Abstract
Repetitive DNA is a major component in most eukaryotic genomes but is ignored in most genome sequencing projects. Here, we report the quantitative composition in repetitive DNA for a supernumerary (B) chromosome, in the migratory locust (Locusta migratoria), by Illumina sequencing of genomic DNA from B-carrying and B-lacking individuals and DNA obtained from a microdissected B chromosome, as well as the physical mapping of some elements. B chromosome DNA of 94.9% was repetitive, in high contrast with the 64.1% of standard (A) chromosomes. B chromosomes are enriched in satellite DNA (satDNA) (65.2% of B-DNA), with a single satellite (LmiSat02-176) comprising 55% of the B. Six satDNAs were visualized by FISH on the B chromosome, and the only A chromosome carrying all these satellites was autosome 9, pointing to this chromosome, along with autosome 8 (which shares histone genes with the B) as putative ancestors of the B chromosome. We found several transposable elements (TEs) showing nucleotidic variation specific to B-carrying individuals, which was also present in B-carrying transcriptomes. Remarkably, an interstitial region of the B chromosome included a 17 kb chimera composed of 29 different TEs, suggesting reiterative TE insertion in this B chromosome region.
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References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Anjos A, Ruiz-Ruano FJ, Camacho JPM, Loreto V, Cabrero J, de Souza MJ (2015) U1 snDNA clusters in grasshoppers: chromosomal dynamics and genomic organization. Heredity 114:207–219
Bao W, Kojima KK, Kohany O (2015) Repbase update, a database of repetitive elements in eukaryotic genomes. Mob DNA 6:11
Bauerly E, Hughes SE, Vietti DR, Miller DE, McDowell W, Hawley RS (2014) Discovery of supernumerary B chromosomes in Drosophila melanogaster. Genetics 196:1007–1016
Bradfield JY, Locke J, Wyatt GR (1985) An ubiquitous interspersed DNA sequence family in an insect. DNA 4:357–363
Bueno D, Palacios-Gimenez OM, Cabral-de-Mello DC (2013) Chromosomal mapping of repetitive DNAs in the grasshopper Abracris flavolineata reveal possible ancestry of the B chromosome and H3 histone spreading. PLoS One 8:e66532
Cabrero J, Viseras E, Camacho JPM (1984) The B-chromosomes of Locusta migratoria I. Detection of negative correlation between mean chiasma frequency and the rate of accumulation of the B’s; a reanalysis of the available data about the transmission of these B-chromosomes. Genetica 64:155–164
Cabrero J, Bakkali M, Bugrov A, Warchalowska-Sliwa E, López-León MD, Perfectti F, Camacho JPM (2003) Multiregional origin of B chromosomes in the grasshopper Eyprepocnemis plorans. Chromosoma 112:207–211
Camacho JPM, Sharbel TF, Beukeboom LW (2000) B-chromosome evolution. Philos Trans R Soc Lond Ser B Biol Sci 355:163–178
Camacho JPM (2005) B chromosomes. In: Gregory TR (ed) The evolution of the genome. Elsevier, San Diego, pp 223–286
Dearn JM (1974) Phase transformation and chiasma frequency variation in locusts. Chromosoma 45:321–338
Drummond AJ, Ashton B, Cheung M, Heled J, Kearse M (2009) Geneious v.4.8.5, biomatters ltd. Aukland, New Zealand
Eickbush TH, Eickbush DG (2007) Finely orchestrated movements: evolution of the ribosomal RNA genes. Genetics 175:477–485
Hahn C, Bachmann L, Chevreux B (2013) Reconstructing mitochondrial genomes directly from genomic next-generation sequencing reads—a baiting and iterative mapping approach. Nucleic Acids Res 41:e129
Houben A, Banaei-Moghaddam AM, Klemme S, Timmis JN (2014) Evolution and biology of supernumerary B chromosomes, Cell Mol. Life Sci 71:467–478
Hsiang W (1958) Cytological studies on migratory locust hybrid, Locusta migratoria migratoria L. x Locusta migratoria manilensis Meyen. Acta Zool Sin 10:53–59
Hu J, Chen C, Peever T, Dang H, Lawrence C, Mitchell T (2012) Genomic characterization of the conditionally dispensable chromosome in Alternaria arborescens provides evidence for horizontal gene transfer. BMC Genomics 13:171
Huang W, Du Y, Zhao X, Jin W (2016) B chromosome contains active genes and impacts the transcription of a chromosomes in maize (Zea mays L.) BMC Plant Biol 16:1
Itoh H (1934) Chromosomal variation in the spermatogenesis of a grasshopper, Locusta danica. Jap J Genet 10:115–134
Jang TS, Parker JS, Weiss-Schneeweiss H (2016) Structural polymorphisms and distinct genomic composition suggest recurrent origin and ongoing evolution of B chromosomes in the Prospero autumnale complex (Hyacinthaceae). New Phytol 210:669–679
Kayano H (1971) Accumulation of B chromosomes in the germ line of Locusta migratoria. Heredity 27:119–123
Kent WJ (2002) BLAT—the BLAST-like alignment tool. Genome Res 12:656–664
Kim YB, Oh JH, McIver LJ, Rashkovetsky E, Michalak K, Garner HR, Kang L, Nevo E, Korol AB, Michalak P (2014) Divergence of Drosophila melanogaster repeatomes in response to a sharp microclimate contrast in evolution canyon, Israel. Proc Natl Acad Sci U S A 111:10630–10635
King M, John B (1980) Regularities and restrictions governing C-band variation in acridoid grasshoppers. Chromosoma 76:123–150
Klemme S, Banaei-Moghaddam AM, Macas J, Wicker T, Novák P, Houben A (2013) High-copy sequences reveal distinct evolution of the rye B chromosome. New Phytol 199:550–558
Kour G, Kaul S, Dhar MK (2013) Molecular characterization of repetitive DNA sequences from B chromosome in Plantago lagopus L. Cytogenet Genome Res 142:121–128
Lespinasse R (1973) Comportement des chromosomes surnuméraires et relation avec le taux de mortalité dans une population africaine de Locusta migratoria migratorioides. Chromosoma 44:107–122
Lespinasse R (1977) Analyse de la transmission des chromosomes surnuméraires chez Locusta migratoria migratorioides R. Et F. (Orthoptera, Acrididae). Chromosoma 59:307–322
Li W, Fu L, Niu B, Wu S, Wooley J (2012) Ultrafast clustering algorithms for metagenomic sequence analysis. Brief Bioinform 13:656–668
Littlewood DTJ, Olson PD (2001) Small subunit rDNA and the Platyhelminthes: signal, noise, conflict and compromise. In: Littlewood DTJ, Bray RA (eds) Interrelationships of the Platyhelminthes. Taylor & Francis, London, pp 262–278
Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964
Ma W, Gabriel TS, Martis MM, Gursinsky T, Schubert V, Vrána J, Doležel J, Grundlach H, Alschmied L, Scholz U, Himmelbach A, Behrens S, Banaei-Moghaddam AM, Houben A (2017) Rye B chromosomes encode a functional Argonaute-like protein with in vitro slicer activities similar to its a chromosome paralog. New Phytol 213:916–928
Martis MM, Klemme S, Banaei-Moghaddam AM, Blattner FR, Macas J, Schmutzer T, Scholz U, Gundlach H, Wicker T, Šimková H, Novák P, Neumann P, Kubaláková M, Bauer E, Haseneyer G, Fuchs J, Doležel J, Stein N, Mayer KF, Houben A (2012) Selfish supernumerary chromosome reveals its origin as a mosaic of host genome and organellar sequences. Proc Natl Acad Sci U S A 109:13343–13346
Menezes-de-Carvalho NZ, Palacios-Gimenez OM, Milani D, Cabral-de-Mello DC (2015) High similarity of U2 snDNA sequence between a and B chromosomes in the grasshopper Abracris flavolineata. Mol Gen Genomics 290:1787–1792
Miga KH (2015) Completing the human genome: the progress and challenge of satellite DNA assembly. Chromosom Res 23:421–426
Montiel EE, Cabrero J, Camacho JPM, López-León MD (2012) Gypsy, RTE and mariner transposable elements populate Eyprepocnemis plorans genome. Genetica 140:365–374
Montiel EE, Cabrero J, Ruiz-Estévez M, Burke WD, Eickbush TH, Camacho JPM, López-León MD (2014) Preferential occupancy of R2 retroelements on the B chromosomes of the grasshopper Eyprepocnemis plorans. PLoS One 9:e91820
Navarro-Dominguez B, Ruiz-Ruano FJ, Cabrero J, Corral JM, López-León MD, Sharbel TF, Camacho JPM (2017) Protein-coding genes in B chromosomes of the grasshopper Eyprepocnemis plorans. Sci Rep 7:45200
Ning Z, Cox AJ, Mullikin JC (2001) SSAHA: a fast search method for large DNA databases. Genome Res 11:1725–1729
Novák P, Neumann P, Pech J, Steinhaisl J, Macas J (2013) RepeatExplorer: a galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads. Bioinformatics 29:792–793
Nur U (1969) Mitotic instability leading to an accumulation of B-chromosomes in grasshoppers. Chromosoma 27:1–19
Oliveira NL, Cabral-de-Mello DC, Rocha MF, Loreto V, Martins C, Moura RC (2011) Chromosomal mapping of rDNAs and H3 histone sequences in the grasshopper Rhammatocerus brasiliensis (Acrididae, Gomphocerinae): extensive chromosomal dispersion and co-localization of 5S rDNA/H3 histone clusters in the a complement and B chromosome. Mol Cytogenet 4:24
Pardo MC, López-León MD, Cabrero J, Camacho JPM (1994) Transmission analysis of mitotically unstable B chromosomes in Locusta migratoria. Genome 37:1027–1034
Pardo MC, Lopez-Leon MD, Viseras E, Cabrero J, Camacho JPM (1995) Mitotic instability of B chromosomes during embryo development in Locusta migratoria. Heredity 74:164–169
Peng SF, Cheng YM (2011) Characterization of satellite CentC repeats from heterochromatic regions on the long arm of maize B-chromosome. Chromosom Res 19:183–191
Poletto AB, Ferreira IA, Martins C (2010) The B chromosomes of the African cichlid fish Haplochromis obliquidens harbour 18S rRNA gene copies. BMC Genet 11:1
Rees H, Jamieson A (1954) A supernumerary chromosome in Locusta. Nature 173:43–44
Ruiz-Estévez M, Cabrero J, Camacho JPM, López-León MD (2014) B chromosomes in the grasshopper Eyprepocnemis plorans are present in all body parts analyzed and show extensive variation for rDNA copy number. Cytogenet Genome Res 143:268–274
Ruiz-Ruano FJ, Ruiz-Estévez M, Rodríguez-Pérez J, López-Pino JL, Cabrero J, Camacho JPM (2011) DNA amount of X and B chromosomes in the grasshoppers Eyprepocnemis plorans and Locusta migratoria. Cytogenet Genome Res 134:120–126
Ruiz-Ruano FJ, Cuadrado Á, Montiel EE, Camacho JPM, López-León MD (2015) Next generation sequencing and FISH reveal uneven and nonrandom microsatellite distribution in two grasshopper genomes. Chromosoma 124:221–234
Ruiz-Ruano FJ, López-León MD, Cabrero J, Camacho JPM (2016) High-throughput analysis of the satellitome illuminates satellite DNA evolution. Sci Rep 6:28333
Ruiz-Ruano FJ, Cabrero J, López-León MD, Camacho JPM (2017) Satellite DNA content illuminates the ancestry of a supernumerary (B) chromosome. Chromosoma 126:487–500
Schwarzacher T, Heslop-Harrison P (2000) Practical in situ hybridization. BIOS Scientific Publishers Ltd.
Teruel M, Cabrero J, Perfectti F, Camacho JPM (2010) B chromosome ancestry revealed by histone genes in the migratory locust. Chromosoma 119:217–225
Teruel M, Ruiz-Ruano FJ, Marchal JA, Sánchez A, Cabrero J, Camacho JPM, Perfectti F (2014) Disparate molecular evolution of two types of repetitive DNAs in the genome of the grasshopper Eyprepocnemis plorans. Heredity 112:531–542
Thorvaldsdóttir H, Robinson JT, Mesirov JP (2013) Integrative genomics viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 14:178–192
Silva DM, Pansonato-Alves JC, Utsunomia R, Araya-Jaime C, Ruiz-Ruano FJ, Daniel SN, Hashimoto DT, Oliveira C, JPM C, Porto-Foresti F, Foresti F (2014) Delimiting the origin of a B chromosome by FISH mapping, chromosome painting and DNA sequence analysis in Astyanax paranae (Teleostei, Characiformes). PLoS One 9:e94896
Smit AFA, Hubley R (2017) RepeatModeler Open-1.0. http://www.repeatmasker.org
Smit AFA, Hubley R, Green P (2017) RepeatMasker Open-4.0. http://www.repeatmasker.org
Smith GP (1976) Evolution of repeated DNA sequences by unequal crossover. Science 191:528–535
Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3—new capabilities and interfaces. Nucleic Acids Res 40:e115
Utsunomia R, Silva DM, Ruiz-Ruano FJ, Araya-Jaime C, Pansonato-Alves JC, Scacchetti PC, Hashimoto DT, Oliveira C, Trifonov VA, Porto-Foresti F, Camacho JPM, Foresti F (2016) Uncovering the ancestry of B chromosomes in Moenkhausia sanctaefilomenae (Teleostei, Characidae). PLoS One 11:e0150573
Valente GT, Conte MA, Fantinatti BEA, Cabral-de-Mello DC, Carvalho RF, Vicari MR, Kocher TD, Martins C (2014) Origin and evolution of B chromosomes in the cichlid fish Astatotilapia latifasciata based on integrated genomic analyses. Mol Biol Evol 31:2061–2072
Viseras E, Camacho JPM, Cano MI, Santos JL (1990) Relationship between mitotic instability and accumulation of B chromosomes in males and females of Locusta migratoria. Genome 33:23–29
Wang X, Fang X, Yang P, Jiang X, Jiang F, Zhao D, Li B, Cui F, Wei J, Ma C et al (2014) The locust genome provides insight into swarm formation and long-distance flight. Nat Commun 5:2957
Xie S, Marasek-Ciolakowska A, Ramanna MS, Arens P, Visser RG, van Tuyl JM (2014) Characterization of B chromosomes in Lilium hybrids through GISH and FISH. Plant Syst Evol 300:1771–1777
Zhou Q, Zhu HM, Huang QF, Zhao L, Zhang GJ, Roy SW, Vicoso B, Xuan ZL, Ruan J, Zhang Y, Zhao RP, Ye C, Zhang XQ, Wang J, Wang W, Bachtrog D (2012) Deciphering neo-sex and B chromosome evolution by the draft genome of Drosophila albomicans. BMC Genomics 13:109
Acknowledgements
We thank Francisco Jiménez-Cazalla and Jorge Doña for their collaboration in obtaining the material from Los Barrios (Cádiz). This study was supported by grants from the Spanish Plan Andaluz de Investigacion (CVI-6649) and Secretaría de Estado de Investigación, Desarrollo e Innovación (CGL2015-70750-P), and was partially performed by FEDER funds. FJ Ruiz-Ruano was supported by a Junta de Andalucía fellowship.
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Ruiz-Ruano, F.J., Cabrero, J., López-León, M.D. et al. Quantitative sequence characterization for repetitive DNA content in the supernumerary chromosome of the migratory locust. Chromosoma 127, 45–57 (2018). https://doi.org/10.1007/s00412-017-0644-7
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DOI: https://doi.org/10.1007/s00412-017-0644-7