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Heterochromatin-Enriched Assemblies Reveal the Sequence and Organization of the Drosophila melanogaster Y Chromosome

Chang, Ching-Ho, Larracuente, Amanda M·2019·Genetics
DOI 10.1534/genetics.118.301765PMC PMC6325706

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Abstract

Heterochromatic repeat-rich regions are often missing from even the best genome assemblies. Chang and Larracuente designed a de novo assembly strategy to improve the Drosophila melanogaster assembly in heterochromatin, extending the reference assembly by 11.9 Mb, including 10.6 Mb from the Y chromosome..... Heterochromatic regions of the genome are repeat-rich and poor in protein coding genes, and are therefore underrepresented in even the best genome assemblies. One of the most difficult regions of the genome to assemble are sex-limited chromosomes. The Drosophila melanogaster Y chromosome is entirely heterochromatic, yet has wide-ranging effects on male fertility, fitness, and genome-wide gene expression. The genetic basis of this phenotypic variation is difficult to study, in part because we do not know the detailed organization of the Y chromosome. To study Y chromosome organization in D. melanogaster, we develop an assembly strategy involving the in silico enrichment of heterochromatic long single-molecule reads and use these reads to create targeted de novo assemblies of heterochromatic sequences. We assigned contigs to the Y chromosome using Illumina reads to identify male-specific sequences. Our pipeline extends the D. melanogaster reference genome by 11.9 Mb, closes 43.8% of the gaps, and improves overall contiguity. The addition of 10.6 MB of Y-linked sequence permitted us to study the organization of repeats and genes along the Y chromosome. We detected a high rate of duplication to the pericentric regions of the Y chromosome from other regions in the genome. Most of these duplicated genes exist in multiple copies. We detail the evolutionary history of one sex-linked gene family, crystal-Stellate. While the Y chromosome does not undergo crossing over, we observed high gene conversion rates within and between members of the crystal-Stellate gene family, Su(Ste), and PCKR, compared to genome-wide estimates. Our results suggest that gene conversion and gene duplication play an important role in the evolution of Y-linked genes.

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Figure 1 Overview of the heterochromatin-enriched assembly approach. (A) We obtain a set of heterochromatin-enriched PacBio reads by mapping reads to the R6 assembly and retaining reads that map to known pericentric heterochromatin, Y chromosome contigs, or are unmapped (orange lines). (B) We generate separate de novo PacBio assemblies for all reads (orange and blue lines) and for heterochromatin-enriched reads (orange lines) with Canu and Falcon. (C) We merge assemblies sequentially using quickmerge to create the final assembly (Table S1). All assemblies were manually inspected and adjusted (see Materials and Methods). (D) We polished the final de novo assembly with one round of quiver (using raw PacBio reads) and 10 iterations of Pilon (using male Illumina reads). (E) We assign contigs in the final assembly to the X, Y, or autosomes using relative mapping of female-to-male Illumina reads (see Materials and Methods). (F) Finally, we join contigs into super scaffolds using exon orientation information from known gene structures.
Figure 1 Overview of the heterochromatin-enriched assembly approach. (A) We obtain a set of heterochromatin-enriched PacBio reads by mapping reads to the R6 assembly and retaining reads that map to known pericentric heterochromatin, Y chromosome contigs, or are unmapped (orange lines). (B) We generate separate de novo PacBio assemblies for all reads (orange and blue lines) and for heterochromatin-enriched reads (orange lines) with Canu and Falcon. (C) We merge assemblies sequentially using quickmerge to create the final assembly (Table S1). All assemblies were manually inspected and adjusted (see Materials and Methods). (D) We polished the final de novo assembly with one round of quiver (using raw PacBio reads) and 10 iterations of Pilon (using male Illumina reads). (E) We assign contigs in the final assembly to the X, Y, or autosomes using relative mapping of female-to-male Illumina reads (see Materials and Methods). (F) Finally, we join contigs into super scaffolds using exon orientation information from known gene structures.CC BY · PubMed Central
Figure 2 Schematic of Y chromosome organization. (A) The Y chromosome is organized into 25 cytological bands. The position of the Y-linked genes is shown based on deletion mapping (Carvalho et al. 2000, 2001; Vibranovski et al. 2008). The major scaffolds (orange bars) and contigs (dark red bars) that span each Y-linked gene, from left to right, are as follows: Y_scaffold6, Y_scaffold7, Y_scaffold4, Y_Contig10, Y_Contig2, Y_scaffold5, and Y_scaffold3. Note that scaffolds contain gaps. (B) The approximate cytological location of large blocks of simple tandem repeats (Bonaccorsi and Lohe 1991) agrees with the organization of our scaffolds and contigs: blue bars indicate that a block of satellite appears in that contig/scaffold, and black bars indicate that a block of repeats is missing from that contig/scaffold. Note that missing repeats may fall entirely in the gaps in our scaffolds, and potential cross-hybridization between AAGAG and AAGAGAG might explain the three discrepancies between our assembly and the cytological map.
Figure 2 Schematic of Y chromosome organization. (A) The Y chromosome is organized into 25 cytological bands. The position of the Y-linked genes is shown based on deletion mapping (Carvalho et al. 2000, 2001; Vibranovski et al. 2008). The major scaffolds (orange bars) and contigs (dark red bars) that span each Y-linked gene, from left to right, are as follows: Y_scaffold6, Y_scaffold7, Y_scaffold4, Y_Contig10, Y_Contig2, Y_scaffold5, and Y_scaffold3. Note that scaffolds contain gaps. (B) The approximate cytological location of large blocks of simple tandem repeats (Bonaccorsi and Lohe 1991) agrees with the organization of our scaffolds and contigs: blue bars indicate that a block of satellite appears in that contig/scaffold, and black bars indicate that a block of repeats is missing from that contig/scaffold. Note that missing repeats may fall entirely in the gaps in our scaffolds, and potential cross-hybridization between AAGAG and AAGAGAG might explain the three discrepancies between our assembly and the cytological map.CC BY · PubMed Central
Figure 3 Repeat composition on the Y chromosome compared to the rest of the genome. (A) The major repeat class composition on Y-linked contigs and all other contigs in our assembly (from the X and autosomes). (B) A comparison of complex repeats and transposable elements between autosomes, X, Y, and fourth chromosomes. We indicate the presence/absence (Y/N, respectively) of repeat classes for which cytological and/or Southern hybridization data exists in the literature. I elements have conflicting reports of Y-linkage in the literature. References: (1) Carmena and Gonzalez (1995); (2) Pimpinelli et al. (1995); (3) Junakovic et al. (1998); (4) Ritossa and Spiegelman (1965); (5) Agudo et al. (1999); (6) Balakireva et al. (1992); (7) Abad et al. (1992).
Figure 3 Repeat composition on the Y chromosome compared to the rest of the genome. (A) The major repeat class composition on Y-linked contigs and all other contigs in our assembly (from the X and autosomes). (B) A comparison of complex repeats and transposable elements between autosomes, X, Y, and fourth chromosomes. We indicate the presence/absence (Y/N, respectively) of repeat classes for which cytological and/or Southern hybridization data exists in the literature. I elements have conflicting reports of Y-linkage in the literature. References: (1) Carmena and Gonzalez (1995); (2) Pimpinelli et al. (1995); (3) Junakovic et al. (1998); (4) Ritossa and Spiegelman (1965); (5) Agudo et al. (1999); (6) Balakireva et al. (1992); (7) Abad et al. (1992).CC BY · PubMed Central
Figure 4 Evolution of the Cry-Ste family. (A) The evolutionary history of Cry-Ste family in D. melanogaster [modified from Usakin et al. (2005)]. (B) A Bayesian phylogenetic tree constructed with 606 full-length copies of genes in the Cry-Ste family including Ssl (parent gene) as the outgroup. Tip colors represent the location of genes in our assembly. Posterior node confidence is shown for a subset of the primary nodes separating repeat types. SCLR is a nonfunctional variant of Ste. (C) The alignment of representative repeats for heterochromatic Ste (hetSte), euchromatic Ste (euSte), PCKR, three main variants of Su(Ste), and two chimeric genes are shown (also indicated with red * in tree). Vertical colored lines indicate where base changes (red = A; yellow = G; green = T; blue = C; gray = missing) occur and dashes indicate indels.
Figure 4 Evolution of the Cry-Ste family. (A) The evolutionary history of Cry-Ste family in D. melanogaster [modified from Usakin et al. (2005)]. (B) A Bayesian phylogenetic tree constructed with 606 full-length copies of genes in the Cry-Ste family including Ssl (parent gene) as the outgroup. Tip colors represent the location of genes in our assembly. Posterior node confidence is shown for a subset of the primary nodes separating repeat types. SCLR is a nonfunctional variant of Ste. (C) The alignment of representative repeats for heterochromatic Ste (hetSte), euchromatic Ste (euSte), PCKR, three main variants of Su(Ste), and two chimeric genes are shown (also indicated with red * in tree). Vertical colored lines indicate where base changes (red = A; yellow = G; green = T; blue = C; gray = missing) occur and dashes indicate indels.CC BY · PubMed Central

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Cites

Research works printed but not linked: 134

  1. Abad, 2004, Genomic and cytological analysis of the Y chromosome of Drosophila melanogaster: telomere-derived sequences at internal regions., Chromosoma, 113, 295, 10.1007/s00412-004-0318-0 · DOI
  2. Agudo, 1999, Centromeres from telomeres? The centromeric region of the Y chromosome of Drosophila melanogaster contains a tandem array of telomeric HeT-A- and TART-related sequences., Nucleic Acids Res., 27, 3318, 10.1093/nar/27.16.3318 · DOI
  3. Altschul, 1990, Basic local alignment search tool., J. Mol. Biol., 215, 403, 10.1016/S0022-2836(05)80360-2 · DOI · Paper page
  4. Backström, 2005, Gene conversion drives the evolution of HINTW, an ampliconic gene on the female-specific avian W chromosome., Mol. Biol. Evol., 22, 1992, 10.1093/molbev/msi198 · DOI
  5. Bailly-Bechet, 2014, “One code to find them all”: a perl tool to conveniently parse RepeatMasker output files., Mob. DNA, 5, 13, 10.1186/1759-8753-5-13 · DOI
  6. Balakireva, 1992, Structural organization and diversification of Y-linked sequences comprising Su(Ste) genes in Drosophila melanogaster., Nucleic Acids Res., 20, 3731, 10.1093/nar/20.14.3731 · DOI
  7. Bayes, 2009, Altered heterochromatin binding by a hybrid sterility protein in Drosophila sibling species., Science, 326, 1538, 10.1126/science.1181756 · DOI
  8. Berlin, 2015, Assembling large genomes with single-molecule sequencing and locality-sensitive hashing., Nat. Biotechnol., 33, 623, 10.1038/nbt.3238 · DOI
  9. Bhutkar, 2007, Inferring genome-scale rearrangement phylogeny and ancestral gene order: a Drosophila case study., Genome Biol., 8, R236, 10.1186/gb-2007-8-11-r236 · DOI
  10. Bonaccorsi, 1991, Fine mapping of satellite DNA sequences along the Y chromosome of Drosophila melanogaster: relationships between satellite sequences and fertility factors., Genetics, 129, 177, 10.1093/genetics/129.1.177 · DOI
  11. Bozzetti, 1995, The Ste locus, a component of the parasitic cry-Ste system of Drosophila melanogaster, encodes a protein that forms crystals in primary spermatocytes and mimics properties of the beta subunit of casein kinase 2., Proc. Natl. Acad. Sci. USA, 92, 6067, 10.1073/pnas.92.13.6067 · DOI
  12. Branton, 2008, The potential and challenges of nanopore sequencing., Nat. Biotechnol., 26, 1146, 10.1038/nbt.1495 · DOI
  13. Brown, 2014, The chromatin landscape of Drosophila: comparisons between species, sexes, and chromosomes., Genome Res., 24, 1125, 10.1101/gr.172155.114 · DOI
  14. Bucheton, 1976, Non-mendelian female sterility in Drosophila melanogaster: quantitative variations in the efficiency of inducer and reactive strains., Heredity (Edinb), 36, 305, 10.1038/hdy.1976.38 · DOI
  15. Carlson, 1977, Cloning and characterization of a complex satellite DNA from Drosophila melanogaster., Cell, 11, 371, 10.1016/0092-8674(77)90054-X · DOI
  16. Carmena, 1995, Transposable elements map in a conserved pattern of distribution extending from beta-heterochromatin to centromeres in Drosophila melanogaster., Chromosoma, 103, 676, 10.1007/BF00344228 · DOI
  17. Carvalho, 2000, Y chromosomal fertility factors kl-2 and kl-3 of Drosophila melanogaster encode dynein heavy chain polypeptides., Proc. Natl. Acad. Sci. USA, 97, 13239, 10.1073/pnas.230438397 · DOI
  18. Carvalho, 2001, Identification of five new genes on the Y chromosome of Drosophila melanogaster., Proc. Natl. Acad. Sci. USA, 98, 13225, 10.1073/pnas.231484998 · DOI
  19. Carvalho, 2003, Y chromosome and other heterochromatic sequences of the Drosophila melanogaster genome: how far can we go?, Genetica, 117, 227, 10.1023/A:1022900313650 · DOI
  20. Carvalho, 2015, Birth of a new gene on the Y chromosome of Drosophila melanogaster., Proc. Natl. Acad. Sci. USA, 112, 12450, 10.1073/pnas.1516543112 · DOI
  21. Carvalho, 2016, Improved assembly of noisy long reads by k-mer validation., Genome Res., 26, 1710, 10.1101/gr.209247.116 · DOI
  22. Cattani, 2012, Incompatibility between X chromosome factor and pericentric heterochromatic region causes lethality in hybrids between Drosophila melanogaster and its sibling species., Genetics, 191, 549, 10.1534/genetics.112.139683 · DOI
  23. Chaisson, 2012, Mapping single molecule sequencing reads using basic local alignment with successive refinement (BLASR): application and theory., BMC Bioinformatics, 13, 238, 10.1186/1471-2105-13-238 · DOI
  24. Chaisson, 2015, Resolving the complexity of the human genome using single-molecule sequencing., Nature, 517, 608, 10.1038/nature13907 · DOI
  25. Chakraborty, 2016, Contiguous and accurate de novo assembly of metazoan genomes with modest long read coverage., Nucleic Acids Res., 44, e147
  26. Chakraborty, 2018, Hidden genetic variation shapes the structure of functional elements in Drosophila., Nat. Genet., 50, 20, 10.1038/s41588-017-0010-y · DOI
  27. Chang, 2017, Genomic changes following the reversal of a Y chromosome to an autosome in Drosophila pseudoobscura., Evolution, 71, 1285, 10.1111/evo.13229 · DOI
  28. Charlesworth, 2003, The organization and evolution of the human Y chromosome., Genome Biol., 4, 226, 10.1186/gb-2003-4-9-226 · DOI
  29. Charlesworth, 2000, The degeneration of Y chromosomes., Philos. Trans. R. Soc. Lond. B Biol. Sci., 355, 1563, 10.1098/rstb.2000.0717 · DOI
  30. Charlesworth, 1986, The evolution of restricted recombination and the accumulation of repeated DNA sequences., Genetics, 112, 947, 10.1093/genetics/112.4.947 · DOI
  31. Chin, 2013, Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data., Nat. Methods, 10, 563, 10.1038/nmeth.2474 · DOI · Paper page
  32. Chin, 2016, Phased diploid genome assembly with single-molecule real-time sequencing., Nat. Methods, 13, 1050, 10.1038/nmeth.4035 · DOI
  33. Chippindale, 2001, Y chromosome polymorphism is a strong determinant of male fitness in Drosophila melanogaster., Proc. Natl. Acad. Sci. USA, 98, 5677, 10.1073/pnas.101456898 · DOI
  34. Clifton, 2017, Rapid functional and sequence differentiation of a tandemly repeated species-specific multigene family in Drosophila., Mol. Biol. Evol., 34, 51, 10.1093/molbev/msw212 · DOI
  35. Comeron, 2012, The many landscapes of recombination in Drosophila melanogaster., PLoS Genet., 8, e1002905, 10.1371/journal.pgen.1002905 · DOI
  36. Connallon, 2010, Gene duplication, gene conversion and the evolution of the Y chromosome., Genetics, 186, 277, 10.1534/genetics.110.116756 · DOI
  37. Csink, 1996, Genetic modification of heterochromatic association and nuclear organization in Drosophila., Nature, 381, 529, 10.1038/381529a0 · DOI
  38. Danilevskaya, 1991, He-T family DNA sequences in the Y chromosome of Drosophila melanogaster share homology with the X-linked stellate genes., Chromosoma, 100, 118, 10.1007/BF00418245 · DOI
  39. Dernburg, 1996, Direct evidence of a role for heterochromatin in meiotic chromosome segregation., Cell, 86, 135, 10.1016/S0092-8674(00)80084-7 · DOI
  40. Dimitri, 1989, Position effect variegation in Drosophila melanogaster: relationship between suppression effect and the amount of Y chromosome., Genetics, 122, 793, 10.1093/genetics/122.4.793 · DOI
  41. Eid, 2009, Real-time DNA sequencing from single polymerase molecules., Science, 323, 133, 10.1126/science.1162986 · DOI · Paper page
  42. Elgin, 1996, Heterochromatin and gene regulation in Drosophila., Curr. Opin. Genet. Dev., 6, 193, 10.1016/S0959-437X(96)80050-5 · DOI
  43. Ferree, 2009, Species-specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila., PLoS Biol., 7, e1000234, 10.1371/journal.pbio.1000234 · DOI
  44. Francisco, 2014, How do y-chromosomes modulate genome-wide epigenetic states: genome folding, chromatin sinks, and gene expression., J Genomics, 2, 94, 10.7150/jgen.8043 · DOI
  45. Garavís, 2015, The structure of an endogenous Drosophila centromere reveals the prevalence of tandemly repeated sequences able to form i-motifs., Sci. Rep., 5, 13307, 10.1038/srep13307 · DOI
  46. Gatti, 1992, Functional elements in Drosophila melanogaster heterochromatin., Annu. Rev. Genet., 26, 239, 10.1146/annurev.ge.26.120192.001323 · DOI
  47. Hall, 2013, Six novel Y chromosome genes in Anopheles mosquitoes discovered by independently sequencing males and females., BMC Genomics, 14, 273, 10.1186/1471-2164-14-273 · DOI
  48. Han, 2012, Inferring the history of interchromosomal gene transposition in Drosophila using n-dimensional parsimony., Genetics, 190, 813, 10.1534/genetics.111.135947 · DOI
  49. Henikoff, 1996, Dosage-dependent modification of position-effect variegation in Drosophila., BioEssays, 18, 401, 10.1002/bies.950180510 · DOI
  50. Hoskins, 2002, Heterochromatic sequences in a Drosophila whole-genome shotgun assembly., RESEARCH0085
  51. Hoskins, 2015, The Release 6 reference sequence of the Drosophila melanogaster genome., Genome Res., 25, 445, 10.1101/gr.185579.114 · DOI
  52. Huddleston, 2014, Reconstructing complex regions of genomes using long-read sequencing technology., Genome Res., 24, 688, 10.1101/gr.168450.113 · DOI
  53. Hudson, 1987, Estimating the recombination parameter of a finite population model without selection., Genet. Res., 50, 245, 10.1017/S0016672300023776 · DOI
  54. Hughes, 2015, The biology and evolution of mammalian Y chromosomes., Annu. Rev. Genet., 49, 507, 10.1146/annurev-genet-112414-055311 · DOI
  55. Hughes, 2012, Strict evolutionary conservation followed rapid gene loss on human and rhesus Y chromosomes., Nature, 483, 82, 10.1038/nature10843 · DOI
  56. Hurst, 1996, Further evidence consistent with Stellate’s involvement in meiotic drive., Genetics, 142, 641, 10.1093/genetics/142.2.641 · DOI
  57. Jagannathan, 2017, Comparative analysis of satellite DNA in the Drosophila melanogaster species complex., G3 (Bethesda), 7, 693, 10.1534/g3.116.035352 · DOI
  58. Jain, 2018, Linear assembly of a human centromere on the Y chromosome., Nat. Biotechnol, 36, 321, 10.1038/nbt.4109 · DOI
  59. Junakovic, 1998, Accumulation of transposable elements in the heterochromatin and on the Y chromosome of Drosophila simulans and Drosophila melanogaster., J. Mol. Evol., 46, 661, 10.1007/PL00006346 · DOI
  60. Karpen, 1994, Position-effect variegation and the new biology of heterochromatin., Curr. Opin. Genet. Dev., 4, 281, 10.1016/S0959-437X(05)80055-3 · DOI
  61. Kearse, 2012, Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data., Bioinformatics, 28, 1647, 10.1093/bioinformatics/bts199 · DOI
  62. Keightley, 2014, Estimation of the spontaneous mutation rate per nucleotide site in a Drosophila melanogaster full-sib family., Genetics, 196, 313, 10.1534/genetics.113.158758 · DOI
  63. Kennison, 1981, The genetic and cytological organization of the Y chromosome of Drosophila melanogaster., Genetics, 98, 529, 10.1093/genetics/98.3.529 · DOI
  64. Kent, 2002, BLAT–the BLAST-like alignment tool., Genome Res., 12, 656, 10.1101/gr.229202 · DOI · Paper page
  65. Khost, 2017, Single-molecule sequencing resolves the detailed structure of complex satellite DNA loci in Drosophila melanogaster., Genome Res., 27, 709, 10.1101/gr.213512.116 · DOI
  66. Kim, 2015, HISAT: a fast spliced aligner with low memory requirements., Nat. Methods, 12, 357, 10.1038/nmeth.3317 · DOI · Paper page
  67. Kim, 2014, Long-read, whole-genome shotgun sequence data for five model organisms., Sci. Data, 1, 140045, 10.1038/sdata.2014.45 · DOI
  68. Koerich, 2008, Low conservation of gene content in the Drosophila Y chromosome., Nature, 456, 949, 10.1038/nature07463 · DOI
  69. Kogan, 2000, Molecular evolution of two paralogous tandemly repeated heterochromatic gene clusters linked to the X and Y chromosomes of Drosophila melanogaster., Mol. Biol. Evol., 17, 697, 10.1093/oxfordjournals.molbev.a026348 · DOI
  70. Kogan, 2012, Expansion and evolution of the X-linked testis specific multigene families in the melanogaster species subgroup., PLoS One, 7, e37738, 10.1371/journal.pone.0037738 · DOI
  71. Kopp, 2006, Interspecific divergence, intrachromosomal recombination, and phylogenetic utility of Y-chromosomal genes in Drosophila., Mol. Phylogenet. Evol., 38, 731, 10.1016/j.ympev.2005.10.006 · DOI
  72. Koren, 2017, Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation., Genome Res., 27, 722, 10.1101/gr.215087.116 · DOI
  73. Kost, 2015, Multimerization of Drosophila sperm protein Mst77F causes a unique condensed chromatin structure., Nucleic Acids Res., 43, 3033, 10.1093/nar/gkv015 · DOI
  74. Krsticevic, 2010, Functional copies of the Mst77F gene on the Y chromosome of Drosophila melanogaster., Genetics, 184, 295, 10.1534/genetics.109.107516 · DOI
  75. Krsticevic, 2015, Long-read single molecule sequencing to resolve tandem gene copies: the Mst77Y region on the Drosophila melanogaster Y chromosome., G3 (Bethesda), 5, 1145, 10.1534/g3.115.017277 · DOI
  76. Kurek, 2000, Molecular aspects of intron evolution in dynein encoding mega-genes on the heterochromatic Y chromosome of Drosophila sp., Genetica, 109, 113, 10.1023/A:1026552604229 · DOI
  77. Kurtz, 2004, Versatile and open software for comparing large genomes., Genome Biol., 5, R12, 10.1186/gb-2004-5-2-r12 · DOI · Paper page
  78. Kutch, 2017, A test for Y-linked additive and epistatic effects on surviving bacterial infections in Drosophila melanogaster., J. Evol. Biol., 30, 1400, 10.1111/jeb.13118 · DOI
  79. Larracuente, 2013, Surprising differences in the variability of Y chromosomes in African and cosmopolitan populations of Drosophila melanogaster., Genetics, 193, 201, 10.1534/genetics.112.146167 · DOI
  80. Lemos, 2008, Polymorphic Y chromosomes harbor cryptic variation with manifold functional consequences., Science, 319, 91, 10.1126/science.1148861 · DOI
  81. Lemos, 2010, Epigenetic effects of polymorphic Y chromosomes modulate chromatin components, immune response, and sexual conflict., Proc. Natl. Acad. Sci. USA, 107, 15826, 10.1073/pnas.1010383107 · DOI
  82. Li, 2016, Minimap and miniasm: fast mapping and de novo assembly for noisy long sequences., Bioinformatics, 32, 2103, 10.1093/bioinformatics/btw152 · DOI
  83. Li, 2010, Fast and accurate long-read alignment with Burrows-Wheeler transform., Bioinformatics, 26, 589, 10.1093/bioinformatics/btp698 · DOI · Paper page
  84. Li, 2009, The sequence alignment/map format and SAMtools., Bioinformatics, 25, 2078, 10.1093/bioinformatics/btp352 · DOI · Paper page
  85. Livak, 1984, Organization and mapping of a sequence on the Drosophila melanogaster X and Y chromosomes that is transcribed during spermatogenesis., Genetics, 107, 611, 10.1093/genetics/107.4.611 · DOI
  86. Lohe, 1987, Adjacent satellite DNA segments in Drosophila structure of junctions., J. Mol. Biol., 194, 171, 10.1016/0022-2836(87)90366-4 · DOI
  87. Lohe, 1987, Identical satellite DNA sequences in sibling species of Drosophila., J. Mol. Biol., 194, 161, 10.1016/0022-2836(87)90365-2 · DOI
  88. Lohe, 1993, Mapping simple repeated DNA sequences in heterochromatin of Drosophila melanogaster., Genetics, 134, 1149, 10.1093/genetics/134.4.1149 · DOI
  89. Lyckegaard, 1989, Ribosomal DNA and Stellate gene copy number variation on the Y chromosome of Drosophila melanogaster., Proc. Natl. Acad. Sci. USA, 86, 1944, 10.1073/pnas.86.6.1944 · DOI
  90. Mahajan, 2017, Convergent evolution of Y chromosome gene content in flies., Nat. Commun., 8, 785, 10.1038/s41467-017-00653-x · DOI
  91. Mahajan, 2018, De novo assembly of a young Drosophila Y chromosome using single-molecule sequencing and chromatin conformation capture., e2006348, 10.1371/journal.pbio.2006348 · DOI
  92. Malone, 2015, The cellular basis of hybrid dysgenesis and Stellate regulation in Drosophila., Curr. Opin. Genet. Dev., 34, 88, 10.1016/j.gde.2015.09.003 · DOI
  93. McKee, 1996, Structure of the Y chromosomal Su(Ste) locus in Drosophila melanogaster and evidence for localized recombination among repeats., Genetics, 142, 149, 10.1093/genetics/142.1.149 · DOI
  94. McKee, 2000, On the roles of heterochromatin and euchromatin in meiosis in drosophila: mapping chromosomal pairing sites and testing candidate mutations for effects on X-Y nondisjunction and meiotic drive in male meiosis., Genetica, 109, 77, 10.1023/A:1026536200594 · DOI
  95. Méndez-Lago, 2009, Novel sequencing strategy for repetitive DNA in a Drosophila BAC clone reveals that the centromeric region of the Y chromosome evolved from a telomere., Nucleic Acids Res., 37, 2264, 10.1093/nar/gkp085 · DOI
  96. Mendez-Lago, 2011, A large palindrome with interchromosomal gene duplications in the pericentromeric region of the D. melanogaster Y chromosome., Mol. Biol. Evol., 28, 1967, 10.1093/molbev/msr034 · DOI
  97. Mikheenko, 2018, Versatile genome assembly evaluation with QUAST-LG., Bioinformatics, 34, i142, 10.1093/bioinformatics/bty266 · DOI
  98. Miller, 2012, A whole-chromosome analysis of meiotic recombination in Drosophila melanogaster., G3 (Bethesda), 2, 249, 10.1534/g3.111.001396 · DOI
  99. Miller, 2016, Whole-genome analysis of individual meiotic events in Drosophila melanogaster reveals that noncrossover gene conversions are insensitive to interference and the centromere effect., Genetics, 203, 159, 10.1534/genetics.115.186486 · DOI
  100. Morgan, 2017, Sequence and structural diversity of mouse Y chromosomes., Mol. Biol. Evol., 34, 3186, 10.1093/molbev/msx250 · DOI
  101. Nishida, 2007, Gene silencing mechanisms mediated by Aubergine piRNA complexes in Drosophila male gonad., RNA, 13, 1911, 10.1261/rna.744307 · DOI
  102. Nurminsky, 1994, Structure, molecular evolution and maintenance of copy number of extended repeated structures in the X-heterochromatin of Drosophila melanogaster., Chromosoma, 103, 277, 10.1007/BF00352252 · DOI
  103. Ohta, 1984, Some models of gene conversion for treating the evolution of multigene families., Genetics, 106, 517, 10.1093/genetics/106.3.517 · DOI
  104. Paradis, 2004, APE: analyses of phylogenetics and evolution in R language., Bioinformatics, 20, 289, 10.1093/bioinformatics/btg412 · DOI · Paper page
  105. Paredes, 2011, Ribosomal DNA deletions modulate genome-wide gene expression: “rDNA-sensitive” genes and natural variation., PLoS Genet., 7, e1001376, 10.1371/journal.pgen.1001376 · DOI
  106. Pertea, 2015, StringTie enables improved reconstruction of a transcriptome from RNA-seq reads., Nat. Biotechnol., 33, 290, 10.1038/nbt.3122 · DOI
  107. Pimpinelli, 1995, Transposable elements are stable structural components of Drosophila melanogaster heterochromatin., Proc. Natl. Acad. Sci. USA, 92, 3804, 10.1073/pnas.92.9.3804 · DOI
  108. Reijo, 1995, Diverse spermatogenic defects in humans caused by Y chromosome deletions encompassing a novel RNA-binding protein gene., Nat. Genet., 10, 383, 10.1038/ng0895-383 · DOI
  109. Repping, 2003, Polymorphism for a 1.6-Mb deletion of the human Y chromosome persists through balance between recurrent mutation and haploid selection., Nat. Genet., 35, 247, 10.1038/ng1250 · DOI
  110. Reugels, 2000, Mega-introns in the dynein gene DhDhc7(Y) on the heterochromatic Y chromosome give rise to the giant threads loops in primary spermatocytes of Drosophila hydei., Genetics, 154, 759, 10.1093/genetics/154.2.759 · DOI
  111. Ritossa, 1965, Localization of DNA complementary to ribosomal Rna in the nucleolus organizer region of Drosophila melanogaster., Proc. Natl. Acad. Sci. USA, 53, 737, 10.1073/pnas.53.4.737 · DOI
  112. Rohmer, 2004, Heat induced male sterility in Drosophila melanogaster: adaptive genetic variations among geographic populations and role of the Y chromosome., J. Exp. Biol., 207, 2735, 10.1242/jeb.01087 · DOI
  113. Rošić, 2014, Repetitive centromeric satellite RNA is essential for kinetochore formation and cell division., J. Cell Biol., 207, 335, 10.1083/jcb.201404097 · DOI
  114. Rozen, 2003, Abundant gene conversion between arms of palindromes in human and ape Y chromosomes., Nature, 423, 873, 10.1038/nature01723 · DOI
  115. Shevelyov, 1992, Copies of a Stellate gene variant are located in the X heterochromatin of Drosophila melanogaster and are probably expressed., Genetics, 132, 1033, 10.1093/genetics/132.4.1033 · DOI
  116. Soh, 2014, Sequencing the mouse Y chromosome reveals convergent gene acquisition and amplification on both sex chromosomes., Cell, 159, 800, 10.1016/j.cell.2014.09.052 · DOI
  117. Thornton, 2003, Libsequence: a C++ class library for evolutionary genetic analysis., Bioinformatics, 19, 2325, 10.1093/bioinformatics/btg316 · DOI
  118. Tobler, 2017, High rate of translocation-based gene birth on the Drosophila Y chromosome., Proc. Natl. Acad. Sci. USA, 114, 11721, 10.1073/pnas.1706502114 · DOI
  119. Tomaszkiewicz, 2016, A time- and cost-effective strategy to sequence mammalian Y Chromosomes: an application to the de novo assembly of gorilla Y., Genome Res., 26, 530, 10.1101/gr.199448.115 · DOI
  120. Traverse, 1989, Studies of He-T DNA sequences in the pericentric regions of Drosophila chromosomes., Chromosoma, 97, 261, 10.1007/BF00371965 · DOI
  121. Treangen, 2011, Repetitive DNA and next-generation sequencing: computational challenges and solutions., Nat. Rev. Genet., 13, 36, 10.1038/nrg3117 · DOI · Paper page
  122. Tulin, 1997, Heterochromatic Stellate gene cluster in Drosophila melanogaster: structure and molecular evolution., Genetics, 146, 253, 10.1093/genetics/146.1.253 · DOI
  123. Usakin, 2005, An alien promoter capture as a primary step of the evolution of testes-expressed repeats in the Drosophila melanogaster genome., Mol. Biol. Evol., 22, 1555, 10.1093/molbev/msi147 · DOI
  124. Vibranovski, 2008, Two new Y-linked genes in Drosophila melanogaster., Genetics, 179, 2325, 10.1534/genetics.108.086819 · DOI
  125. Vogt, 1996, Human Y chromosome azoospermia factors (AZF) mapped to different subregions in Yq11., Hum. Mol. Genet., 5, 933, 10.1093/hmg/5.7.933 · DOI
  126. Wakimoto, 1998, Beyond the nucleosome: epigenetic aspects of position-effect variegation in Drosophila., Cell, 93, 321, 10.1016/S0092-8674(00)81159-9 · DOI
  127. Walker, 2014, Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement., PLoS One, 9, e112963, 10.1371/journal.pone.0112963 · DOI
  128. Wang, 2018, The Y chromosome modulates splicing and sex-biased intron retention rates in Drosophila., Genetics, 208, 1057, 10.1534/genetics.117.300637 · DOI
  129. Wang, 2014, A distinct type of heterochromatin at the telomeric region of the Drosophila melanogaster Y chromosome., PLoS One, 9, e86451, 10.1371/journal.pone.0086451 · DOI
  130. Wei, 2018, Variable rates of simple satellite gains across the Drosophila phylogeny., Mol. Biol. Evol., 35, 925, 10.1093/molbev/msy005 · DOI
  131. Zhao, 2014, CrossMap: a versatile tool for coordinate conversion between genome assemblies., Bioinformatics, 30, 1006, 10.1093/bioinformatics/btt730 · DOI
  132. Zhou, 2012, Y chromosome mediates ribosomal DNA silencing and modulates the chromatin state in Drosophila., Proc. Natl. Acad. Sci. USA, 109, 9941, 10.1073/pnas.1207367109 · DOI
  133. Zimin, 2017, Hybrid assembly of the large and highly repetitive genome of Aegilops tauschii, a progenitor of bread wheat, with the MaSuRCA mega-reads algorithm., Genome Res., 27, 787, 10.1101/gr.213405.116 · DOI
  134. Zurovcova, 1999, Lack of nucleotide polymorphism in the Y-linked sperm flagellar dynein gene Dhc-Yh3 of Drosophila melanogaster and D. simulans., Genetics, 153, 1709, 10.1093/genetics/153.4.1709 · DOI

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Metadata

Authors
Chang, C.-H., & Larracuente, A. M.
Affiliations
Department of Biology , University of Rochester, New York 14627
Venue
Genetics
Publisher
Oxford University Press (OUP)
Published
2018-11-12
Volume
211
Issue
1
Pages
333-348
ISSN
1943-2631
DOI
10.1534/genetics.118.301765
PMC
PMC6325706
Cited by
141
References
2
Language
en
Licence
academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)

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