Comparative analysis of morabine grasshopper genomes reveals highly abundant transposable elements and rapidly proliferating satellite DNA repeats

Abstract Background Repetitive DNA sequences, including transposable elements (TEs) and tandemly repeated satellite DNA (satDNAs), collectively called the “repeatome”, are found in high proportion in organisms across the Tree of Life. Grasshoppers have large genomes, averaging 9 Gb, that contain a high proportion 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 repetitive DNA sequences in four chromosomal races of the morabine grasshopper Vandiemenella viatica species complex and determine their contribution to genome evolution. Results We 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. 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 sizes are likely due to similar rates of TE accumulation. 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 diversity 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. Conclusion This in-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. Despite an overall high similarity of the TE and satDNA diversity between races, the patterns of TE expression and satDNA proliferation suggest rapid evolution of grasshopper genomes on recent timescales.

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

10.1101/2020.08.22.247130 ◽

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.

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Structures and stability of simple DNA repeats from bacteria

Biochemical Journal ◽

10.1042/bcj20190703 ◽

2020 ◽

Vol 477 (2) ◽

pp. 325-339 ◽

Cited By ~ 4

Author(s):

Vaclav Brazda ◽

Miroslav Fojta ◽

Richard P. Bowater

Keyword(s):

Repetitive Dna ◽

Dna Sequences ◽

Genetic Instability ◽

Repetitive Sequences ◽

Biological Significance ◽

Human Diseases ◽

Repetitive Dna Sequences ◽

Dna Repeats ◽

Diverse Range ◽

Dna Structures

DNA is a fundamentally important molecule for all cellular organisms due to its biological role as the store of hereditary, genetic information. On the one hand, genomic DNA is very stable, both in chemical and biological contexts, and this assists its genetic functions. On the other hand, it is also a dynamic molecule, and constant changes in its structure and sequence drive many biological processes, including adaptation and evolution of organisms. DNA genomes contain significant amounts of repetitive sequences, which have divergent functions in the complex processes that involve DNA, including replication, recombination, repair, and transcription. Through their involvement in these processes, repetitive DNA sequences influence the genetic instability and evolution of DNA molecules and they are located non-randomly in all genomes. Mechanisms that influence such genetic instability have been studied in many organisms, including within human genomes where they are linked to various human diseases. Here, we review our understanding of short, simple DNA repeats across a diverse range of bacteria, comparing the prevalence of repetitive DNA sequences in different genomes. We describe the range of DNA structures that have been observed in such repeats, focusing on their propensity to form local, non-B-DNA structures. Finally, we discuss the biological significance of such unusual DNA structures and relate this to studies where the impacts of DNA metabolism on genetic stability are linked to human diseases. Overall, we show that simple DNA repeats in bacteria serve as excellent and tractable experimental models for biochemical studies of their cellular functions and influences.

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Long-Term Rasamsonia argillacea Complex Species Colonization Revealed by PCR Amplification of Repetitive DNA Sequences in Cystic Fibrosis Patients

Journal of Clinical Microbiology ◽

10.1128/jcm.01462-16 ◽

2016 ◽

Vol 54 (11) ◽

pp. 2804-2812 ◽

Cited By ~ 10

Author(s):

Abdelmounaim Mouhajir ◽

Olivier Matray ◽

Sandrine Giraud ◽

Laurent Mély ◽

Christophe Marguet ◽

...

Keyword(s):

Cystic Fibrosis ◽

Repetitive Dna ◽

Dna Sequences ◽

Species Complex ◽

Pcr Amplification ◽

Patient Specific ◽

Molecular Evidence ◽

Repetitive Dna Sequences ◽

Complex Species ◽

Content Type

The aim of this work was to document molecular epidemiology of Rasamsonia argillacea species complex isolates from cystic fibrosis (CF) patients. In this work, 116 isolates belonging to this species complex and collected from 26 CF patients and one patient with chronic granulomatous disease were characterized using PCR amplification assays of repetitive DNA sequences and electrophoretic separation of amplicons (rep-PCR). Data revealed a clustering consistent with molecular species identification. A single species was recovered from most patients. Rasamsonia aegroticola was the most common species, followed by R. argillacea sensu stricto and R. piperina , while R. eburnea was not identified. Of 29 genotypes, 7 were shared by distinct patients while 22 were patient specific. In each clinical sample, most isolates exhibited an identical genotype. Genotyping of isolates recovered from sequential samples from the same patient confirmed the capability of R. aegroticola and R. argillacea isolates to chronically colonize the airways. A unique genotype was recovered from two siblings during a 6-month period. In the other cases, a largely dominant genotype was detected. Present results which support the use of rep-PCR for both identification and genotyping for the R. argillacea species complex provide the first molecular evidence of chronic airway colonization by these fungi in CF patients.

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Highly Species-Specific Centromeric Repetitive DNA Sequences in Lizards: Molecular Cytogenetic Characterization of a Novel Family of Satellite DNA Sequences Isolated from the Water Monitor Lizard (Varanus salvator macromaculatus, Platynota)

Journal of Heredity ◽

10.1093/jhered/est061 ◽

2013 ◽

Vol 104 (6) ◽

pp. 798-806 ◽

Cited By ~ 15

Author(s):

N. Chaiprasertsri ◽

Y. Uno ◽

S. Peyachoknagul ◽

O. Prakhongcheep ◽

S. Baicharoen ◽

...

Keyword(s):

Repetitive Dna ◽

Dna Sequences ◽

Satellite Dna ◽

Repetitive Dna Sequences ◽

Molecular Cytogenetic ◽

Monitor Lizard ◽

Varanus Salvator ◽

Cytogenetic Characterization ◽

Species Specific

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Genome-wide analysis of DNA repeats in Burkholderia cenocepacia J2315 identifies a novel adhesin-like gene unique to epidemic-associated strains of the ET-12 lineage

Microbiology ◽

10.1099/mic.0.032623-0 ◽

2010 ◽

Vol 156 (4) ◽

pp. 1084-1096 ◽

Cited By ~ 23

Author(s):

Dalila Mil-Homens ◽

Eduardo P. C. Rocha ◽

Arsenio M. Fialho

Keyword(s):

Repetitive Dna ◽

Dna Sequences ◽

Matrix Protein ◽

Cellular Adhesion ◽

The Other ◽

Burkholderia Cenocepacia ◽

Extracellular Matrix Protein ◽

Repetitive Dna Sequences ◽

Type I ◽

Dna Repeats

Members of the Burkholderia cepacia complex (Bcc) are respiratory pathogens in patients with cystic fibrosis (CF). Close repetitive DNA sequences often associate with surface antigens to promote genetic variability in pathogenic bacteria. The genome of Burkholderia cenocepacia J2315, a CF isolate belonging to the epidemic lineage Edinburgh–Toronto (ET-12), was analysed for the presence of close repetitive DNA sequences. Among the 422 DNA close repeats, 45 genes potentially involved in virulence were identified and grouped into 12 classes; of these, 13 genes were included in the antigens class. Two trimeric autotransporter adhesins (TAA) among the 13 putative antigens are absent from the other Burkholderia genomes and are clustered downstream of the cci island that is a marker for transmissible B. cenocepacia strains. This cluster contains four adhesins, one outer-membrane protein, one sensor histidine kinase and two transcriptional regulators. By using PCR, we analysed three genes among 47 Bcc isolates to determine whether the cluster was conserved. These three genes were present in the isolates of the ET-12 lineage but absent in all the other members. Furthermore, the BCAM0224 gene was exclusively detected in this epidemic lineage and may serve as a valuable new addition to the field of Bcc diagnostics. The BCAM0224 gene encodes a putative TAA that demonstrates adhesive properties to the extracellular matrix protein collagen type I. Quantitative real-time PCR analysis indicated that BCAM0224 gene expression occurred preferentially for cells grown under high osmolarity, oxygen-limited conditions and oxidative stress. Inactivation of BCAM0224 in B. cenocepacia attenuates the ability of the mutant to promote cell adherence in vitro and impairs the overall bacterial virulence against Galleria mellonella as a model of infection. Together, our data show that BCAM0224 from B. cenocepacia J2315 represents a new collagen-binding TAA with no bacterial orthologues which has an important role in cellular adhesion and virulence.

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Chromosomal Locations of a Non-LTR Retrotransposon, Menolird18, in Cucumis melo and Cucumis sativus, and Its Implication on Genome Evolution of Cucumis Species

Cytogenetic and Genome Research ◽

10.1159/000511119 ◽

2020 ◽

Vol 160 (9) ◽

pp. 554-564

Author(s):

Agus B. Setiawan ◽

Chee H. Teo ◽

Shinji Kikuchi ◽

Hidenori Sassa ◽

Kenji Kato ◽

...

Keyword(s):

Genome Evolution ◽

Repetitive Dna ◽

Dna Sequences ◽

18S Rdna ◽

Cucumis Melo ◽

Repetitive Dna Sequences ◽

Ltr Retrotransposon ◽

Ltr Retrotransposons ◽

Mitotic Chromosomes ◽

Rna Genes

Mobile elements are major regulators of genome evolution through their effects on genome size and chromosome structure in higher organisms. Non-long terminal repeat (non-LTR) retrotransposons, one of the subclasses of transposons, are specifically inserted into repetitive DNA sequences. While studies on the insertion of non-LTR retrotransposons into ribosomal RNA genes and other repetitive DNA sequences have been reported in the animal kingdom, studies in the plant kingdom are limited. Here, using FISH, we confirmed that Menolird18, a member of LINE (long interspersed nuclear element) in non-LTR retrotransposons and found in Cucumis melo, was inserted into ITS and ETS (internal and external transcribed spacers) regions of 18S rDNA in melon and cucumber. Beside the 18S rDNA regions, Menolird18 was also detected in all centromeric regions of melon, while it was located at pericentromeric and sub-telomeric regions in cucumber. The fact that FISH signals of Menolird18 were found in centromeric and rDNA regions of mitotic chromosomes suggests that Menolird18 is a rDNA and centromere-specific non-LTR retrotransposon in melon. Our findings are the first report on a non-LTR retrotransposon that is highly conserved in 2 different plant species, melon and cucumber. The clear distinction of chromosomal localization of Menolird18 in melon and cucumber implies that it might have been involved in the evolutionary processes of the melon (C. melo) and cucumber (C. sativus) genomes.

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Extrachromosomal DNA forms of copia-like transposable elements, F elements and middle repetitive DNA sequences in Drosophila melanogaster

Journal of Molecular Biology ◽

10.1016/0022-2836(85)90025-7 ◽

1985 ◽

Vol 182 (1) ◽

pp. 31-43 ◽

Cited By ~ 18

Author(s):

Kevin G. Mossie ◽

Michael W. Young ◽

Harold E. Varmus

Keyword(s):

Drosophila Melanogaster ◽

Transposable Elements ◽

Repetitive Dna ◽

Dna Sequences ◽

Repetitive Dna Sequences ◽

Extrachromosomal Dna

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Evolution of genome structure in the Drosophila simulans species complex

10.1101/2020.02.27.968743 ◽

2020 ◽

Cited By ~ 6

Author(s):

Mahul Chakraborty ◽

Ching-Ho Chang ◽

Danielle E. Khost ◽

Jeffrey Vedanayagam ◽

Jeffrey R. Adrion ◽

...

Keyword(s):

Transposable Elements ◽

Dna Sequences ◽

Satellite Dna ◽

Species Complex ◽

Repetitive Sequences ◽

Drosophila Simulans ◽

Gene Duplications ◽

Phenotypic Evolution ◽

Complex Species ◽

Structural Divergence

ABSTRACTThe rapid evolution of repetitive DNA sequences, including satellite DNA, tandem duplications, and transposable elements, underlies phenotypic evolution and contributes to hybrid incompatibilities between species. However, repetitive genomic regions are fragmented and misassembled in most contemporary genome assemblies. We generated highly contiguous de novo reference genomes for the Drosophila simulans species complex (D. simulans, D. mauritiana, and D. sechellia), which speciated ∼250,000 years ago. Our assemblies are comparable in contiguity and accuracy to the current D. melanogaster genome, allowing us to directly compare repetitive sequences between these four species. We find that at least 15% of the D. simulans complex species genomes fail to align uniquely to D. melanogaster due to structural divergence—twice the number of single-nucleotide substitutions. We also find rapid turnover of satellite DNA and extensive structural divergence in heterochromatic regions, while the euchromatic gene content is mostly conserved. Despite the overall preservation of gene synteny, euchromatin in each species has been shaped by clade and species-specific inversions, transposable elements, expansions and contractions of satellite and tRNA tandem arrays, and gene duplications. We also find rapid divergence among Y-linked genes, including copy number variation and recent gene duplications from autosomes. Our assemblies provide a valuable resource for studying genome evolution and its consequences for phenotypic evolution in these genetic model species.

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