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Characterization of a Cdc14 Null Allele in Drosophila Melanogaster

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Characterization of a Cdc14 Null Allele in Drosophila Melanogaster © 2018. Published by The Company of Biologists Ltd | Biology Open (2018) 7, bio037705. doi:10.1242/bio.037705 CORRECTION Correction: Characterization of a cdc14 null allele in Drosophila melanogaster (doi:10.1242/bio.035394) Leif Neitzel, Matthew Broadus, Nailing Zhang, Leah Sawyer, Heather Wallace, Julie Merkle, Jeanne Jodoin, Poojitha Sitaram, Emily Crispi, William Rork, Laura Lee, Duojia Pan, Kathleen Gould, Andrea Page-McCaw and Ethan Lee There were errors published in Biology Open 2018 7: bio035394 doi:10.1242/bio.035394 Incorrect versions of Figure 2B and Figure S5B were used for the published version of this article. The corrected figures are shown below. Fig. 2. cdc14 null males exhibit decreased sperm competition. (B) A control experiment was performed using white-eyed ywmales for both the first and second males. A second control experiment was performed using red-eyed cdc14 null males for both the first and second males. The cdc14 null males are less competitive compared to control males regardless of whether they are the first or second male to mate. Results for a single representative replicates (n≥15 vials per cross) are shown. Additional data can be found in Fig. S5B. Data were analyzed using a Chi-squared test with Bonferroni correction. Six pairwise comparisons were made. Red-eyed control males were compared to the cdc14 null, rescue, or overexpression males; cdc14 null males were compared to rescue or overexpression male; and rescue males were compared to overexpression males. *P<0.009. ***P<0.0002. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed. Biology Open 1 CORRECTION Biology Open (2018) 7, bio037705. doi:10.1242/bio.037705 Figure S5. cdc14 null males mate overnight at the same rate as controls. (B) Eye color of offspring from all replicates of the sperm competition assay. The proportion of offspring from cdc14 null males was significantly lower than the control (red). This decrease was rescued by expression of nos>myc-cdc14. Data were analyzed by Chi-squared test with Bonferroni correction. Control (red) was compared to the cdc14 null, rescue, and overexpression. The cdc14 null was compared to the rescue. *ρ<0.02, **ρ<0.003, ***ρ<0.0003. In (A) and (B), N≥48 vials aggregated in N≥3 experiments. None of these errors affected the conclusions of the paper. The authors apologize for any inconvenience caused by these changes. Biology Open 2 © 2018. Published by The Company of Biologists Ltd | Biology Open (2018) 7, bio035394. doi:10.1242/bio.035394 RESEARCH ARTICLE Characterization of a cdc14 null allele in Drosophila melanogaster Leif R. Neitzel1,2, Matthew R. Broadus1,3, Nailing Zhang4, Leah Sawyer1, Heather A. Wallace1,5,6, Julie A. Merkle1,7, Jeanne N. Jodoin1,8, Poojitha Sitaram9, Emily E. Crispi1, William Rork1, Laura A. Lee10, Duojia Pan4, Kathleen L. Gould1, Andrea Page-McCaw1,2,11,* and Ethan Lee1,2,11,* ABSTRACT 2008; Stegmeier and Amon, 2004). Despite its conservation, Cdc14 Cdc14 is an evolutionarily conserved serine/threonine phosphatase. orthologs are not essential for cell division in all organisms, although Originally identified in Saccharomyces cerevisiae as a cell cycle they play important roles in an array of biological processes, regulator, its role in other eukaryotic organisms remains unclear. In including chromosome segregation (Clemente-Blanco et al., Drosophila melanogaster, Cdc14 is encoded by a single gene, thus 2011; Machin et al., 2016; Mocciaro et al., 2010; Stegmeier facilitating its study. We found that Cdc14 expression is highest in the and Amon, 2004), cytokinesis (Clifford et al., 2008), centrosome testis of adult flies and that cdc14 null flies are viable. cdc14 null duplication (Mocciaro et al., 2010; Rüthnick and Schiebel, female and male flies do not display altered fertility. cdc14 null males, 2016), mitotic exit (Wolfe and Gould, 2004), transcription however, exhibit decreased sperm competitiveness. Previous studies (Clemente-Blanco et al., 2009, 2011; Guillamot et al., 2011; have shown that Cdc14 plays a role in ciliogenesis during zebrafish Papadopoulou et al., 2010), the DNA damage response (Mocciaro development. In Drosophila, sensory neurons are ciliated. We et al., 2010), and ciliogenesis (Clément et al., 2011, 2012). found that the Drosophila cdc14 null mutants have defects in Although they have been much studied, a comprehensive chemosensation and mechanosensation as indicated by decreased understanding of Cdc14 phosphatases in higher eukaryotes in avoidance of repellant substances and decreased response to particular is still lacking. touch. In addition, we show that cdc14 null mutants have defects in A thorough dissection of the role(s) of Cdc14 phosphatases in lipid metabolism and resistance to starvation. These studies metazoans is complicated by the existence of multiple Cdc14 highlight the diversity of Cdc14 function in eukaryotes despite its paralogs in vertebrates (Table S1) (Clément et al., 2011; Kaiser structural conservation. et al., 2004; Krasinska et al., 2007; Li et al., 2000; Mocciaro et al., 2010). For example, human Cdc14 phosphatases are encoded by KEY WORDS: Cdc14, Drosophila, Sensilla, Sperm, Chemosensation, three different genes, CDC14A, CDC14B,andCDC14C (Clément Mechanosensation et al., 2011; Kaiser et al., 2004; Krasinska et al., 2007; Li et al., 2000; Mocciaro et al., 2010). Knockout studies of individual INTRODUCTION human CDC14 genes failed to demonstrate growth or mitotic Cdc14 phosphatases are a well conserved family of proline-directed defects, possibly reflecting functional redundancy between the serine/threonine phosphatases (Mocciaro et al., 2010). Initially paralogs (Berdougo et al., 2008; Mocciaro et al., 2010). However, identified in Saccharomyces cerevisiae as an essential cell cycle it is still unclear whether the cellular functions of Cdc14 paralogs protein (Stegmeier and Amon, 2004), Cdc14 functions to antagonize are fully redundant or simply overlapping. It is clear that they have cyclin-dependent kinase (CDK)-mediated phosphorylation events distinct intracellular locations with CDC14A at centrosomes and (Machin et al., 2016; Mocciaro et al., 2010; Queralt and Uhlmann, CDC14B in the nucleolus of interphase cells (Clément et al., 2011; Kaiser et al., 2004; Krasinska et al., 2007; Li et al., 2000; 1Department of Cell and Developmental Biology, Vanderbilt University Medical Mocciaro et al., 2010), and they have been assigned some distinct Center, Nashville, TN 37232, USA. 2Program in Developmental Biology, functions. While CDC14A has been implicated in cytokinesis, Vanderbilt University School of Medicine, Nashville, TN 37232, USA. 3Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA. transcriptional repression, and DNA damage repair, CDC14B is 4Department of Physiology, University of Texas Southwestern Medical Center, implicated in G1-phase length, centriole duplication, spindle Dallas, TX 75390-9040, USA. 5Division of Genetics, Brigham and Women’s stability, zygotic genome activation, DNA damage repair and Hospital, Boston, MA 02115, USA. 6Department of Genetics, Harvard Medical School, Boston, MA 02115, USA. 7Department of Molecular Biology, Princeton checkpoint response (Buffone et al., 2014; Cho et al., 2005; University, Princeton, NJ 08544, USA. 8Department of Biology, Massachusetts Clemente-Blanco et al., 2011; Rodier et al., 2008; Wu et al., Institute of Technology, Cambridge, MA 02142, USA. 9Department of Microbiology, New York University Langone Medical Center, New York, 2008). The biological role of CDC14C is currently unknown NY 10016, USA. 10Department of Pathology, Microbiology, and Immunology, (Rosso et al., 2008). Vanderbilt University Medical Center, Nashville, TN 37232, USA. 11Vanderbilt Like yeast, the roundworm, Caenorhabditis elegans, has only Ingram Cancer Center, Vanderbilt University Medical Center, Nashville, TN 37232, USA. one identified Cdc14 orthologue. The lack of multiple paralogs makes the roundworm an attractive organism to gain a comprehensive *Authors for correspondence ([email protected]; [email protected]). understanding of Cdc14 phosphatase function in a higher eukaryote. However, in C. elegans, Cdc14 functions in a manner unrelated to N.Z., 0000-0003-3612-215X; D.P., 0000-0003-2890-4645; K.L.G., 0000-0002- that in any other organism reported to date – to promote cellular 3810-4070; A.P., 0000-0003-3193-5362; E.L., 0000-0001-8405-6156 quiescence of specific precursor cells (Cueille et al., 2001; Saito This is an Open Access article distributed under the terms of the Creative Commons Attribution et al., 2004). License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed. The common fruit fly, Drosophila melanogaster also has a single gene that encodes Cdc14 (Dmel\cdc14), the role of which Received 30 April 2018; Accepted 13 June 2018 has not yet been reported (Fisher et al., 2012). Herein, we Biology Open 1 Downloaded from http://bio.biologists.org/ by Benedict Techset on August 20, 2018 RESEARCH ARTICLE Biology Open (2018) 7, bio035394. doi:10.1242/bio.035394 demonstrate that the Drosophila cdc14 gene plays a role in sperm cdc14 to be approximately eleven times higher than whole male competitiveness,
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