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Identification and Characterization of Breakpoints and Mutations on Drosophila melanogaster Balancer Chromosomes

Miller, Danny E, Kahsai, Lily, Buddika, Kasun, Dixon, Michael J, Kim, Bernard Y, Calvi, Brian R, Sokol, Nicholas S, Hawley, R Scott, Cook, Kevin R·2020·G3 Genes|Genomes|Genetics
DOI 10.1534/g3.120.401559PMC PMC7642927
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Abstract

Balancers are rearranged chromosomes used in Drosophila melanogaster to maintain deleterious mutations in stable populations, preserve sets of linked genetic elements and construct complex experimental stocks. Here, we assess the phenotypes associated with breakpoint-induced mutations on commonly used third chromosome balancers and show remarkably few deleterious effects. We demonstrate that a breakpoint in p53 causes loss of radiation-induced apoptosis and a breakpoint in Fucosyltransferase A causes loss of fucosylation in nervous and intestinal tissue—the latter study providing new markers for intestinal cell identity and challenging previous conclusions about the regulation of fucosylation. We also describe thousands of potentially harmful mutations shared among X or third chromosome balancers, or unique to specific balancers, including an Ankyrin 2 mutation present on most TM3 balancers, and reiterate the risks of using balancers as experimental controls. We used long-read sequencing to confirm or refine the positions of two inversions with breakpoints lying in repetitive sequences and provide evidence that one of the inversions, In(2L)Cy, arose by ectopic recombination between foldback transposon insertions and the other, In(3R)C, cleanly separates subtelomeric and telomeric sequences and moves the subtelomeric sequences to an internal chromosome position. In addition, our characterization of In(3R)C shows that balancers may be polymorphic for terminal deletions. Finally, we present evidence that extremely distal mutations on balancers can add to the stability of stocks whose purpose is to maintain homologous chromosomes carrying mutations in distal genes. Overall, these studies add to our understanding of the structure, diversity and effectiveness of balancer chromosomes.

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Figure 1 The TM3 breakpoint at 94D disrupts p53 apoptosis activity. Irradiation-induced apoptosis is seen as TUNEL staining in stage 1–5 follicle cells counterstained with DAPI of control females (e.g., y1 w67c23 homozygotes shown here). TUNEL staining is absent in follicle cells of females carrying TM3 combined with chromosomal deletions removing the p53 gene (e.g., TM3/Df(3R)ED6103 shown here) and females carrying TM3 and loss-of-function p53 alleles (e.g., TM3/p535A-1-4 shown here). TUNEL-stained cells in p53 mutants are polar follicle cells, which undergo p53-independent, developmentally programmed cell death. See Table S5 for all genotypes tested.
Figure 1 The TM3 breakpoint at 94D disrupts p53 apoptosis activity. Irradiation-induced apoptosis is seen as TUNEL staining in stage 1–5 follicle cells counterstained with DAPI of control females (e.g., y1 w67c23 homozygotes shown here). TUNEL staining is absent in follicle cells of females carrying TM3 combined with chromosomal deletions removing the p53 gene (e.g., TM3/Df(3R)ED6103 shown here) and females carrying TM3 and loss-of-function p53 alleles (e.g., TM3/p535A-1-4 shown here). TUNEL-stained cells in p53 mutants are polar follicle cells, which undergo p53-independent, developmentally programmed cell death. See Table S5 for all genotypes tested.CC BY · PubMed Central
Figure 2 The TM3 breakpoint in FucTA is associated with loss of anti-HRP antibody staining in nervous tissue and intestinal epithelial cells. A. TM3/Sb1 flies were crossed to mutation- or deletion-bearing flies. Anti-HRP staining was not detected in adult brains when deletions of FucTA (Df(3L)BSC837 and Df(3L)Brd15) or a FucTA mutation (FucTAf03774) were combined with TM3, but it was seen in control crosses where a chromosome with no FucTA mutation (Sb1) was combined with the same deletions or mutation. Staining was seen with either TM3 or Sb1 combined with a Tollo deletion (Df(3L)BSC578) or mutations (Tollo1 and TolloMI11573). Anti-HRP staining shown in green; anti-BRP counterstaining shown in magenta to highlight neuropils. B. Crosses between mira-His2A.mCherry.HA; wgSp-1/CyO; TM3/TM6B females and males carrying the same deletions or mutations gave identical results for anti-HRP staining of intestinal epithelial cells where TM6B serves as the FucTA+ control (and only wgSp-1/+ progeny were scored). Anti-HRP staining shown in green; miranda-expressing progenitor and enteroendocrine cells shown in red; DAPI staining of nuclei shown in blue. C. The 71B breakpoint in TM3 lies within an alternative 5′ UTR of FucTA and ∼85 kb distal to Tollo. Df(3L)Brd15 deletes both genes while Df(3L)BSC837 disrupts only FucTA and Df(3L)BSC578 deletes only Tollo. FucTA-specific mutations and deletions failed to complement TM3 with respect to anti-HRP staining while Tollo-specific mutations and deletions complemented. A 412 transposon insertion in the 3′ UTR and a polymorphism leading to substitution of phenylalanine for leucine are present in Tollo in all TM3 chromosomes examined, but they may be neutral with respect to Tollo function.
Figure 2 The TM3 breakpoint in FucTA is associated with loss of anti-HRP antibody staining in nervous tissue and intestinal epithelial cells. A. TM3/Sb1 flies were crossed to mutation- or deletion-bearing flies. Anti-HRP staining was not detected in adult brains when deletions of FucTA (Df(3L)BSC837 and Df(3L)Brd15) or a FucTA mutation (FucTAf03774) were combined with TM3, but it was seen in control crosses where a chromosome with no FucTA mutation (Sb1) was combined with the same deletions or mutation. Staining was seen with either TM3 or Sb1 combined with a Tollo deletion (Df(3L)BSC578) or mutations (Tollo1 and TolloMI11573). Anti-HRP staining shown in green; anti-BRP counterstaining shown in magenta to highlight neuropils. B. Crosses between mira-His2A.mCherry.HA; wgSp-1/CyO; TM3/TM6B females and males carrying the same deletions or mutations gave identical results for anti-HRP staining of intestinal epithelial cells where TM6B serves as the FucTA+ control (and only wgSp-1/+ progeny were scored). Anti-HRP staining shown in green; miranda-expressing progenitor and enteroendocrine cells shown in red; DAPI staining of nuclei shown in blue. C. The 71B breakpoint in TM3 lies within an alternative 5′ UTR of FucTA and ∼85 kb distal to Tollo. Df(3L)Brd15 deletes both genes while Df(3L)BSC837 disrupts only FucTA and Df(3L)BSC578 deletes only Tollo. FucTA-specific mutations and deletions failed to complement TM3 with respect to anti-HRP staining while Tollo-specific mutations and deletions complemented. A 412 transposon insertion in the 3′ UTR and a polymorphism leading to substitution of phenylalanine for leucine are present in Tollo in all TM3 chromosomes examined, but they may be neutral with respect to Tollo function.CC BY · PubMed Central
Figure 3 The structure of In(3R)C. A. The wild-type and inverted arrangement of the In(3R)C inversion breakpoints with neighboring genes labeled. The exact position of the distal (C|D) breakpoint was not previously known, but was suspected to lie within subtelomeric heterochromatin. B. Assembly of long sequencing reads revealed the molecular structure of the proximal (A|C) junction, with nearly 12 kb of sequence between the distal end of the reference 3R assembly at 32,079,331 and the distal break. This region contained three transposable elements that were, in all likelihood, originally positioned immediately proximal to the telomeric transposon repeats. C. The distal In(3R)C breakpoint fell immediately proximal to telomeric repeats. Our assembly of this region extended ∼103 kb distally from the distal (B|D) junction and contained the HeT-A, TAHRE, and TART-A elements expected for a telomeric region as well as repeated fragments of HeT-A and TART-A at the distal end of the assembly. The positions and number of elements shown distal to the second TART-A element are estimates. All elements, including the incomplete HeT-A and TAHRE fragments, are oriented with their 3′ ends toward the centromere. D. Having established the structure of In(3R)C, we interpret the ∼17 kb deletion of sequences immediately distal to 3R:20,308,209–20,308,213 observed by Ghavi-Helm et al. (2019) as evidence of a 3R terminal deletion specific to the TM3 chromosome they characterized.
Figure 3 The structure of In(3R)C. A. The wild-type and inverted arrangement of the In(3R)C inversion breakpoints with neighboring genes labeled. The exact position of the distal (C|D) breakpoint was not previously known, but was suspected to lie within subtelomeric heterochromatin. B. Assembly of long sequencing reads revealed the molecular structure of the proximal (A|C) junction, with nearly 12 kb of sequence between the distal end of the reference 3R assembly at 32,079,331 and the distal break. This region contained three transposable elements that were, in all likelihood, originally positioned immediately proximal to the telomeric transposon repeats. C. The distal In(3R)C breakpoint fell immediately proximal to telomeric repeats. Our assembly of this region extended ∼103 kb distally from the distal (B|D) junction and contained the HeT-A, TAHRE, and TART-A elements expected for a telomeric region as well as repeated fragments of HeT-A and TART-A at the distal end of the assembly. The positions and number of elements shown distal to the second TART-A element are estimates. All elements, including the incomplete HeT-A and TAHRE fragments, are oriented with their 3′ ends toward the centromere. D. Having established the structure of In(3R)C, we interpret the ∼17 kb deletion of sequences immediately distal to 3R:20,308,209–20,308,213 observed by Ghavi-Helm et al. (2019) as evidence of a 3R terminal deletion specific to the TM3 chromosome they characterized.CC BY · PubMed Central
Figure 4 In(2L)Cy was likely created by ectopic recombination between two foldback transposable elements. A. The distal In(2L)Cy breakpoint (A|B) lies in the 3′ UTR of GlyP and proximal breakpoint (C|D) lies between CG5776 and spict. Reference genome coordinates are shown. B. The general structure of the breakpoint-associated FB insertions. Both insertions have end sequences, spacer sequences and blocks of repeats in mirrored orientations flanking a middle region. Each block contains a single copy of five distinct short repeats, blocks are repeated tandemly a variable number of times, and each block terminates with a CTC motif. An additional 23 bp may be appended to a consensus end sequence. C. The distal (A|C) end of In(2L)Cy includes 2,418 bp of FB sequences, which contain an alternative end sequence and clusters of two and seven repeat blocks, but lack one spacer sequence. Consistent with a recombinant origin, the FB sequences are flanked by a 9 bp tandem site duplication from FB transposition into GlyP (shown as “A”) and another from FB transposition into the CG5776–spict region (“B”). D. The proximal (B|D) end includes 2,563 bp of FB sequences including two spacer sequences and clusters of two and eight repeat blocks. These FB sequences are flanked by the 9 bp duplicated sequences from FB transposition into GlyP (“A”) and the CG5776–spict region (“B”) expected for inversion via ectopic recombination. E. In(2L)Cy arose by recombination between progenitor FB insertions. The high similarity of the FB sequences at the In(2L)Cy ends and the presence of an alternative end sequence at the distal In(2L)Cy end suggests that an FB element within GlyP transposed to the CG5776–spict region and subsequently recombined with an FB element at the donor site.
Figure 4 In(2L)Cy was likely created by ectopic recombination between two foldback transposable elements. A. The distal In(2L)Cy breakpoint (A|B) lies in the 3′ UTR of GlyP and proximal breakpoint (C|D) lies between CG5776 and spict. Reference genome coordinates are shown. B. The general structure of the breakpoint-associated FB insertions. Both insertions have end sequences, spacer sequences and blocks of repeats in mirrored orientations flanking a middle region. Each block contains a single copy of five distinct short repeats, blocks are repeated tandemly a variable number of times, and each block terminates with a CTC motif. An additional 23 bp may be appended to a consensus end sequence. C. The distal (A|C) end of In(2L)Cy includes 2,418 bp of FB sequences, which contain an alternative end sequence and clusters of two and seven repeat blocks, but lack one spacer sequence. Consistent with a recombinant origin, the FB sequences are flanked by a 9 bp tandem site duplication from FB transposition into GlyP (shown as “A”) and another from FB transposition into the CG5776–spict region (“B”). D. The proximal (B|D) end includes 2,563 bp of FB sequences including two spacer sequences and clusters of two and eight repeat blocks. These FB sequences are flanked by the 9 bp duplicated sequences from FB transposition into GlyP (“A”) and the CG5776–spict region (“B”) expected for inversion via ectopic recombination. E. In(2L)Cy arose by recombination between progenitor FB insertions. The high similarity of the FB sequences at the In(2L)Cy ends and the presence of an alternative end sequence at the distal In(2L)Cy end suggests that an FB element within GlyP transposed to the CG5776–spict region and subsequently recombined with an FB element at the donor site.CC BY · PubMed Central
Figure 5 A deleterious mutation can prevent stock breakdown when a crossover occurs distal to the distalmost balancer breakpoint. Panel A shows that a meiotic crossover distal to the CyO breakpoint in region 22D can result in the formation of mutation-free recombinant chromosomes, which will have a selective advantage in a stock population. In contrast, panel B shows that the addition of a recessive lethal or sterile mutation (shown here as a female-sterile mutation) to the balancer leads to elimination of the same recombinant chromosomes through routine population dynamics.
Figure 5 A deleterious mutation can prevent stock breakdown when a crossover occurs distal to the distalmost balancer breakpoint. Panel A shows that a meiotic crossover distal to the CyO breakpoint in region 22D can result in the formation of mutation-free recombinant chromosomes, which will have a selective advantage in a stock population. In contrast, panel B shows that the addition of a recessive lethal or sterile mutation (shown here as a female-sterile mutation) to the balancer leads to elimination of the same recombinant chromosomes through routine population dynamics.CC BY · PubMed Central

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Research works printed but not linked: 83

  1. Anderson, 2008, Molecular Population Genetics of Drosophila Subtelomeric DNA., Genetics, 178, 477, 10.1534/genetics.107.083196 · DOI
  2. Asahina, 2014, Tachykinin-expressing neurons control male-specific aggressive arousal in Drosophila., Cell, 156, 221, 10.1016/j.cell.2013.11.045 · DOI
  3. Ashburner, 1972, New Mutants Report., Drosoph. Inf. Serv., 49, 34
  4. Asif-Laidin, 2017, Short and long-term evolutionary dynamics of subtelomeric piRNA clusters in Drosophila., DNA Res., 24, 459, 10.1093/dnares/dsx017 · DOI
  5. Baas, 2011, Sugar-free frosting, a homolog of SAD kinase, drives neural-specific glycan expression in the Drosophila embryo., Development, 138, 553, 10.1242/dev.055376 · DOI
  6. Badal, 2006, An FB-NOF mediated duplication of the white gene is responsible for the zeste 1 phenotype in some Drosophila melanogaster unstable strains., Mol. Genet. Genomics, 275, 35, 10.1007/s00438-005-0068-6 · DOI
  7. Badal, 2006, Molecular and bioinformatic analysis of the FB-NOF transposable element., Gene, 371, 130, 10.1016/j.gene.2005.11.020 · DOI
  8. Badal, 2013, FB-NOF is a non-autonomous transposable element, expressed in Drosophila melanogaster and present only in the melanogaster group., Gene, 526, 459, 10.1016/j.gene.2013.04.082 · DOI
  9. Bardin, 2010, Transcriptional control of stem cell maintenance in the Drosophila intestine., Development, 137, 705, 10.1242/dev.039404 · DOI
  10. Besse, 2003, Apoptosis-mediated cell death within the ovarian polar cell lineage of Drosophila melanogaster., Development, 130, 1017, 10.1242/dev.00313 · DOI
  11. Biessmann, 1988, Progressive loss of DNA sequences from terminal chromosome deficiencies in Drosophila melanogaster., EMBO J., 7, 1081, 10.1002/j.1460-2075.1988.tb02916.x · DOI
  12. Brodsky, 2004, Drosophila melanogaster MNK/Chk2 and p53 Regulate Multiple DNA Repair and Apoptotic Pathways following DNA Damage., Mol. Cell. Biol., 24, 1219, 10.1128/MCB.24.3.1219-1231.2004 · DOI
  13. Buddika, 2020, Canonical nucleators are dispensable for stress granule assembly in Drosophila intestinal progenitors., J. Cell Sci., 133, jcs243451, 10.1242/jcs.243451 · DOI
  14. Cáceres, 1999, Generation of a Widespread Drosophila Inversion by a Transposable Element., Science, 285, 415, 10.1126/science.285.5426.415 · DOI
  15. Casals, 2003, The Foldback-like Transposon Galileo Is Involved in the Generation of Two Different Natural Chromosomal Inversions of Drosophila buzzatii., Mol. Biol. Evol., 20, 674, 10.1093/molbev/msg070 · DOI
  16. de Celis, 1995, Ventral veinless, the gene encoding the Cf1a transcription factor, links positional information and cell differentiation during embryonic and imaginal development in Drosophila melanogaster., Development, 121, 3405, 10.1242/dev.121.10.3405 · DOI
  17. Cingolani, 2012, A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3., Fly (Austin), 6, 80, 10.4161/fly.19695 · DOI · Paper page
  18. Comeron, 2012, The many landscapes of recombination in Drosophila melanogaster., PLoS Genet., 8, e1002905, 10.1371/journal.pgen.1002905 · DOI
  19. Danecek, 2011, The variant call format and VCFtools., Bioinformatics, 27, 2156, 10.1093/bioinformatics/btr330 · DOI
  20. Delprat, 2009, The transposon Galileo generates natural chromosomal inversions in Drosophila by ectopic recombination., PLoS One, 4, e7883, 10.1371/journal.pone.0007883 · DOI
  21. Dexter, 1914, The Analysis of a Case of Continuous Variation in Drosophila by a Study of Its Linkage Relations., Am. Nat., 48, 712, 10.1086/279446 · DOI
  22. Diaz-Benjumea, 1990, Genetic analysis of the wing vein pattern of Drosophila., Roux’s Archives Dev Biology Official Organ Edbo, 198, 336, 10.1007/BF00383772 · DOI
  23. Duncan, 1998, Control of distal antennal identity and tarsal development in Drosophila by spineless-aristapedia, a homolog of the mammalian dioxin receptor., Genes Dev., 12, 1290, 10.1101/gad.12.9.1290 · DOI
  24. Fabini, 2001, Identification of core alpha 1,3-fucosylated glycans and cloning of the requisite fucosyltransferase cDNA from Drosophila melanogaster. Potential basis of the neural anti-horseadish peroxidase epitope., J. Biol. Chem., 276, 28058, 10.1074/jbc.M100573200 · DOI
  25. Gray, 1996, P-element-induced recombination in Drosophila melanogaster: hybrid element insertion., Genetics, 144, 1601, 10.1093/genetics/144.4.1601 · DOI
  26. Gutzwiller, 2015, Dynamics of Wolbachia pipientis Gene Expression Across the Drosophila melanogaster Life Cycle., G3 (Bethesda), 5, 2843, 10.1534/g3.115.021931 · DOI
  27. Haase, 2001, A tissue-specific marker of Ecdysozoa., Dev. Genes Evol., 211, 428, 10.1007/s004270100173 · DOI
  28. Hawley, 1980, Chromosomal sites necessary for normal levels of meiotic recombination in Drosophila melanogaster. I. Evidence for and mapping of the sites., Genetics, 94, 625, 10.1093/genetics/94.3.625 · DOI
  29. Inoue, 1994, On the category of naturally occurring inversions of Drosophila melanogaster., Jpn. J. Genet., 69, 105, 10.1266/jjg.69.105 · DOI
  30. Jan, 1982, Antibodies to horseradish peroxidase as specific neuronal markers in Drosophila and in grasshopper embryos., Proc. Natl. Acad. Sci. USA, 79, 2700, 10.1073/pnas.79.8.2700 · DOI
  31. Kahsai, 2018, Mapping Second Chromosome Mutations to Defined Genomic Regions in Drosophila melanogaster., G3 (Bethesda), 8, 9, 10.1534/g3.117.300289 · DOI
  32. Kahsai, 2010, Neuropeptides in the Drosophila central complex in modulation of locomotor behavior., J. Exp. Biol., 213, 2256, 10.1242/jeb.043190 · DOI
  33. Koch, 2008, Drosophila ankyrin 2 is required for synaptic stability., Neuron, 58, 210, 10.1016/j.neuron.2008.03.019 · DOI
  34. Kolmogorov, 2019, Assembly of long, error-prone reads using repeat graphs., Nat. Biotechnol., 37, 540, 10.1038/s41587-019-0072-8 · DOI · Paper page
  35. Kurzhals, 2011, Chk2 and p53 are haploinsufficient with dependent and independent functions to eliminate cells after telomere loss., PLoS Genet., 7, e1002103, 10.1371/journal.pgen.1002103 · DOI
  36. Larsson, 1996, Mutations in the Drosophila melanogaster gene encoding S-adenosylmethionine synthetase suppress position-effect variegation., Genetics, 143, 887, 10.1093/genetics/143.2.887 · DOI
  37. Lee, 2007, Loss of LRRK2/PARK8 induces degeneration of dopaminergic neurons in Drosophila., Biochem. Biophys. Res. Commun., 358, 534, 10.1016/j.bbrc.2007.04.156 · DOI
  38. Lee, 2003, In vivo p53 function is indispensable for DNA damage-induced apoptotic signaling in Drosophila., FEBS Lett., 550, 5, 10.1016/S0014-5793(03)00771-3 · DOI
  39. Levis, 1993, Transposons in place of telomeric repeats at a Drosophila telomere., Cell, 75, 1083, 10.1016/0092-8674(93)90318-K · DOI
  40. Li, 2009, Fast and accurate short read alignment with Burrows–Wheeler transform., Bioinformatics, 25, 1754, 10.1093/bioinformatics/btp324 · DOI · Paper page
  41. Li, 2009, The Sequence Alignment/Map format and SAMtools., Bioinformatics, 25, 2078, 10.1093/bioinformatics/btp352 · DOI · Paper page
  42. Mason, 2004, A Deficiency Screen for Dominant Suppressors of Telomeric Silencing in Drosophila., Genetics, 168, 1353, 10.1534/genetics.104.030676 · DOI
  43. Mehrotra, 2008, Endocycling cells do not apoptose in response to DNA rereplication genotoxic stress., Genes Dev., 22, 3158, 10.1101/gad.1710208 · DOI
  44. Micchelli, 2006, Evidence that stem cells reside in the adult Drosophila midgut epithelium., Nature, 439, 475, 10.1038/nature04371 · DOI
  45. Miller, 2016, Third Chromosome Balancer Inversions Disrupt Protein-Coding Genes and Influence Distal Recombination Events in Drosophila melanogaster., G3 (Bethesda), 6, 1959, 10.1534/g3.116.029330 · DOI
  46. Miller, 2019, The joy of balancers., PLoS Genet., 15, e1008421, 10.1371/journal.pgen.1008421 · DOI
  47. Miller, 2018, The Molecular and Genetic Characterization of Second Chromosome Balancers in Drosophila melanogaster, G3 (Bethesda), 8, 1161, 10.1534/g3.118.200021 · DOI
  48. Miller, 2016, Rare recombination events generate sequence diversity among balancer chromosomes in Drosophila melanogaster., Proc. Natl. Acad. Sci. USA, 113, E1352, 10.1073/pnas.1601232113 · DOI
  49. Miller, 2018, Highly Contiguous Genome Assemblies of 15 Drosophila Species Generated Using Nanopore Sequencing., G3 (Bethesda), 8, 3131, 10.1534/g3.118.200160 · DOI
  50. Morata, 1978, Anterior and posterior compartments in the head of Drosophila., Nature, 274, 473, 10.1038/274473a0 · DOI
  51. Morgan, 1937, Constitution of the germinal material in relation to heredity., Yearb. Carnegie Instn, 36, 298
  52. Moschetti, 2004, FB elements can promote exon shuffling: a promoter-less white allele can be reactivated by FB mediated transposition in Drosophila melanogaster., Mol. Genet. Genomics, 271, 394, 10.1007/s00438-004-1007-7 · DOI
  53. Muller, 1918, Genetic Variability, Twin Hybrids and Constant Hybrids, in a Case of Balanced Lethal Factors., Genetics, 3, 422, 10.1093/genetics/3.5.422 · DOI
  54. Nüsslein-Volhard, 1984, Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster: I. Zygotic loci on the second chromosome., Wihelm Roux Arch. Dev. Biol., 193, 267, 10.1007/BF00848156 · DOI
  55. O’Brien, 2011, Altered modes of stem cell division drive adaptive intestinal growth., Cell, 147, 603, 10.1016/j.cell.2011.08.048 · DOI
  56. Orengo, 2019, The molecular characterization of fixed inversions breakpoints unveils the ancestral character of the Drosophila guanche chromosomal arrangements., Sci Rep-uk, 9, 1706, 10.1038/s41598-018-37121-5 · DOI
  57. Payne, 1924, Crossover Modifiers in the Third Chromosome of Drosophila melanogaster., Genetics, 9, 327, 10.1093/genetics/9.4.327 · DOI
  58. Phalke, 2009, Retrotransposon silencing and telomere integrity in somatic cells of Drosophila depends on the cytosine-5 methyltransferase DNMT2., Nat. Genet., 41, 696, 10.1038/ng.360 · DOI
  59. Qi, 2016, Different cell cycle modifications repress apoptosis at different steps independent of developmental signaling in Drosophila., Mol. Biol. Cell, 27, 1885, 10.1091/mbc.e16-03-0139 · DOI
  60. Radion, 2018, Key role of piRNAs in telomeric chromatin maintenance and telomere nuclear positioning in Drosophila germline., Epigenetics Chromatin, 11, 40, 10.1186/s13072-018-0210-4 · DOI
  61. Ranz, 2007, Principles of Genome Evolution in the Drosophila melanogaster Species Group., PLoS Biol., 5, e152, 10.1371/journal.pbio.0050152 · DOI
  62. Rein, 1999, A quantitative three-dimensional model of the Drosophila optic lobes., Curr. Biol., 9, 93, 10.1016/S0960-9822(99)80021-9 · DOI
  63. Reis, 2018, Origin and consequences of chromosomal inversions in the virilis group of Drosophila., Genome Biol. Evol., 10, 3152, 10.1093/gbe/evy239 · DOI
  64. Roegiers, 2009, Frequent unanticipated alleles of lethal giant larvae in Drosophila second chromosome stocks., Genetics, 182, 407, 10.1534/genetics.109.101808 · DOI
  65. Rong, 2002, Targeted mutagenesis by homologous recombination in D. melanogaster., Genes Dev., 16, 1568, 10.1101/gad.986602 · DOI
  66. Schwartz, 2008, 10.4159/9780674043336 · DOI
  67. Seppo, 2003, Induction of neuron-specific glycosylation by Tollo/Toll-8, a Drosophila Toll-like receptor expressed in non-neural cells., Development, 130, 1439, 10.1242/dev.00347 · DOI
  68. Shearin, 2014, Hexameric GFP and mCherry reporters for the Drosophila GAL4, Q, and LexA transcription systems., Genetics, 196, 951, 10.1534/genetics.113.161141 · DOI
  69. Snow, 1987, Neural-specific carbohydrate moiety shared by many surface glycoproteins in Drosophila and grasshopper embryos., J. Neurosci., 7, 4137, 10.1523/JNEUROSCI.07-12-04137.1987 · DOI
  70. Sogame, 2003, Drosophila p53 preserves genomic stability by regulating cell death., Proc. Natl. Acad. Sci. USA, 100, 4696, 10.1073/pnas.0736384100 · DOI
  71. Struhl, 1982, Spineless-aristapedia: a homeotic gene that does not control the development of specific compartments in Drosophila., Genetics, 102, 737, 10.1093/genetics/102.4.737 · DOI
  72. Sturtevant, 1926, A crossover reducer in Drosophila melanogaster due to inversion of a section of the third chromosome., Biol. Zent. Bl., 697, 702
  73. Sturtevant, 1931, Known and probable inverted sections of the autosomes of Drosophila melanogaster., Publications of the Carnegie Institution, 421, 1
  74. Tang, 2020, Mutant p53 on the Path to Metastasis., Trends Cancer, 6, 62, 10.1016/j.trecan.2019.11.004 · DOI
  75. Tearle, 1987, Tübingen mutants and stock list., Drosoph. Inf. Serv., 66, 209
  76. Tinderholt, 1960, New Mutants Report., Drosoph. Inf. Serv., 34, 53
  77. Wagh, 2006, Bruchpilot, a Protein with Homology to ELKS/CAST, Is Required for Structural Integrity and Function of Synaptic Active Zones in Drosophila., Neuron, 49, 833, 10.1016/j.neuron.2006.02.008 · DOI · Paper page
  78. Ward, 1923, The Genetics of Curly Wing in Drosophila. Another Case of Balanced Lethal Factors., Genetics, 8, 276, 10.1093/genetics/8.3.276 · DOI
  79. Xie, 2004, Gene Deletions by Ends-In Targeting in Drosophila melanogaster., Genetics, 168, 1477, 10.1534/genetics.104.030882 · DOI
  80. Yagi, 2010, Functional analysis of Toll-related genes in Drosophila., Dev. Growth Differ., 52, 771, 10.1111/j.1440-169X.2010.01213.x · DOI
  81. Yamamoto-Hino, 2010, Identification of genes required for neural-specific glycosylation using functional genomics., PLoS Genet., 6, e1001254, 10.1371/journal.pgen.1001254 · DOI
  82. Yazdani, 2008, The glucose transporter (GLUT4) enhancer factor is required for normal wing positioning in Drosophila., Genetics, 178, 919, 10.1534/genetics.107.078030 · DOI
  83. Zhou, 2019, Advances in Experimental Medicine and Biology., Adv. Exp. Med. Biol., 1167, 105, 10.1007/978-3-030-23629-8_6 · DOI

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Metadata

Authors
Miller, D. E., Kahsai, L., Buddika, K., Dixon, M. J., Kim, B. Y., Calvi, B. R., Sokol, N. S., Hawley, R. S., & Cook, K. R.
Affiliations
  • Department of Pediatrics, Division of Genetic Medicine, University of Washington, and Seattle Children’s Hospital, Seattle, WA 98105
  • Department of Biology, Indiana University, Bloomington, IN 47405
  • Department of Biology, Stanford University, Stanford, CA 94305
  • Department of Molecular and Integrative Physiology, University of Kansas Medical Center, Kansas City, KS 66160
Venue
G3 Genes|Genomes|Genetics
Publisher
Oxford University Press (OUP)
Published
2020-11-01
Volume
10
Issue
11
Pages
4271-4285
ISSN
2160-1836
DOI
10.1534/g3.120.401559
PMC
PMC7642927
Cited by
16
References
2
Language
en
Licence
academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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