DOCSLIB.ORG

Divergence of Drosophila Melanogaster Repeatomes in Response to a Sharp Microclimate Contrast in Evolution Canyon, Israel

Total Page：16

File Type：pdf, Size：1020Kb

Download full-text PDF Read full-text
Divergence of Drosophila Melanogaster Repeatomes in Response to a Sharp Microclimate Contrast in Evolution Canyon, Israel Divergence of Drosophila melanogaster repeatomes in response to a sharp microclimate contrast in Evolution Canyon, Israel Young Bun Kima, Jung Hun Ohb, Lauren J. McIvera, Eugenia Rashkovetskyc, Katarzyna Michalaka, Harold R. Garnera,d, Lin Kanga, Eviatar Nevoc,1,2, Abraham B. Korolc,1, and Pawel Michalaka,d,e,1,2 aVirginia Bioinformatics Institute and Departments of dBiological Sciences and eFish and Wildlife Conservation, Virginia Tech, Blacksburg, VA 24061; bDepartment of Medical Physics, Memorial Sloan–Kettering Cancer Center, New York, NY 10065; and cInstitute of Evolution, Haifa University, Haifa 3498838, Israel Contributed by Eviatar Nevo, June 4, 2014 (sent for review May 8, 2014; reviewed by Alan R. Templeton and Harmit S. Malik) Repeat sequences, especially mobile elements, make up large was polymorphic for a 1.2-kb P-element insertion, with the insert portions of most eukaryotic genomes and provide enormous, albeit being 28 times more frequent in NFS- than SFS-inhabiting flies. commonly underappreciated, evolutionary potential. We analyzed The P-element disruption was associated with decreased Hsp70 repeatomes of Drosophila melanogaster that have been diverging expression and heat-shock survival, but increased reproductive in response to a microclimate contrast in Evolution Canyon (Mount success in temperate conditions (13). Although elevated levels of Carmel, Israel), a natural evolutionary laboratory with two abutting Hsp70 are beneficial during thermotolerance challenges, they tend slopes at an average distance of only 200 m, which pose a constant to be deleterious for growth and development (14, 15). ecological challenge to their local biotas. Flies inhabiting the colder In parallel with a common pattern of slope-specific adapta- and more humid north-facing slope carried about 6% more trans- tions observed across many other taxa inhabiting this remarkable posable elements than those from the hot and dry south-facing ecological microgradient (16, 17), SFS-derived D. melanogaster slope, in parallel to a suite of other genetic and phenotypic differ- outperform their conspecific neighbors from NFS not only in ences between the two populations. Nearly 50% of all mobile ele- basal and inducible thermotolerance after diverse heat shocks ment insertions were slope unique, with many of them disrupting (18–20), but also in resistance to desiccation and starvation (18, coding sequences of genes critical for cognition, olfaction, and ther- 21). In addition to stress resistance, the two populations differ in motolerance, consistent with the observed patterns of thermotoler- oviposition site preferences (18), male courtship song parameters ance differences and assortative mating. (22), sexual and reproductive behavior (23) leading to partial assortative mating within slopes (24), and phenotypic plasticity for adaptive evolution | genome sequencing | microsatellite | wing morphology (25)—all this despite the physical proximity and incipient speciation migration between slopes (26). A recent genome analysis of the two populations (27) reveals ne of the greatest surprises of comparative genomics has a number of chromosomal regions of interslope divergence and Obeen the discovery that eukaryotic genomes are loaded with low sequence polymorphism, suggestive of selective sweeps among ubiquitous repeat sequences, such as transposable elements genes enriched for functions related to stimulus responses and (TEs) and tandem array repeats (satellites). Once relegated to developmental and reproductive processes, remarkably consistent junk DNA, today many repeat elements emerge as potent func- with our previous findings on the phenotypic patterns of stress tional genetic units, providing inspiration for new research ini- responses, life history, and mating functions. Sequence divergence tiatives (1). Although traditionally viewed as selfish DNA, TEs are increasingly being recognized as agents of adaptive change and a rich source of evolutionary novelties, including hybrid Significance dysgenesis (2), insecticide resistance (3), mammalian placenta (4), and vertebrate adaptive immune system (4), as well as flower Repeatome, or the ensemble of all repeat sequences, with its development and plant fitness (5). Domesticated TEs can be enormous variability and internal epigenetic dynamics, emerges repurposed to function as transcription factors, whereas others play as a critical source of potentially adaptive changes and evolu- various roles in heterochromatin formation, genome stability, cen- tionary novelties. This conclusion is exemplified here by the tromere binding, chromosome segregation, meiotic recombination, cosmopolitan Drosophila melanogaster from a sharp ecological TE silencing, programmed genome rearrangement, V(D)J recom- contrast in North Israel. Flies derived from the opposing sides bination, and translational regulation (4, 6). Even low-complexity of this long-studied microsite exhibit a significant difference in sequence repeats, such as microsatellites, may act as novel regula- the contents and distribution of mobile elements, as well as tory elements (7), enhance alternative splicing (8), and provide new microsatellite allele frequencies, corresponding well with ear- substrate for protein coding variation (9). lier reported phenotypic patterns of stress resistance and TEs have been implicated in adaptations to environmental assortative mating in the system. changes either through somewhat elusive direct remobilization Author contributions: E.N., A.B.K., and P.M. designed research; Y.B.K., E.R., and K.M. after stress (10) or more indirectly as a source of new and pre- performed research; Y.B.K., J.H.O., L.J.M., H.R.G., L.K., A.B.K., and P.M. analyzed data; existing genetic variation (11). A striking example of adaptive TE and Y.B.K., A.B.K., and P.M. wrote the paper. insertion polymorphism has been found in Drosophila mela- Reviewers: A.R.T., Washington University in St. Louis; and H.S.M., Fred Hutchinson Cancer nogaster from Evolution Canyon (lower Nahal Oren, Israel) (12, Research Center. 13), in which slopes 100–400 m apart differ dramatically in The authors declare no conflict of interest. aridity, solar radiation, and associated vegetation due to the 1E.N., A.B.K., and P.M. contributed equally to this work. higher insolation on the south-facing slope (SFS) relative to the 2To whom correspondence may be addressed. Email: [email protected] or pawel@ north-facing slope (NFS).The promoter region of heat-shock- vbi.vt.edu. protein-70Ba (hsp70Ba), one of the five Hsp70 paralogs that This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. encode a major inducible heat-shock protein in D. melanogaster, 1073/pnas.1410372111/-/DCSupplemental. 10630–10635 | PNAS | July 22, 2014 | vol. 111 | no. 29 www.pnas.org/cgi/doi/10.1073/pnas.1410372111 Downloaded by guest on September 29, 2021 Table 1. Chromosomal distribution of transposable elements in female germ-line mobilization in the progeny of certain D. mela- Evolution Canyon D. melanogaster nogaster intraspecific crosses, responsible for a maternal effect Chr. 5UTR 3UTR Intron CDS Promoter Intergenic Total embryonic lethality known as the I-R type of hybrid dysgenesis (32). Quasimodo and roo LTRs were the next most slope-di- SFS vergent TEs, followed by LINE-like jockey and Doc. The most X 26 51 778 78 20 1,054 2,007 slope-differential TIR was P-element, represented by 45 unique 2L 36 48 1,162 94 25 1,485 2,850 insertion sites. Interestingly, P-element insertions in the Hsp70Ba 2R 49 72 1,308 112 28 1,418 2,987 promoter reported earlier (12, 13) were absent in the current 3L 34 51 1,301 108 30 1,449 2,973 samples, a result of either demographic dynamics or selection 3R 44 80 1,262 120 30 1,261 2,797 against the insertion over the course of 13 y separating the fly 4 4 13 361 22 1 175 576 collections in the field. However, there were 76 other unique TE Total 193 315 6,172 534 134 6,842 14,190 insertions in SFS and 107 in NFS within the putative promoter NFS X 27 48 852 66 24 1,077 2,094 regions, including a P-element in a gene from the small heat shock 2L 32 46 1,276 93 33 1,642 3,122 protein (HSP20) family, Hsp67Ba, in SFS flies. Although expres- 2R 50 69 1,338 105 35 1,495 3,092 sion of Hsp67Ba was not directly investigated in D. melanogaster 3L 44 54 1,415 96 29 1,601 3,239 from Evolution Canyon, we have previously shown that small 3R 50 75 1,370 107 41 1,257 2,900 Hsps, such as Hsp40 and Hsp23, can contribute to thermotol- 4 0 12 369 21 2 174 578 erance in the system (33). There were at least 20 significant gene Total 203 304 6,620 488 164 7,246 15,025 ontology (GO) term enrichments representing genes with slope- unique TE insertions in their putative promoters, with functional Chr., chromosome; NFS, north-facing slope; SFS, south-facing slope. activities related to hydrolases and alternative splicing being most conspicuous (Tables S2 and S3). in genes underlying adaptive changes, coupled with assortative An additional 426 genes were disrupted by 511 slope-specific mating within populations, can be interpreted as signatures of TE insertions within coding sequences, presumably leading to ’ incipient speciation (21). The picture of adaptive divergence in the the genes functional inactivation. Interestingly, there were 20 natural system remains largely incomplete without looking into cognition-related and 17 sensory perception-related genes af- noncoding parts of the genomes, primarily those occupied by re- fected by the inserts, including 8 olfactory receptor and 8 gus- peat elements. To fill the void, we have now used high-coverage tatory receptor genes, all critical for detecting food and avoiding (40×) genome sequencing and analyzed variation of TEs and toxicants, as well as for courtship and mating. Cognition, sensory microsatellites in the two D. melanogaster populations. perception of chemical stimuli, and olfaction were among the most significantly overrepresented GO terms (Benjamini–Hochberg- Results and Discussion adjusted P < 0.01) among genes with TE-disrupted coding In D.
Load more

Recommended publications
  • Understanding Brassicaceae Evolution Through Ancestral
    Understanding Brassicaceae evolution through ancestral genome reconstruction Florent Murat, Alexandra Louis, Florian Maumus, Alix Armero Villanueva, Richard Cooke, Hadi Quesneville, Hugues Roest Crollius, Jerome Salse To cite this version: Florent Murat, Alexandra Louis, Florian Maumus, Alix Armero Villanueva, Richard Cooke, et al.. Understanding Brassicaceae evolution through ancestral genome reconstruction. Genome Biology, BioMed Central, 2015, 16 (262), 10.1186/s13059-015-0814-y. hal-01281832 HAL Id: hal-01281832 https://hal.archives-ouvertes.fr/hal-01281832 Submitted on 2 Mar 2016 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Murat et al. Genome Biology (2015) 16:262 DOI 10.1186/s13059-015-0814-y RESEARCH Open Access Understanding Brassicaceae evolution through ancestral genome reconstruction Florent Murat1†, Alexandra Louis2,3,4†, Florian Maumus5†, Alix Armero1, Richard Cooke6, Hadi Quesneville5, Hugues Roest Crollius2,3,4 and Jerome Salse1* Abstract Background: Brassicaceae is a family of green plants of high scientific and economic interest, including thale cress (Arabidopsis thaliana), cruciferous vegetables (cabbages) and rapeseed. Results: We reconstruct an evolutionary framework of Brassicaceae composed of high-resolution ancestral karyotypes using the genomes of modern A. thaliana, Arabidopsis lyrata, Capsella rubella, Brassica rapa and Thellungiella parvula.
    [Show full text]
  • The Future of Transposable Element Annotation and Their Classification in the Light of Functional Genomics
    The future of transposable element annotation and their classification in the light of functional genomics -what we can learn from the fables of Jean de la Fontaine? Peter Arensburger, Benoit Piegu, Yves Bigot To cite this version: Peter Arensburger, Benoit Piegu, Yves Bigot. The future of transposable element annotation and their classification in the light of functional genomics - what we can learn from thefables of Jean de la Fontaine?. Mobile Genetic Elements, Taylor & Francis, 2016, 6 (6), pp.e1256852. 10.1080/2159256X.2016.1256852. hal-02385838 HAL Id: hal-02385838 https://hal.archives-ouvertes.fr/hal-02385838 Submitted on 27 May 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Copyright The future of transposable element annotation and their classification in the light of functional genomics - what we can learn from the fables of Jean de la Fontaine? Peter Arensburger1, Benoît Piégu2, and Yves Bigot2 1 Biological Sciences Department, California State Polytechnic University, Pomona, CA 91768 - United States of America. 2 Physiologie de la reproduction et des Comportements, UMR INRA-CNRS 7247, PRC, 37380 Nouzilly – France Corresponding author address: Biological Sciences Department, California State Polytechnic University, Pomona, CA 91768 - United States of America.
    [Show full text]
  • The Tritryps Comparative Repeatome: Insights on Repetitive Element Evolution in Trypanosomatid Pathogens
    GBE The Tritryps Comparative Repeatome: Insights on Repetitive Element Evolution in Trypanosomatid Pathogens Sebastian Pita1,2,FlorenciaDıaz-Viraque1, Gregorio Iraola3,4, and Carlos Robello1,5,* 1Laboratory of Host Pathogen Interactions, Unidad de Biologıa Molecular, Institut Pasteur de Montevideo, Montevideo, Uruguay 2Seccion Genetica Evolutiva, Facultad de Ciencias, Universidad de la Republica, Montevideo, Uruguay 3Microbial Genomics Laboratory, Institut Pasteur Montevideo, Montevideo, Uruguay 4Centro de Biologıa Integrativa, Universidad Mayor, Santiago de Chile, Chile Downloaded from https://academic.oup.com/gbe/article-abstract/11/2/546/5306335 by guest on 31 July 2019 5Departamento de Bioquımica, Facultad de Medicina, Universidad de la Republica, Montevideo, Uruguay *Corresponding author: E-mail: [email protected]. Accepted: February 1, 2019 Data deposition: This project has been deposited at NCBI under the accesion SRP155233 Abstract The major human pathogens Trypanosoma cruzi, Trypanosoma brucei,andLeishmania major are collectively known as the Tritryps. The initial comparative analysis of their genomes has uncovered that Tritryps share a great number of genes, but repetitive DNA seems to be extremely variable between them. However, the in-depth characterization of repetitive DNA in these pathogens has been in part neglected, mainly due to the well-known technical challenges of studying repetitive sequences from de novo assemblies using short reads. Here, we compared the repetitive DNA repertories between the Tritryps genomes using genome-wide, low- coverage Illumina sequencing coupled to RepeatExplorer analysis. Our work demonstrates that this extensively implemented ap- proach for studying higher eukaryote repeatomes is also useful for protozoan parasites like trypanosomatids, as we recovered previously observed differences in the presence and amount of repetitive DNA families.
    [Show full text]
  • Transposable Elements Are Constantly Exchanged by Horizontal Transfer Reshaping Mosquito Genomes
    bioRxiv preprint doi: https://doi.org/10.1101/2020.06.23.166744; this version posted June 23, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 1 1 2 3 4 5 Transposable elements are constantly exchanged by horizontal transfer 6 reshaping mosquito genomes 7 8 9 10 Elverson Soares de Melo 1, Gabriel da Luz Wallau 1,* 11 12 13 1 Department of Entomology, Aggeu Magalhães Institute – Oswaldo Cruz Foundation (Fiocruz), 14 Recife, Pernambuco, Brazil 15 16 * Corresponding author 17 E-mail: [email protected] 18 19 20 21 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.23.166744; this version posted June 23, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 2 22 Abstract 23 Transposable elements (TEs) are a set of mobile elements within a genome. Due to their complexity, an in- 24 depth TE characterization is only available for a handful of model organisms. In the present study, we 25 performed a de novo and homology-based characterization of TEs in the genomes of 24 mosquito species 26 and investigated their mode of inheritance. More than 40% of the genome of Aedes aegypti, Aedes 27 albopictus, and Culex quinquefasciatus is composed of TEs, varying substantially among Anopheles 28 species (0.13%–19.55%).
    [Show full text]
  • Divergence of Drosophila Melanogaster Repeatomes in Response to a Sharp Microclimate Contrast in ‘Evolution Canyon’, Israel
    Classification BIOLOGICAL SCIENCES/Evolution Divergence of Drosophila melanogaster repeatomes in response to a sharp microclimate contrast in ‘Evolution Canyon’, Israel Short title Divergence of Drosophila repeat elements Young Bun Kim1, Jung Hun Oh2, Lauren J. McIver1, Eugenia Rashkovetsky3, Katarzyna Michalak1, Harold R. Garner1,4, Lin Kang1, Eviatar Nevo3§, Abraham Korol3§, Pawel Michalak1,4,5§ 1Virginia Bioinformatics Institute, Virginia Tech, Blacksburg, VA 24061, USA 2Department of Medical Physics, Memorial Sloan-Kettering Cancer Center, New York, NY 10065, USA 3Institute of Evolution, Haifa University, Haifa, Israel 4Department of Biological Sciences, Virginia Tech, Blacksburg, VA 24061, USA 5Department of Fish and Wildlife Conservation, Virginia Tech, Blacksburg, VA 24061, USA §These senior authors contributed equally to the paper Abstract Repeat sequences, especially mobile elements, make up large portions of most eukaryotic genomes and provide enormous, albeit commonly underappreciated, evolutionary potential. We analyzed repeatomes of Drosophila melanogaster that have been diverging in response to a microclimate contrast in ‘Evolution Canyon’ (Mount Carmel, Israel), a natural evolutionary laboratory with two abutting slopes at an average distance of only 200 meters posing a constant ecological challenge to their local biotas. Flies inhabiting the colder and more humid North- facing slope carried about 5% more transposable elements than those from the hot and dry South-facing slope, in parallel to a suite of other genetic and phenotypic differences between the two populations. Nearly 50% of all mobile element insertions were slope-unique, with many of them disrupting coding sequences of genes critical for cognition, olfaction, and thermotolerance, consistent with the observed patterns of thermotolerance differences and assortative mating.
    [Show full text]
  • On the Importance to Acknowledge Transposable Elements in Epigenomic Analyses
    G C A T T A C G G C A T genes Review On the Importance to Acknowledge Transposable Elements in Epigenomic Analyses Emmanuelle Lerat 1,* , Josep Casacuberta 2, Cristian Chaparro 3 and Cristina Vieira 1 1 CNRS, Laboratoire de Biométrie et Biologie Evolutive, Université de Lyon, Université Lyon 1, UMR 5558, F-69622 Villeurbanne, France; [email protected] 2 Center for Research in Agricultural Genomics, CRAG (CSIC-IRTA-UAB-UB), Campus UAB, Cerdanyola del Vallès, 08193 Barcelona, Spain; [email protected] 3 CNRS, IHPE UMR 5244, University of Perpignan Via Domitia, IFREMER, University Montpellier, F-66860 Perpignan, France; [email protected] * Correspondence: [email protected]; Tel.: +33-472-432-918; Fax: +33-472-431-388 Received: 4 February 2019; Accepted: 27 March 2019; Published: 31 March 2019 Abstract: Eukaryotic genomes comprise a large proportion of repeated sequences, an important fraction of which are transposable elements (TEs). TEs are mobile elements that have a significant impact on genome evolution and on gene functioning. Although some TE insertions could provide adaptive advantages to species, transposition is a highly mutagenic event that has to be tightly controlled to ensure its viability. Genomes have evolved sophisticated mechanisms to control TE activity, the most important being epigenetic silencing. However, the epigenetic control of TEs can also affect genes located nearby that can become epigenetically regulated. It has been proposed that the combination of TE mobilization and the induced changes in the epigenetic landscape could allow a rapid phenotypic adaptation to global environmental changes. In this review, we argue the crucial need to take into account the repeated part of genomes when studying the global impact of epigenetic modifications on an organism.
    [Show full text]
  • Impact of Repetitive DNA Elements on Snake Genome Biology and Evolution
    cells Review Impact of Repetitive DNA Elements on Snake Genome Biology and Evolution Syed Farhan Ahmad 1,2,3,4, Worapong Singchat 1,3,4, Thitipong Panthum 1,3,4 and Kornsorn Srikulnath 1,2,3,4,5,* 1 Animal Genomics and Bioresource Research Center (AGB Research Center), Faculty of Science, Kasetsart University, 50 Ngamwongwan, Chatuchak, Bangkok 10900, Thailand; [email protected] (S.F.A.); [email protected] (W.S.); [email protected] (T.P.) 2 The International Undergraduate Program in Bioscience and Technology, Faculty of Science, Kasetsart University, 50 Ngamwongwan, Chatuchak, Bangkok 10900, Thailand 3 Laboratory of Animal Cytogenetics and Comparative Genomics (ACCG), Department of Genetics, Faculty of Science, Kasetsart University, 50 Ngamwongwan, Chatuchak, Bangkok 10900, Thailand 4 Special Research Unit for Wildlife Genomics (SRUWG), Department of Forest Biology, Faculty of Forestry, Kasetsart University, 50 Ngamwongwan, Chatuchak, Bangkok 10900, Thailand 5 Amphibian Research Center, Hiroshima University, 1-3-1, Kagamiyama, Higashihiroshima 739-8526, Japan * Correspondence: [email protected] Abstract: The distinctive biology and unique evolutionary features of snakes make them fascinating model systems to elucidate how genomes evolve and how variation at the genomic level is inter- linked with phenotypic-level evolution. Similar to other eukaryotic genomes, large proportions of snake genomes contain repetitive DNA, including transposable elements (TEs) and satellite re- peats. The importance of repetitive DNA and its structural and functional role in the snake genome, remain unclear. This review highlights the major types of repeats and their proportions in snake genomes, reflecting the high diversity and composition of snake repeats. We present snakes as an emerging and important model system for the study of repetitive DNA under the impact of sex Citation: Ahmad, S.F.; Singchat, W.; and microchromosome evolution.
    [Show full text]
  • Genome Relationships and LTR-Retrotransposon Diversity in Three Cultivated Capsicum L. (Solanaceae) Species
    Genome relationships and LTR-retrotransposon diversity in three cultivated Capsicum L. (Solanaceae) species Rafael de Assis Universidade Estadual de Londrina Viviane Yumi Baba Universidade Estadual de Londrina Leonardo Adabo Cintra Universidade Estadual de Londrina Leandro Simões Azeredo Gonçalves Universidade Estadual de Londrina Rosana Rodrigues Universidade Estadual do Norte Fluminense Darcy Ribeiro Andre Vanzela ( [email protected] ) https://orcid.org/0000-0002-2442-2211 Research article Keywords: chili peppers, FISH, LTR retrotransposons, plant genome, transposable elements Posted Date: October 23rd, 2019 DOI: https://doi.org/10.21203/rs.2.16380/v1 License: This work is licensed under a Creative Commons Attribution 4.0 International License. Read Full License Page 1/25 Abstract Background: Plant genomes are rich in repetitive sequences, and Transposable Elements (TE, mobile fraction) are the most accumulated of them. This mobile fraction can be divided into Class I (retrotransposons) and Class II (transposons). Retrotransposons that are transposed using an intermediated RNA and accumulate in a “copy-and-paste” way have been screened in three completely sequenced genomes of peppers (Solanaceae family). The goal of this study was to understand the genome relationships among Capsicum annuum , C. chinense and C. baccatum , based on a comparative analysis of function, diversity and the chromosome distribution of TE lineages in the Capsicum karyotypes. Due to the great commercial importance of pepper in natura , as a spice or as an ornamental plant, these genomes have been widely sequenced, and all the assemblies are available in the SolGenomics group. These sequences have been used to compare all repetitive fractions from a cytogenomic point of view.
    [Show full text]
  • Less Effective Selection Leads to Larger Genomes
    Downloaded from genome.cshlp.org on September 29, 2021 - Published by Cold Spring Harbor Laboratory Press Research Less effective selection leads to larger genomes Tristan Lefébure,1 Claire Morvan,1 Florian Malard,1 Clémentine François,1 Lara Konecny-Dupré,1 Laurent Guéguen,2 Michèle Weiss-Gayet,3 Andaine Seguin-Orlando,4 Luca Ermini,4 Clio Der Sarkissian,4 N. Pierre Charrier,1 David Eme,1 Florian Mermillod-Blondin,1 Laurent Duret,2 Cristina Vieira,2,5 Ludovic Orlando,4,6 and Christophe Jean Douady1,5 1Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5023, ENTPE, Laboratoire d’Ecologie des Hydrosystèmes Naturels et Anthropisés, F-69622 Villeurbanne, France; 2Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5558, Laboratoire de Biométrie et Biologie Evolutive, F-69622 Villeurbanne, France; 3Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5310, INSERM, Institut NeuroMyoGène, F-69622 Villeurbanne, France; 4Center for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350K Copenhagen, Denmark; 5Institut Universitaire de France, F-75005 Paris, France; 6Université de Toulouse, University Paul Sabatier (UPS), CNRS UMR 5288, Laboratoire AMIS, F-31073 Toulouse, France The evolutionary origin of the striking genome size variations found in eukaryotes remains enigmatic. The effective size of populations, by controlling selection efficacy, is expected to be a key parameter underlying genome size evolution. However, this hypothesis has proved difficult to investigate using empirical data sets. Here, we tested this hypothesis using 22 de novo transcriptomes and low-coverage genomes of asellid isopods, which represent 11 independent habitat shifts from surface water to resource-poor groundwater.
    [Show full text]
  • Dark Matter of Primate Genomes: Satellite DNA Repeats and Their Evolutionary Dynamics
    cells Review Dark Matter of Primate Genomes: Satellite DNA Repeats and Their Evolutionary Dynamics Syed Farhan Ahmad 1,2, Worapong Singchat 1,2, Maryam Jehangir 1,3, Aorarat Suntronpong 1,2, Thitipong Panthum 1,2, Suchinda Malaivijitnond 4,5 and Kornsorn Srikulnath 1,2,4,6,7,* 1 Laboratory of Animal Cytogenetics and Comparative Genomics (ACCG), Department of Genetics, Faculty of Science, Kasetsart University, Bangkok 10900, Thailand; [email protected] (S.F.A.); [email protected] (W.S.); [email protected] (M.J.); [email protected] (A.S.); [email protected] (T.P.) 2 Special Research Unit for Wildlife Genomics (SRUWG), Department of Forest Biology, Faculty of Forestry, Kasetsart University, Bangkok 10900, Thailand 3 Department of Structural and Functional Biology, Institute of Bioscience at Botucatu, São Paulo State University (UNESP), Botucatu, São Paulo 18618-689, Brazil 4 National Primate Research Center of Thailand, Chulalongkorn University, Saraburi 18110, Thailand; [email protected] 5 Department of Biology, Faculty of Science, Chulalongkorn University, Bangkok 10330, Thailand 6 Center of Excellence on Agricultural Biotechnology (AG-BIO/PERDO-CHE), Bangkok 10900, Thailand 7 Omics Center for Agriculture, Bioresources, Food and Health, Kasetsart University (OmiKU), Bangkok 10900, Thailand * Correspondence: [email protected] Received: 27 October 2020; Accepted: 16 December 2020; Published: 18 December 2020 Abstract: A substantial portion of the primate genome is composed of non-coding regions, so-called “dark matter”, which includes an abundance of tandemly repeated sequences called satellite DNA. Collectively known as the satellitome, this genomic component offers exciting evolutionary insights into aspects of primate genome biology that raise new questions and challenge existing paradigms.
    [Show full text]
  • Decoding the Role of Satellite DNA in Genome Architecture and Plasticity—An Evolutionary and Clinical Affair
    G C A T T A C G G C A T genes Review Decoding the Role of Satellite DNA in Genome Architecture and Plasticity—An Evolutionary and Clinical Affair Sandra Louzada 1,2, Mariana Lopes 1,2 , Daniela Ferreira 1,2 , Filomena Adega 1,2, Ana Escudeiro 1,2, Margarida Gama-Carvalho 2 and Raquel Chaves 1,2,* 1 Laboratory of Cytogenomics and Animal Genomics (CAG), Department of Genetics and Biotechnology (DGB), University of Trás-os-Montes and Alto Douro (UTAD), 5000-801 Vila Real, Portugal; [email protected] (S.L.); [email protected] (M.L.); [email protected] (D.F.); fi[email protected] (F.A.); [email protected] (A.E.) 2 Biosystems and Integrative Sciences Institute (BioISI), Faculty of Sciences, University of Lisboa, 1749-016 Lisbon, Portugal; [email protected] * Correspondence: [email protected] Received: 16 December 2019; Accepted: 8 January 2020; Published: 9 January 2020 Abstract: Repetitive DNA is a major organizational component of eukaryotic genomes, being intrinsically related with their architecture and evolution. Tandemly repeated satellite DNAs (satDNAs) can be found clustered in specific heterochromatin-rich chromosomal regions, building vital structures like functional centromeres and also dispersed within euchromatin. Interestingly, despite their association to critical chromosomal structures, satDNAs are widely variable among species due to their high turnover rates. This dynamic behavior has been associated with genome plasticity and chromosome rearrangements, leading to the reshaping of genomes. Here we present the current knowledge regarding satDNAs in the light of new genomic technologies, and the challenges in the study of these sequences. Furthermore, we discuss how these sequences, together with other repeats, influence genome architecture, impacting its evolution and association with disease.
    [Show full text]
  • Heterochromatin Evolution in Arachis Investigated Through Genome-Wide
    Planta https://doi.org/10.1007/s00425-019-03096-4 ORIGINAL ARTICLE Heterochromatin evolution in Arachis investigated through genome‑wide analysis of repetitive DNA Sergio S. Samoluk1 · Laura M. I. Chalup1 · Carolina Chavarro2 · Germán Robledo1,3 · David J. Bertioli2 · Scott A. Jackson2 · Guillermo Seijo1,3 Received: 30 October 2018 / Accepted: 18 January 2019 © Springer-Verlag GmbH Germany, part of Springer Nature 2019 Abstract Main conclusion The most conspicuous diference among chromosomes and genomes in Arachis species, the patterns of heterochromatin, was mainly modeled by diferential amplifcation of diferent members of one superfamily of satellite DNAs. Divergence in repetitive DNA is a primary driving force for genome and chromosome evolution. Section Arachis is karyo- typically diverse and has six diferent genomes. Arachis glandulifera (D genome) has the most asymmetric karyotype and the highest reproductive isolation compared to the well-known A and B genome species. These features make A. glandulifera an interesting model species for studying the main repetitive components that accompanied the genome and chromosome diversifcation in the section. Here, we performed a genome-wide analysis of repetitive sequences in A. glandulifera and investigated the chromosome distribution of the identifed satellite DNA sequences (satDNAs). LTR retroelements, mainly the Ty3-gypsy families “Fidel/Feral” and “Pipoka/Pipa”, were the most represented. Comparative analyses with the A and B genomes showed that many of the previously described transposable elements (TEs) were diferently represented in the D genome, and that this variation accompanied changes in DNA content. In addition, four major satDNAs were character- ized. Agla_CL8sat was the major component of pericentromeric heterochromatin, while Agla_CL39sat, Agla_CL69sat, and Agla_CL122sat were found in heterochromatic and/or euchromatic regions.
    [Show full text]