The Low-Copy-Number Satellite DNAs of the Model Beetle Tribolium castaneum

The red flour beetle Tribolium castaneum is an important pest of stored agricultural products and the first beetle whose genome was sequenced. So far, one high-copy-number and ten moderate-copy-number satellite DNAs (satDNAs) have been described in the assembled part of its genome. In this work, we aimed to catalog the entire collection of T. castaneum satDNAs. We resequenced the genome using Illumina technology and predicted potential satDNAs via graph-based sequence clustering. In this way, we discovered 46 novel satDNAs that occupied a total of 2.1% of the genome and were, therefore, considered low-copy-number satellites. Their repeat units, preferentially 140–180 bp and 300–340 bp long, showed a high A + T composition ranging from 59.2 to 80.1%. In the current assembly, we annotated the majority of the low-copy-number satDNAs on one or a few chromosomes, discovering mainly transposable elements in their vicinity. The current assembly also revealed that many of the in silico predicted satDNAs were organized into short arrays not much longer than five consecutive repeats, and some of them also had numerous repeat units scattered throughout the genome. Although 20% of the unassembled genome sequence masked the genuine state, the predominance of scattered repeats for some low-copy satDNAs raises the question of whether these are essentially interspersed repeats that occur in tandem only sporadically, with the potential to be satDNA “seeds”.

[1]  M. Plohl,et al.  Satellite DNAs—From Localized to Highly Dispersed Genome Components , 2023, Genes.

[2]  S. Louzada,et al.  Human Satellite 1A analysis provides evidence of pericentromeric transcription , 2023, BMC Biology.

[3]  F. Panzera,et al.  Making the Genome Huge: The Case of Triatoma delpontei, a Triatominae Species with More than 50% of Its Genome Full of Satellite DNA , 2023, Genes.

[4]  Michelle Louise Zattera,et al.  Transposable Elements as a Source of Novel Repetitive DNA in the Eukaryote Genome , 2022, Cells.

[5]  P. Lorite,et al.  Satellitome of the Red Palm Weevil, Rhynchophorus ferrugineus (Coleoptera: Curculionidae), the Most Diverse Among Insects , 2022, Frontiers in Ecology and Evolution.

[6]  S. Henikoff,et al.  The genetics and epigenetics of satellite centromeres , 2022, Genome research.

[7]  M. Garrido-Ramos,et al.  Satellitome comparison of two oedipodine grasshoppers highlights the contingent nature of satellite DNA evolution , 2022, BMC biology.

[8]  J. Campbell,et al.  Tribolium castaneum: A Model Insect for Fundamental and Applied Research. , 2021, Annual review of entomology.

[9]  Muhammad Majid,et al.  Comparative Analysis of Transposable Elements in Genus Calliptamus Grasshoppers Revealed That Satellite DNA Contributes to Genome Size Variation , 2021, Insects.

[10]  Aaron M. Streets,et al.  Complete genomic and epigenetic maps of human centromeres , 2021, bioRxiv.

[11]  M. Plohl,et al.  Satellitome Analysis of the Pacific Oyster Crassostrea gigas Reveals New Pattern of Satellite DNA Organization, Highly Scattered across the Genome , 2021, International journal of molecular sciences.

[12]  F. Panzera,et al.  Satellitome Analysis of Rhodnius prolixus, One of the Main Chagas Disease Vector Species , 2021, International journal of molecular sciences.

[13]  Aaron M. Streets,et al.  The complete sequence of a human genome , 2021, bioRxiv.

[14]  Sudhir Kumar,et al.  MEGA11: Molecular Evolutionary Genetics Analysis Version 11 , 2021, Molecular biology and evolution.

[15]  G. Dias,et al.  Structure, Organization, and Evolution of Satellite DNAs: Insights from the Drosophila repleta and D. virilis Species Groups. , 2021, Progress in molecular and subcellular biology.

[16]  Matthias Benoit,et al.  A Predictive Approach to Infer the Activity and Natural Variation of Retrotransposon Families in Plants. , 2021, Methods in molecular biology.

[17]  Carola Greve,et al.  The Pontastacus leptodactylus (Astacidae) Repeatome Provides Insight Into Genome Evolution and Reveals Remarkable Diversity of Satellite DNA , 2021, Frontiers in Genetics.

[18]  T. Shenk,et al.  HSATII RNA is induced via a noncanonical ATM-regulated DNA damage response pathway and promotes tumor cell proliferation and movement , 2020, Proceedings of the National Academy of Sciences.

[19]  Pavel Neumann,et al.  Global analysis of repetitive DNA from unassembled sequence reads using RepeatExplorer2 , 2020, Nature Protocols.

[20]  M. Plohl,et al.  CenH3 distribution reveals extended centromeres in the model beetle Tribolium castaneum , 2020, PLoS genetics.

[21]  M. Plohl,et al.  Satellite DNA-like repeats are dispersed throughout the genome of the Pacific oyster Crassostrea gigas carried by Helentron non-autonomous mobile elements , 2020, Scientific Reports.

[22]  P. Lorite,et al.  Satellitome Analysis in the Ladybird Beetle Hippodamia variegata (Coleoptera, Coccinellidae) , 2020, Genes.

[23]  S. Henikoff,et al.  What makes a centromere? , 2020, Experimental cell research.

[24]  S. Griffiths-Jones,et al.  Enhanced genome assembly and a new official gene set for Tribolium castaneum , 2019, BMC Genomics.

[25]  J. Macas,et al.  Characterization of repeat arrays in ultra‐long nanopore reads reveals frequent origin of satellite DNA from retrotransposon‐derived tandem repeats , 2019, The Plant journal : for cell and molecular biology.

[26]  F. Foresti,et al.  Satellitome landscape analysis of Megaleporinus macrocephalus (Teleostei, Anostomidae) reveals intense accumulation of satellite sequences on the heteromorphic sex chromosome , 2019, Scientific Reports.

[27]  Joseph G. Mccarter,et al.  Birth, evolution, and transmission of satellite-free mammalian centromeric domains , 2018, Genome research.

[28]  Reidar Andreson,et al.  Primer3_masker: integrating masking of template sequence with primer design software , 2018, Bioinform..

[29]  J. Macas,et al.  Satellite DNA in Vicia faba is characterized by remarkable diversity in its sequence composition, association with centromeres, and replication timing , 2018, Scientific Reports.

[30]  Francisco J. Ruiz-Ruano,et al.  High-throughput analysis of satellite DNA in the grasshopper Pyrgomorpha conica reveals abundance of homologous and heterologous higher-order repeats , 2018, Chromosoma.

[31]  M. Garrido-Ramos Satellite DNA: An Evolving Topic , 2017, Genes.

[32]  Á. Cuadrado,et al.  Comparative repeatome analysis on Triatoma infestans Andean and Non-Andean lineages, main vector of Chagas disease , 2017, PloS one.

[33]  J. Macas,et al.  TAREAN: a computational tool for identification and characterization of satellite DNA from unassembled short reads , 2017, Nucleic acids research.

[34]  Francisco J. Ruiz-Ruano,et al.  High-throughput analysis of the satellitome illuminates satellite DNA evolution , 2016, Scientific Reports.

[35]  M. Plohl,et al.  Genome-wide analysis of tandem repeats in Tribolium castaneum genome reveals abundant and highly dynamic tandem repeat families with satellite DNA features in euchromatic chromosomal arms , 2015, DNA research : an international journal for rapid publication of reports on genes and genomes.

[36]  I. Feliciello,et al.  Correction: Satellite DNA Modulates Gene Expression in the Beetle Tribolium castaneum after Heat Stress , 2015, PLoS genetics.

[37]  M. Plohl,et al.  Structural and functional liaisons between transposable elements and satellite DNAs , 2015, Chromosome Research.

[38]  O. Kohany,et al.  Repbase Update, a database of repetitive elements in eukaryotic genomes , 2015, Mobile DNA.

[39]  I. Feliciello,et al.  Satellite DNA as a Driver of Population Divergence in the Red Flour Beetle Tribolium castaneum , 2014, Genome biology and evolution.

[40]  Nicolas Pollet,et al.  Insights on genome size evolution from a miniature inverted repeat transposon driving a satellite DNA. , 2014, Molecular phylogenetics and evolution.

[41]  A. Ruíz,et al.  Tetris Is a Foldback Transposon that Provided the Building Blocks for an Emerging Satellite DNA of Drosophila virilis , 2014, Genome biology and evolution.

[42]  T. Schwarzacher,et al.  Nucleosomes and centromeric DNA packaging , 2013, Proceedings of the National Academy of Sciences.

[43]  Petr Novák,et al.  RepeatExplorer: a Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads , 2013, Bioinform..

[44]  Jeffrey Ross-Ibarra,et al.  Comparative analysis of tandem repeats from hundreds of species reveals unique insights into centromere evolution , 2012, Genome Biology.

[45]  I. Feliciello,et al.  Satellite DNA-Like Elements Associated With Genes Within Euchromatin of the Beetle Tribolium castaneum , 2012, G3: Genes | Genomes | Genetics.

[46]  Kevin W Eliceiri,et al.  NIH Image to ImageJ: 25 years of image analysis , 2012, Nature Methods.

[47]  G. Kuhn,et al.  The 1.688 repetitive DNA of Drosophila: concerted evolution at different genomic scales and association with genes. , 2012, Molecular biology and evolution.

[48]  M. Plohl,et al.  Parallelism in evolution of highly repetitive DNAs in sibling species. , 2010, Molecular biology and evolution.

[49]  Peer Bork,et al.  The Genome of the Model Beetle and Pest Tribolium Castaneum Vertebrate-specific Orthologues Insect-specific Orthologues Homology Undetectable Similarity , 2022 .

[50]  Susan J. Brown,et al.  Analysis of repetitive DNA distribution patterns in the Tribolium castaneum genome , 2008, Genome Biology.

[51]  Jerzy Jurka,et al.  Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor , 2006, BMC Bioinformatics.

[52]  M. Plohl,et al.  Conserved patterns in the evolution of Tribolium satellite DNAs. , 2004, Gene.

[53]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[54]  D. Franjević,et al.  Long Inversely Oriented Subunits Form a Complex Monomer of Triboliumbrevicornis Satellite DNA , 2004, Journal of Molecular Evolution.

[55]  M. Plohl,et al.  Evolution of satellite DNAs from the genus Palorus--experimental evidence for the "library" hypothesis. , 1998, Molecular biology and evolution.

[56]  M. Plohl,et al.  Satellite DNA of the red flour beetle Tribolium castaneum--comparative study of satellites from the genus Tribolium. , 1996, Molecular biology and evolution.

[57]  M. Plohl,et al.  Evolution of Tribolium madens (Insecta, Coleoptera) Satellite DNA Through DNA Inversion and Insertion , 1996, Journal of Molecular Evolution.

[58]  J. Stuart,et al.  Cytogenetics of chromosome rearrangements in Tribolium castaneum. , 1995, Genome.

[59]  M. Plohl,et al.  Satellite DNA and heterochromatin of the flour beetle Tribolium confusum. , 1993, Genome.

[60]  J. M. Rubio,et al.  Presence of highly repetitive DNA sequences in Tribolium flour-beetles , 1993, Heredity.

[61]  Susan J. Brown,et al.  Molecular genetic manipulation of the red flour beetle: Genome organization and cloning of a ribosomal protein gene , 1990 .

[62]  G. Dover Molecular drive in multigene families: How biological novelties arise, spread and are assimilated , 1986 .

[63]  W. Salser,et al.  Nucleotide sequences of HS-α satellite DNA from kangaroo rat dipodomys ordii and characterization of similar sequences in other rodents , 1977, Cell.

[64]  S. Kit,et al.  Equilibrium sedimentation in density gradients of DNA preparations from animal tissues. , 1961, Journal of molecular biology.