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.

scholarly journals The modular mechanism of chromocenter formation in Drosophila

2018 ◽  
Author(s):  
Madhav Jagannathan ◽  
Ryan Cummings ◽  
Yukiko M. Yamashita
Keyword(s):  
Dna Binding ◽  
Satellite Dna ◽  
Binding Proteins ◽  
Dna Binding Proteins ◽  
Dna Repeats ◽  
Satellite Dnas ◽  
Modular Network ◽  
Full Complement ◽  
Single Nucleus ◽  
Nuclear Structures

AbstractA central principle underlying the ubiquity and abundance of pericentromeric satellite DNA repeats in eukaryotes has remained poorly understood. In our previous study (Jagannathan et al., 2018), we proposed that the interchromosomal clustering of satellite DNAs into nuclear structures known as chromocenters ensures encapsulation of all chromosomes into a single nucleus. Chromocenter disruption led to micronuclei formation, resulting in cell death. Here we show that chromocenter formation is mediated by a ‘modular’ network, where interactions between two sequence-specific satellite DNA-binding proteins, D1 and Prod, bound to their cognate satellite DNAs, bring the full complement of chromosomes into the chromocenter. D1 prod double mutants die during embryogenesis, exhibiting enhanced phenotypes associated with chromocenter disruption, revealing the universal importance of satellite DNAs and chromocenters. Taken together, we propose that interactions between chromocenter modules, consisting of satellite DNA binding proteins and their cognate satellite DNA, package the Drosophila genome within a single nucleus.

scholarly journals The modular mechanism of chromocenter formation in Drosophila

eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Madhav Jagannathan ◽  
Ryan Cummings ◽  
Yukiko M Yamashita
Keyword(s):  
Dna Binding ◽  
Satellite Dna ◽  
Binding Proteins ◽  
Dna Binding Proteins ◽  
Drosophila Genome ◽  
Dna Repeats ◽  
Satellite Dnas ◽  
Full Complement ◽  
Single Nucleus ◽  
Nuclear Structures

A central principle underlying the ubiquity and abundance of pericentromeric satellite DNA repeats in eukaryotes has remained poorly understood. Previously we proposed that the interchromosomal clustering of satellite DNAs into nuclear structures known as chromocenters ensures encapsulation of all chromosomes into a single nucleus (Jagannathan et al., 2018). Chromocenter disruption led to micronuclei formation, resulting in cell death. Here we show that chromocenter formation is mediated by a ‘modular’ network, where associations between two sequence-specific satellite DNA-binding proteins, D1 and Prod, bound to their cognate satellite DNAs, bring the full complement of chromosomes into the chromocenter. D1 prod double mutants die during embryogenesis, exhibiting enhanced phenotypes associated with chromocenter disruption, revealing the universal importance of satellite DNAs and chromocenters. Taken together, we propose that associations between chromocenter modules, consisting of satellite DNA binding proteins and their cognate satellite DNA, package the Drosophila genome within a single nucleus.

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 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.

scholarly journals Rapid divergence of the male reproductive proteins in theDrosophila dunnigroup and implications for postmating incompatibilities between species

2021 ◽  
Vol 11 (4) ◽  
Author(s):  
Tom Hill ◽  
Hazel-Lynn Rosales-Stephens ◽  
Robert L Unckless
Keyword(s):  
Seminal Fluid ◽  
Rapid Evolution ◽  
Reproductive Proteins ◽  
Closely Related Species ◽  
Seminal Fluid Proteins ◽  
Hybrid Incompatibility ◽  
Caribbean Islands ◽  
Rates Of Evolution ◽  
Rapid Divergence ◽  
Postmating Prezygotic Isolation

AbstractProteins involved in post-copulatory interactions between males and females are among the fastest evolving genes in many species, usually attributed to their involvement in reproductive conflict. As a result, these proteins are thought to often be involved in the formation of postmating-prezygotic incompatibilities between species. The Drosophila dunni subgroup consists of a dozen recently diverged species found across the Caribbean islands with varying levels of hybrid incompatibility. We performed experimental crosses between species in the dunni group and see some evidence of hybrid incompatibilities. We also find evidence of reduced survival following hybrid mating, likely due to postmating-prezygotic incompatibilities. We assessed rates of evolution between these species genomes and find evidence of rapid evolution and divergence of some reproductive proteins, specifically the seminal fluid proteins. This work suggests the rapid evolution of seminal fluid proteins may be associated with postmating-prezygotic isolation, which acts as a barrier for gene flow between even the most closely related species.

scholarly journals A conserved function for pericentromeric satellite DNA

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Madhav Jagannathan ◽  
Ryan Cummings ◽  
Yukiko M Yamashita
Keyword(s):  
Dna Damage ◽  
Cell Death ◽  
Satellite Dna ◽  
Interphase Nucleus ◽  
Underlying Mechanism ◽  
Dna Binding Proteins ◽  
Eukaryotic Cells ◽  
Evolutionarily Conserved ◽  
Full Complement ◽  
Single Nucleus

A universal and unquestioned characteristic of eukaryotic cells is that the genome is divided into multiple chromosomes and encapsulated in a single nucleus. However, the underlying mechanism to ensure such a configuration is unknown. Here, we provide evidence that pericentromeric satellite DNA, which is often regarded as junk, is a critical constituent of the chromosome, allowing the packaging of all chromosomes into a single nucleus. We show that the multi-AT-hook satellite DNA-binding proteins, Drosophila melanogaster D1 and mouse HMGA1, play an evolutionarily conserved role in bundling pericentromeric satellite DNA from heterologous chromosomes into ‘chromocenters’, a cytological association of pericentromeric heterochromatin. Defective chromocenter formation leads to micronuclei formation due to budding from the interphase nucleus, DNA damage and cell death. We propose that chromocenter and satellite DNA serve a fundamental role in encapsulating the full complement of the genome within a single nucleus, the universal characteristic of eukaryotic cells.

scholarly journals Rapid Divergence Of The Copulation Proteins In The Drosophila Dunni Group Is Associated With Hybrid Post-Mating-Prezygotic Incompatibilities

2020 ◽  
Author(s):  
Tom Hill ◽  
Hazel-Lynn Rosales-Stephens ◽  
Robert L. Unckless
Keyword(s):  
Seminal Fluid ◽  
Rapid Evolution ◽  
Reproductive Proteins ◽  
Closely Related Species ◽  
Seminal Fluid Proteins ◽  
Hybrid Incompatibility ◽  
Prezygotic Isolation ◽  
Caribbean Islands ◽  
Rates Of Evolution ◽  
Rapid Divergence

Abstract Background: Proteins involved in post-copulatory interactions between males and females are among the fastest evolving genes in many species and this has been attributed to reproductive conflict. Likely as a result, these proteins are frequently involved in cases of post-mating-prezygotic isolation between species. The Drosophila dunni subgroup consists of a dozen recently diverged species found across the Caribbean islands with varying levels of hybrid incompatibility.Results: We performed experimental crosses between species in the dunni group and find evidence of hybrid inviability likely due to post-mating-prezygotic incompatibilities. We next assessed rates of evolution between these species genomes and find evidence of rapid evolution and divergence of some reproductive proteins, specifically the seminal fluid proteins.Conclusions: This work suggests the rapid evolution of seminal fluid proteins can lead to post-mating-prezygotic isolation, which acts as a barrier for gene flow between even the most closely related species.

scholarly journals A conserved function for pericentromeric satellite DNA

2018 ◽  
Author(s):  
Madhav Jagannathan ◽  
Ryan Cummings ◽  
Yukiko M. Yamashita
Keyword(s):  
Cell Death ◽  
Dna Binding ◽  
Satellite Dna ◽  
Interphase Nucleus ◽  
Underlying Mechanism ◽  
Dna Binding Proteins ◽  
Eukaryotic Cells ◽  
Evolutionarily Conserved ◽  
Full Complement ◽  
Single Nucleus

AbstractA universal and unquestioned characteristic of eukaryotic cells is that the genome is divided into multiple chromosomes and encapsulated in a single nucleus. However, the underlying mechanism to ensure such a configuration is unknown. Here we provide evidence that pericentromeric satellite DNA, which is often regarded as junk, is a critical constituent of the chromosome, allowing the packaging of all chromosomes into a single nucleus. We show that the multi AT-hook satellite DNA binding proteins, D. melanogaster D1 and mouse HMGA1, play an evolutionarily conserved role in bundling pericentromeric satellite DNA from heterologous chromosomes into ‘chromocenters’, a cytological association of pericentromeric heterochromatin. Defective chromocenter formation leads to micronuclei formation due to budding off of interphase nucleus and cell death. We propose that chromocenter and satellite DNA serves a fundamental role to achieve the universal characteristic of eukaryotic cells: full complement of the genome within a single nucleus.

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 How Can Satellite DNA Divergence Cause Reproductive Isolation? Let Us Count the Chromosomal Ways

2012 ◽  
Vol 2012 ◽  
pp. 1-11 ◽  
Author(s):  
Patrick M. Ferree ◽  
Satyaki Prasad
Keyword(s):  
Reproductive Isolation ◽  
Developmental Stages ◽  
Rapid Evolution ◽  
Model Organisms ◽  
Cellular Mechanisms ◽  
Closely Related Species ◽  
Heterochromatin Formation ◽  
Interspecies Hybrids ◽  
Postzygotic Reproductive Isolation ◽  
And Function

Satellites are one of the most enigmatic parts of the eukaryotic genome. These highly repetitive, noncoding sequences make up as much as half or more of the genomic content and are known to play essential roles in chromosome segregation during meiosis and mitosis, yet they evolve rapidly between closely related species. Research over the last several decades has revealed that satellite divergence can serve as a formidable reproductive barrier between sibling species. Here we highlight several key studies on Drosophila and other model organisms demonstrating deleterious effects of satellites and their rapid evolution on the structure and function of chromosomes in interspecies hybrids. These studies demonstrate that satellites can impact chromosomes at a number of different developmental stages and through distinct cellular mechanisms, including heterochromatin formation. These findings have important implications for how loci that cause postzygotic reproductive isolation are viewed.

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