Centromeric enrichment of LINE-1 retrotransposons and its significance for the chromosome evolution of Phyllostomid bats

Despite their ubiquitous incidence, little is known about the chromosomal distribution of long interspersed elements (LINEs) in mammalian genomes. Phyllostomid bats, characterized by lineages with distinct trends of chromosomal evolution coupled with remarkable ecological and taxonomic diversity, represent good models to understand how these repetitive sequences contribute to the evolution of genome architecture and its link to lineage diversification. To test the hypothesis that LINE-1 sequences were important modifiers of bat genome architecture, we characterized the distribution of LINE-1-derived sequences on genomes of 13 phyllostomid species within a phylogenetic framework. We found massive accumulation of LINE-1 elements in the centromeres of most species: a rare phenomenon on mammalian genomes. We hypothesize that expansion of these elements has occurred early in the radiation of phyllostomids and recurred episodically. LINE-1 expansions on centromeric heterochromatin probably spurred chromosomal change before the radiation of phyllostomids into the extant 11 subfamilies and contributed to the high degree of karyotypic variation observed among different lineages. Understanding centromere architecture in a variety of taxa promises to explain how lineage-specific changes on centromere structure can contribute to karyotypic diversity while not disrupting functional constraints for proper cell division.

[1]  N. Santos,et al.  Characterization of the constitutive heterochromatin of Carollia perspicillata (Phyllostomidae, Chiroptera) using the base-specific fluorochromes, CMA3 (GC) and DAPI (AT) , 1998 .

[2]  M. Bullejos,et al.  Retroelements (LINEs and SINEs) in vole genomes: Differential distribution in the constitutive heterochromatin , 2008, Chromosome Research.

[3]  Adam Godzik,et al.  Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences , 2006, Bioinform..

[4]  A. Troxel,et al.  Genomic characterization of recent human LINE-1 insertions: evidence supporting random insertion. , 2001, Genome research.

[5]  M. Ferguson-Smith,et al.  Chromosomal Homologies among Vampire Bats Revealed by Chromosome Painting (Phyllostomidae, Chiroptera) , 2010, Cytogenetic and Genome Research.

[6]  August E. Woerner,et al.  Gibbon genome and the fast karyotype evolution of small apes , 2014 .

[7]  G. Valente,et al.  Organization of Repeated DNA Elements in the Genome of the Cichlid Fish Cichla kelberi and Its Contributions to the Knowledge of Fish Genomes , 2009, Cytogenetic and Genome Research.

[8]  Molecular cytogenetic characterization of the Amazon River dolphin Inia geoffrensis , 2012, Genetica.

[9]  M. Ferguson-Smith,et al.  Reciprocal chromosome painting between two South American bats: Carollia brevicauda and Phyllostomus hastatus (Phyllostomidae, Chiroptera) , 2005, Chromosome Research.

[10]  Paul R. Sesink Clee,et al.  Environmental variation and rivers govern the structure of chimpanzee genetic diversity in a biodiversity hotspot , 2015, BMC Evolutionary Biology.

[11]  J. V. Moran,et al.  The Influence of LINE-1 and SINE Retrotransposons on Mammalian Genomes , 2015, Microbiology spectrum.

[12]  H. Akaike.  A new look at the statistical model identification , 1974 .

[13]  R. Baker,et al.  Reduced Number of Ribosomal Sites in Bats: Evidence for a Mechanism to Contain Genome Size , 1992 .

[14]  M. Varella‐Garcia,et al.  A survey of cytogenetic data on Brazilian bats , 1989 .

[15]  Miriam K. Konkel,et al.  Centromere Remodeling in Hoolock leuconedys (Hylobatidae) by a New Transposable Element Unique to the Gibbons , 2012, Genome biology and evolution.

[16]  R. Baker,et al.  TIMESCALE OF DIVERSIFICATION OF FEEDING STRATEGY AND MORPHOLOGY IN NEW WORLD LEAF-NOSED BATS ( PHYLLOSTOMIDAE ) : A PHYLOGENETIC PERSPECTIVE , 2010 .

[17]  C. Redi,et al.  Quantitative variation of LINE-1 sequences in five species and three subspecies of the subgenus Mus and in five Robertsonian races of Mus musculus domesticus , 2009, Chromosome Research.

[18]  D. Mager,et al.  Gene Properties and Chromatin State Influence the Accumulation of Transposable Elements in Genes , 2012, PloS one.

[19]  G. Presting,et al.  Widespread Gene Conversion in Centromere Cores , 2010, PLoS biology.

[20]  R. O’Neill,et al.  Recent Amplification of the Kangaroo Endogenous Retrovirus, KERV, Limited to the Centromere , 2011, Journal of Virology.

[21]  P. Martinez,et al.  A comparative study on karyotypic diversification rate in mammals , 2017, Heredity.

[22]  Fengtang Yang,et al.  Integration of molecular cytogenetics, dated molecular phylogeny, and model-based predictions to understand the extreme chromosome reorganization in the Neotropical genus Tonatia (Chiroptera: Phyllostomidae) , 2015, BMC Evolutionary Biology.

[23]  H. Hameister,et al.  ZOO-FISH Analysis in a Species of the Order Chiroptera: Glossophaga soricina (Phyllostomidae) , 2004, Chromosome Research.

[24]  P. Racey.  Ecological and Behavioral Methods for the Study of Bats , 2011 .

[25]  O. Ryder,et al.  Genomic distribution of heterochromatic sequences in equids: implications to rapid chromosomal evolution. , 1991, The Journal of heredity.

[26]  S. Henikoff,et al.  Diversity in the organization of centromeric chromatin. , 2015, Current opinion in genetics & development.

[27]  R. Bass.  Systematics of the Desmodonitinae and Phyllonycterinae (Chiroptera: Phyllostomatidae) based on G-band chromosomal homologies , 1978 .

[28]  T. Gregory,et al.  Patterns of genome size diversity in bats (order Chiroptera). , 2013, Genome.

[29]  R. Baker,et al.  Transposable elements and the evolution of genome organization in mammals , 2004, Genetica.

[30]  R. Baker,et al.  RETROTRANSPOSON MYS IS CONCENTRATED ON THE SEX CHROMOSOMES: IMPLICATIONS FOR COPY NUMBER CONTAINMENT , 1990, Evolution; international journal of organic evolution.

[31]  B. Ng,et al.  Molecular Cytogenetic Characterization of the Genome Organization of the 6-Banded Armadillo (Euphractus sexcinctus) , 2010, Cytogenetic and Genome Research.

[32]  A. T. Sumner.  A simple technique for demonstrating centromeric heterochromatin. , 1972, Experimental cell research.

[33]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[34]  T. Eickbush,et al.  Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: A mechanism for non-LTR retrotransposition , 1993, Cell.

[35]  R. O’Neill,et al.  Species-specific shifts in centromere sequence composition are coincident with breakpoint reuse in karyotypically divergent lineages , 2007, Genome Biology.

[36]  F. Elder,et al.  Yeast stimulation of bone marrow mitosis for cytogenetic investigations. , 1980, Cytogenetics and cell genetics.

[37]  M. Batzer,et al.  Mammalian retroelements. , 2002, Genome research.

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

[39]  Y. Yonenaga-Yassuda,et al.  Comparative karyology of Brazilian vampire bats Desmodus rotundus and Diphylla ecaudata (Phyllostomidae, Chiroptera): banding patterns, base-specific fluorochromes and FISH of ribosomal genes. , 2004, Hereditas.

[40]  N. Santos,et al.  Use of fluorochromes chromomycin A3 and DAPI to study constitutive heterochromatin and NORs in four species of bats (Phyllostomidae) , 1998 .

[41]  S. Elgin,et al.  Epigenetic Codes for Heterochromatin Formation and Silencing Rounding up the Usual Suspects , 2002, Cell.

[42]  C. ozouF-cosTaz,et al.  LINE-1 amplification accompanies explosive genome repatterning in rodents , 2005, Chromosome Research.

[43]  S. Boissinot,et al.  The Genomic Distribution of L1 Elements: The Role of Insertion Bias and Natural Selection , 2006, Journal of biomedicine & biotechnology.

[44]  Can Alkan,et al.  Genome-wide characterization of centromeric satellites from multiple mammalian genomes. , 2011, Genome research.

[45]  M. Bullejos,et al.  Distribution of L1-retroposons on the giant sex chromosomes of Microtus cabrerae (Arvicolidae, Rodentia): functional and evolutionary implications , 2006, Chromosome Research.

[46]  S. O’Brien,et al.  Atlas of mammalian chromosomes , 2006 .

[47]  Mark A. Miller,et al.  Creating the CIPRES Science Gateway for inference of large phylogenetic trees , 2010, 2010 Gateway Computing Environments Workshop (GCE).

[48]  Robert C. Edgar,et al.  MUSCLE: a multiple sequence alignment method with reduced time and space complexity , 2004, BMC Bioinformatics.

[49]  T. J. Robinson,et al.  Absence of hypomethylation and LINE-1 amplification in a white × black rhinoceros hybrid , 2006, Genetica.

[50]  J W Gray,et al.  Cytogenetic analysis using quantitative, high-sensitivity, fluorescence hybridization. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[51]  Y. Gray,et al.  It takes two transposons to tango: transposable-element-mediated chromosomal rearrangements. , 2000, Trends in genetics : TIG.

[52]  J. Salces-Ortiz,et al.  Looking for adaptive footprints in the HSP90AA1 ovine gene , 2015, BMC Evolutionary Biology.

[53]  R. O’Neill,et al.  Cytogenetic and Molecular Evaluation of Centromere-Associated DNA Sequences From a Marsupial (Macropodidae: Macropus rufogriseus) X Chromosome , 2006, Genetics.

[54]  LINE-1 distribution in six rodent genomes follow a species-specific pattern , 2016, Journal of Genetics.

[55]  R. Baker,et al.  Evolutionary History of Bats: Molecular time scale of diversification of feeding strategy and morphology in New World Leaf-Nosed Bats (Phyllostomidae): a phylogenetic perspective , 2012 .

[56]  P. Deininger,et al.  Inviting instability: Transposable elements, double-strand breaks, and the maintenance of genome integrity. , 2007, Mutation research.

[57]  Fengtang Yang,et al.  Phylogenetic Reconstruction by Cross-Species Chromosome Painting and G-Banding in Four Species of Phyllostomini Tribe (Chiroptera, Phyllostomidae) in the Brazilian Amazon: An Independent Evidence for Monophyly , 2015, PloS one.

[58]  D. Posada.  jModelTest: phylogenetic model averaging. , 2008, Molecular biology and evolution.

[59]  T. Eickbush,et al.  The diversity of retrotransposons and the properties of their reverse transcriptases. , 2008, Virus research.

[60]  R. Baker,et al.  Distribution of LINEs and other repetitive elements in the karyotype of the bat Carollia: implications for X-chromosome inactivation , 2002, Cytogenetic and Genome Research.

[61]  H. Wichman,et al.  Reviving the Dead: History and Reactivation of an Extinct L1 , 2014, PLoS genetics.

[62]  J. Jurka,et al.  L1 repeat is a basic unit of heterochromatin satellites in cetaceans. , 1998, Molecular biology and evolution.

[63]  T. J. Robinson,et al.  LINE-1 distribution in Afrotheria and Xenarthra: implications for understanding the evolution of LINE-1 in eutherian genomes , 2004, Chromosoma.

[64]  M. S. Calixto,et al.  Cytotaxonomy of the subgenus Artibeus (Phyllostomidae, Chiroptera) by characterization of species-specific markers , 2012, Comparative cytogenetics.

[65]  R. Baker,et al.  Karyotypic Evolution in Bats: Evidence of Extensive and Conservative Chromosomal Evolution in Closely Related Taxa , 1980 .

[66]  V. Pande,et al.  Undermethylation associated with retroelement activation and chromosome remodelling in an interspecific mammalian hybrid , 2022 .

[67]  Y. Matsuda,et al.  X accumulation of LINE-1 retrotransposons in Tokudaia osimensis, a spiny rat with the karyotype XO , 2006, Cytogenetic and Genome Research.

[68]  G. Dobigny,et al.  Robertsonian fusions, pericentromeric repeat organization and evolution: a case study within a highly polymorphic rodent species, Gerbillus nigeriae , 2010, Chromosome Research.

[69]  S. Boissinot,et al.  Adaptive evolution in LINE-1 retrotransposons. , 2001, Molecular biology and evolution.

[70]  S. Boissinot,et al.  L1 (LINE-1) retrotransposon diversity differs dramatically between mammals and fish. , 2004, Trends in genetics : TIG.

[71]  A. Rambaut,et al.  BEAST: Bayesian evolutionary analysis by sampling trees , 2007, BMC Evolutionary Biology.

[72]  Fengtang Yang,et al.  Chromosomal evolution among leaf-nosed nectarivorous bats – evidence from cross-species chromosome painting (Phyllostomidae, Chiroptera) , 2013, BMC Evolutionary Biology.

[73]  Fengtang Yang,et al.  Two new cytotypes reinforce that Micronycteris hirsuta Peters, 1869 does not represent a monotypic taxon , 2013, BMC Genetics.

[74]  N. Fedoroff,et al.  Investigation of the organization of mammalian chromosomes at the DNA sequence level. , 1976, Federation proceedings.

[75]  N. Santos,et al.  Comparative cytogenetic analysis between Lonchorhina aurita and Trachops cirrhosus (Chiroptera, Phyllostomidae) , 2009, Genetics and molecular biology.

[76]  R. O’Neill,et al.  The Evolution of Centromeric DNA Sequences , 2014 .