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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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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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CoChat. (2026). Citation check: Heterochromatin-Enriched Assemblies Reveal the Sequence and Organization of the Drosophila melanogaster Y Chromosome. https://app.cochat.ai/papers/10.1534/genetics.118.301765
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Chang, C.-H., & Larracuente, A. M. (2019). Heterochromatin-Enriched Assemblies Reveal the Sequence and Organization of the Drosophila melanogaster Y Chromosome. Genetics. https://doi.org/10.1534/genetics.118.301765