protein ◽  
Genetic Rescue ◽  
Chromatin Proteins ◽  
Genomic Regions ◽  
Female Germline ◽  
Nuclear Processes

Satellite DNA spans megabases of eukaryotic genome sequence. These vast stretches of tandem DNA repeats undergo high rates of sequence turnover, resulting in radically different satellite DNA landscapes between closely related species. Such extreme evolutionary plasticity suggests that satellite DNA accumulates mutations with no functional consequence. Paradoxically, satellite-rich genomic regions support essential, conserved nuclear processes, including chromosome segregation, dosage compensation, and nuclear structure. A leading resolution to this paradox is that deleterious alterations to satellite DNA trigger adaptive evolution of chromatin proteins to preserve these essential functions. Here we experimentally test this model of coevolution between chromatin proteins and DNA satellites by conducting an evolution-guided manipulation of both protein and satellite. We focused on an adaptively evolving, ovary-enriched chromatin protein, called Maternal Haploid (MH) from Drosophila. MH co-localizes with an 11 Mb 359-bp satellite array present in Drosophila melanogaster but absent in its sister species, D. simulans. Using CRISPR/Cas9-mediated transgenesis, we swapped the D. simulans version of MH into D. melanogaster. We discovered that D. melanogaster females encoding only the D. simulans mh (mh[sim]) do not phenocopy the mh null mutation. Instead, MH[sim] is toxic to D. melanogaster ovaries: we observed elevated ovarian cell death, reduced ovary size, and subfertility in mh[sim] females. Using both cell biological and genetic approaches, we demonstrate that MH[sim] poisons oogenesis through a DNA damage pathway. Remarkably, deleting the D. melanogaster-specific 359 satellite array from mh[sim] females completely restores female germline genome integrity and fertility. This genetic rescue offers experimental evidence that rapid evolution resulted in a cross-species incompatibility between the 359 satellite and MH. These data suggest that coevolution between ostensibly inert repetitive DNA and essential chromatin proteins preserves germline genome integrity.

scholarly journals Too much too many: comparative analysis of morabine grasshopper genomes reveals highly abundant transposable elements and rapidly proliferating satellite DNA repeats

2020 ◽  
Author(s):  
Octavio M. Palacios-Gimenez ◽  
Julia Koelman ◽  
Marc Palmada Flores ◽  
Tessa M. Bradford ◽  
Karl K. Jones ◽  
...  
Keyword(s):  
Transposable Elements ◽  
Genome Evolution ◽  
Repetitive Dna ◽  
Dna Sequences ◽  
Satellite Dna ◽  
Species Complex ◽  
Rapid Evolution ◽  
Dna Repeats ◽  
Large Genome ◽  
Chromosomal Races

BackgroundThe repeatome, the collection of repetitive DNA sequences represented by transposable elements (TEs) and tandemly repeated satellite DNA (satDNAs), is found in high proportion in organisms across the tree of life. Grasshoppers have large genomes (average 9 Gb), containing large amounts of repetitive DNA which has hampered progress in assembling reference genomes. Here we combined linked-read genomics with transcriptomics to assemble, characterize, and compare the structure of the repeatome and its contribution to genome evolution, in four chromosomal races of the morabine grasshopper Vandiemenella viatica species complex.ResultsWe obtained linked-read genome assemblies of 2.73-3.27 Gb from estimated genome sizes of 4.26-5.07 Gb DNA per haploid genome of the four chromosomal races of V. viatica. These constitute the third largest insect genomes assembled so far (the largest being two locust grasshoppers). Combining complementary annotation tools and manual curation, we found a large diversity of TEs and satDNAs constituting 66 to 75 % per genome assembly. A comparison of sequence divergence within the TE classes revealed massive accumulation of recent TEs in all four races (314-463 Mb per assembly), indicating that their large genome size is likely due to similar rates of TE accumulation across the four races. Transcriptome sequencing showed more biased TE expression in reproductive tissues than somatic tissues, implying permissive transcription in gametogenesis. Out of 129 satDNA families, 102 satDNA families were shared among the four chromosomal races, which likely represent a repertoire of satDNA families in the ancestor of the V. viatica chromosomal races. Notably, 50 of these shared satDNA families underwent differential proliferation since the recent diversification of the V. viatica species complex.ConclusionIn-depth annotation of the repeatome in morabine grasshoppers provided new insights into the genome evolution of Orthoptera. Our TEs analysis revealed a massive recent accumulation of TEs equivalent to the size of entire Drosophila genomes, which likely explains the large genome sizes in grasshoppers. Although the TE and satDNA repertoires were rather similar between races, the patterns of TE expression and satDNA proliferation suggest rapid evolution of grasshopper genomes on recent timescales.

scholarly journals Defective satellite DNA clustering into chromocenters underlies hybrid incompatibility in Drosophila

2021 ◽  
Author(s):  
Madhav Jagannathan ◽  
Yukiko M Yamashita
Keyword(s):  
Satellite Dna ◽  
Rapid Evolution ◽  
Dna Binding Proteins ◽  
Dna Repeats ◽  
Hybrid Cells ◽  
Entire Genome ◽  
Closely Related Species ◽  
Hybrid Incompatibility ◽  
Cluster Satellite ◽  
Single Nucleus

Although rapid evolution of pericentromeric satellite DNA repeats is theorized to promote hybrid incompatibility (HI), how divergent repeats affect hybrid cells remains poorly understood. Recently, we demonstrated that sequence-specific DNA-binding proteins cluster satellite DNA from multiple chromosomes into chromocenters, thereby bundling chromosomes to maintain the entire genome in a single nucleus. Here we show that ineffective clustering of divergent satellite DNA in the cells of Drosophila hybrids results in chromocenter disruption, associated micronuclei formation and tissue atrophy. We further demonstrate that previously identified HI factors trigger chromocenter disruption and micronuclei in hybrids, linking their function to a conserved cellular process. Together, we propose a unifying framework that explains how the widely observed satellite DNA divergence between closely related species can cause reproductive isolation.

Rapid Evolution of Horse Satellite DNA

Genomics ◽  
1993 ◽  
Vol 18 (1) ◽  
pp. 113-117 ◽  
Author(s):  
Edwin R. Wijers ◽  
Carla Zijlstra ◽  
Johannes A. Lenstra
Keyword(s):  
Satellite Dna ◽  
Rapid Evolution

scholarly journals Why Do Centromeres Evolve So Fast: BIR Replication, Hypermutation, Transposition, and Molecular-Drive

2020 ◽  
Author(s):  
William Rice
Keyword(s):  
Rapid Evolution ◽  
Evolutionary Process ◽  
Epigenetic Mark ◽  
Replication Forks ◽  
Nucleotide Substitutions ◽  
Molecular Drive ◽  
Repeat Structure ◽  
Repeat Units ◽  
Initiation Of Replication ◽  
Genomic Regions

Centromeres are among the fastest evolving genomic regions in a diverse array of organisms. The evolutionary process driving this rapid evolution has not been unambiguously established. Here I integrate diverse information to motivate a model in which centromeres evolve rapidly because of their intrinsic molecular phenotype: they tightly bind centromeric proteins throughout the cell cycle. DNA-bound proteins have been shown to cause stalling and collapse of DNA replication forks in many genomic regions, including centromeres. Collapsed replication forks generate one-sided double strand breaks (DSBs) that are repaired by the Break-Induced Repair (BIR) pathway. Here I show why this repair is expected to generate tandem repeat structure and three key features at centromeres: i) increased nucleotide substitution mutation rates, ii) out-of- register re-initiation of replication that leads to indels spanning one or more repeat units, and iii) elevated rates of large and small transpositions within centromeres and between genomic regions. These phenotypes lead to: i) a rapid rate of nucleotide substitutions within a clade of centromeric sequences, ii) continual turnover of monomers within centromeres that fosters molecular-drift and molecular-drive, and iii) recurrent quantum leaps in centromere sequence due to the formation of mosaic monomers and new sequences transposed into non-homologous centromeres. These features are plausibly the major reason centromeres evolve so rapidly. I also speculate on how the DNA sequence of centromeres might perpetually coevolve with the protein sequence of histone CENH3 –the major epigenetic mark of centromeres.

Evolutionary dynamics of satellite DNA repeats from Phaseolus beans

PROTOPLASMA ◽  
2016 ◽  
Vol 254 (2) ◽  
pp. 791-801 ◽  
Author(s):  
Tiago Ribeiro ◽  
Karla G. B. dos Santos ◽  
Manon M. S. Richard ◽  
Mireille Sévignac ◽  
Vincent Thareau ◽  
...  
Keyword(s):  
Satellite Dna ◽  
Evolutionary Dynamics ◽  
Dna Repeats

Satellite DNA in Plants: More than Just Rubbish

2015 ◽  
Vol 146 (2) ◽  
pp. 153-170 ◽  
Author(s):  
Manuel A. Garrido-Ramos
Keyword(s):  
Dna Sequences ◽  
Satellite Dna ◽  
Dna Repeats ◽  
Satellite Dnas ◽  
Factors Affecting ◽  
Functional Roles ◽  
Tandem Repeat Sequences ◽  
Satellite Repeats ◽  
History Of ◽  
Main Components

For decades, satellite DNAs have been the hidden part of genomes. Initially considered as junk DNA, there is currently an increasing appreciation of the functional significance of satellite DNA repeats and of their sequences. Satellite DNA families accumulate in the heterochromatin in different parts of the eukaryotic chromosomes, mainly in pericentromeric and subtelomeric regions, but they also span the functional centromere. Tandem repeat sequences may spread from subtelomeric to interstitial loci, leading to the formation of chromosome-specific loci or to the accumulation in equilocal sites in different chromosomes. They also appear as the main components of the heterochromatin in the sex-specific region of sex chromosomes. Satellite DNA, required for chromosome organization, also plays a role in pairing and segregation. Some satellite repeats are transcribed and can participate in the formation and maintenance of heterochromatin structure and in the modulation of gene expression. In addition to the identification of the different satellite DNA families, their characteristics and location, we are interested in determining their impact on the genomes, by identifying the mechanisms leading to their appearance and amplification as well as in understanding how they change over time, the factors affecting these changes, and the influence exerted by the evolutionary history of the organisms. On the other hand, satellite DNA sequences are rapidly evolving sequences that may cause reproductive barriers between organisms and promote speciation. The accumulation of experimental data collected in recent years and the emergence of new approaches based on next-generation sequencing and high-throughput genome analysis are opening new perspectives that are changing our understanding of satellite DNA. This review examines recent data to provide a timely update on the overall information gathered about this part of the genome, focusing on the advances in the knowledge of its origin, its evolution, and its potential functional roles.

scholarly journals The bacterial chromatin protein HupA can remodel DNA and associates with the nucleoid in Clostridium difficile

2018 ◽  
Author(s):  
Ana M. Oliveira Paiva ◽  
Annemieke H. Friggen ◽  
Liang Qin ◽  
Roxanne Douwes ◽  
Remus T. Dame ◽  
...  
Keyword(s):  
Protein A ◽  
Chromatin Protein ◽  
Chromosomal Organization ◽  
Cellular Processes ◽  
Hu Proteins ◽  
Architectural Proteins ◽  
Chromatin Proteins

AbstractThe maintenance and organization of the chromosome plays an important role in the development and survival of bacteria. Bacterial chromatin proteins are architectural proteins that bind DNA, modulate its conformation and by doing so affect a variety of cellular processes. No bacterial chromatin proteins of C. difficile have been characterized to date.Here, we investigate aspects of the C. difficile HupA protein, a homologue of the histone-like HU proteins of Escherichia coli. HupA is a 10 kDa protein that is present as a homodimer in vitro and self-interacts in vivo. HupA co-localizes with the nucleoid of C. difficile. It binds to the DNA without a preference for the DNA G+C content. Upon DNA binding, HupA induces a conformational change in the substrate DNA in vitro and leads to compaction of the chromosome in vivo.The present study is the first to characterize a bacterial chromatin protein in C. difficile and opens the way to study the role of chromosomal organization in DNA metabolism and on other cellular processes in this organism.

scholarly journals Satellite DNA-containing gigantic introns in a unique gene expression program during Drosophila spermatogenesis

2018 ◽  
Author(s):  
Jaclyn M Fingerhut ◽  
Jessica V Moran ◽  
Yukiko Yamashita
Keyword(s):  
Gene Expression ◽  
Satellite Dna ◽  
Rna Binding ◽  
Rna Binding Proteins ◽  
Gene Expression Program ◽  
Dna Repeats ◽  
Regulate Gene Expression ◽  
Unique Gene ◽  
Expression Of Genes ◽  
Expression Program

Intron gigantism, where genes contain megabase-sized introns, is observed across species, yet little is known about its purpose or regulation. Here we identify a unique gene expression program utilized for the proper expression of genes with intron gigantism. We find that two Drosophila genes with intron gigantism, kl-3 and kl-5, are transcribed in a spatiotemporal manner over the course of spermatocyte differentiation, which spans ~90 hours. The introns of these genes contain megabases of simple satellite DNA repeats that comprise over 99% of the gene loci, and these satellite-DNA containing introns are transcribed. We identify two RNA-binding proteins that specifically localize to kl-3 and kl-5 transcripts and are needed for the successful transcription or processing of these genes. We propose that genes with intron gigantism require a unique gene expression program, which may serve as a platform to regulate gene expression during cellular differentiation.

scholarly journals Selection constrains high rates of satellite DNA mutation in Daphnia pulex

2017 ◽  
Author(s):  
Jullien M. Flynn ◽  
Ian Caldas ◽  
Melania E. Cristescu ◽  
Andrew G. Clark
Keyword(s):  
Satellite Dna ◽  
Related Species ◽  
Rapid Evolution ◽  
Daphnia Pulex ◽  
Selective Constraint ◽  
Mutation Rates ◽  
Stabilizing Selection ◽  
Closely Related Species ◽  
Dna Mutation ◽  
Evolutionary Forces

AbstractA long-standing evolutionary puzzle is that all eukaryotic genomes contain large amounts of tandemly-repeated satellite DNA whose composition varies greatly among even closely related species. To elucidate the evolutionary forces governing satellite dynamics, quantification of the rates and patterns of mutations in satellite DNA copy number and tests of its selective neutrality are necessary. Here we used whole-genome sequences of 28 mutation accumulation (MA) lines of Daphnia pulex in addition to six isolates from a non-MA population originating from the same progenitor to both estimate mutation rates of abundances of satellite sequences and evaluate the selective regime acting upon them. We found that mutation rates of individual satellite sequence “kmers” were both high and highly variable, ranging from additions/deletions of 0.29 – 105 copies per generation (reflecting changes of 0.12 - 0.80 percent per generation). Our results also provide evidence that new kmer sequences are often formed from existing ones. The non-MA population isolates showed a signal of either purifying or stabilizing selection, with 33 % lower variation in kmer abundance on average than the MA lines, although the level of selective constraint was not evenly distributed across all kmers. The changes between many pairs of kmers were correlated, and the pattern of correlations was significantly different between the MA lines and the non-MA population. Our study demonstrates that kmer sequences can experience extremely rapid evolution in abundance, which can lead to high levels of divergence in genome-wide satellite DNA composition between closely related species.

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