DOCSLIB.ORG

Dephosphorylation of Iqg1 by Cdc14 Regulates Cytokinesis in Budding Yeast

Total Page：16

File Type：pdf, Size：1020Kb

Download full-text PDF Read full-text
Dephosphorylation of Iqg1 by Cdc14 Regulates Cytokinesis in Budding Yeast Missouri University of Science and Technology Scholars' Mine Biological Sciences Faculty Research & Creative Works Biological Sciences 01 Jan 2015 Dephosphorylation of Iqg1 by Cdc14 Regulates Cytokinesis in Budding Yeast Daniel P. Miller Hana Kenton Hall Ryan Chaparian Madison Mara et. al. For a complete list of authors, see https://scholarsmine.mst.edu/biosci_facwork/97 Follow this and additional works at: https://scholarsmine.mst.edu/biosci_facwork Part of the Biology Commons Recommended Citation D. P. Miller et al., "Dephosphorylation of Iqg1 by Cdc14 Regulates Cytokinesis in Budding Yeast," Molecular Biology of the Cell, vol. 26, no. 16, pp. 2913-2926, American Society for Cell Biology, Jan 2015. The definitive version is available at https://doi.org/10.1091/mbc.E14-12-1637 This work is licensed under a Creative Commons Attribution-Noncommercial-Share Alike 3.0 License. This Article - Journal is brought to you for free and open access by Scholars' Mine. It has been accepted for inclusion in Biological Sciences Faculty Research & Creative Works by an authorized administrator of Scholars' Mine. This work is protected by U. S. Copyright Law. Unauthorized use including reproduction for redistribution requires the permission of the copyright holder. For more information, please contact [email protected]. M BoC | ARTICLE Dephosphorylation of Iqg1 by Cdc14 regulates cytokinesis in budding yeast Daniel P. Millera, Hana Hallb, Ryan Chaparianb, Madison Maraa, Alison Muellera, Mark C. Hallb, and Katie B. Shannona aDepartment of Biological Sciences, Missouri University of Science and Technology, Rolla, MO 65401; bDepartment of Biochemistry, Purdue Center for Cancer Research, Purdue University, West Lafayette, IN 47907 ABSTRACT Cytokinesis separates cells by contraction of a ring composed of filamentous Monitoring Editor actin (F-actin) and type II myosin. Iqg1, an IQGAP family member, is an essential protein in Daniel J. Lew Saccharomyces cerevisiae required for assembly and contraction of the actomyosin ring. Lo- Duke University calization of F-actin to the ring occurs only after anaphase and is mediated by the calponin Received: Dec 22, 2014 homology domain (CHD) of Iqg1, but the regulatory mechanisms that temporally restrict ac- Revised: Jun 8, 2015 tin ring assembly are not well defined. We tested the hypothesis that dephosphorylation of Accepted: Jun 9, 2015 four perfect cyclin-dependent kinase (Cdk) sites flanking the CHD promotes actin ring forma- tion, using site-specific alanine mutants. Cells expressing the nonphosphorylatableiqg1-4A allele formed actin rings before anaphase and exhibited defects in myosin contraction and cytokinesis. The Cdc14 phosphatase is required for normal cytokinesis and acts on specific Cdk phosphorylation sites. Overexpression of Cdc14 resulted in premature actin ring assem- bly, whereas inhibition of Cdc14 function prevented actin ring formation. Cdc14 associated with Iqg1, dependent on several CHD-flanking Cdk sites, and efficiently dephosphorylated these sites in vitro. Of importance, the iqg1-4A mutant rescued the inability of cdc14-1 cells to form actin rings. Our data support a model in which dephosphorylation of Cdk sites around the Iqg1 CHD by Cdc14 is both necessary and sufficient to promote actin ring formation. Temporal control of actin ring assembly by Cdk and Cdc14 may help to ensure that cytokine- sis onset occurs after nuclear division is complete. INTRODUCTION Cytokinesis, the final step in cell division, divides the cytoplasm and Pollard, 1992; Fishkind and Wang, 1995). The actomyosin ring between two daughter cells. Precise temporal control is necessary is a transient structure that is precisely positioned to bisect the to coordinate cytokinesis and mitosis so that proper chromosome elongating anaphase spindle, ensuring proper chromosome segre- segregation can be completed. Cytokinetic failure results in tetra- gation (Pollard, 2010). In yeast, actomyosin ring contraction must ploid cells, and there is evidence that tetraploidy is an intermediate be coordinated with septation, the process of adding new cell wall state leading to chromosomal instability, aneuploidy, and tumori- material between the dividing cells (Bi, 2001). genesis (Ganem et al., 2007; Storchova and Kuffer, 2008). In animal In budding yeast, both actomyosin ring assembly and contrac- and fungal cells, cytokinesis is achieved by a ring composed of fila- tion are cell cycle regulated. The type II myosin heavy chain, Myo1, mentous actin (F-actin) and nonmuscle type II myosin (Satterwhite forms a ring at the bud neck in G1 (Bi et al., 1998; Lippincott and Li, 1998b). Localization of F-actin and contraction of the ring occur af- ter anaphase and require the essential protein Iqg1/Cyk1 (Epp and This article was published online ahead of print in MBoC in Press (http://www Chant, 1997; Lippincott and Li, 1998b; Lippincott et al., 2001). Iqg1 .molbiolcell.org/cgi/doi/10.1091/mbc.E14-12-1637) on June 17, 2015. is a 173-kDa scaffolding protein homologous to mammalian Address correspondence to: Katie B. Shannon ([email protected]). IQGAPs. IQGAP family members are essential for actin-based pro- Abbreviations used: Cdk, cyclin-dependent kinase; CHD, calponin homology domain; FEAR, fourteen early anaphase release; MEN, mitotic exit network. cesses such as phagocytosis, cell adhesion, migration, and cytokine- © 2015 Miller et al. This article is distributed by The American Society for Cell Bi- sis (Shannon, 2012; White et al., 2012). Iqg1 shares with other ology under license from the author(s). Two months after publication it is available IQGAPs multiple functional domains: an N-terminal calponin homol- to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License (http://creativecommons.org/licenses/by-nc-sa/3.0). ogy domain (CHD), IQ repeats, a GTPase-related domain (GRD), “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of and a Ras-GAP C-terminus (RGCt; Epp and Chant, 1997; Lippincott the Cell®” are registered trademarks of The American Society for Cell Biology. and Li, 1998a; Shannon, 2012). Iqg1 is recruited to the bud neck by Supplemental Material can be found at: Volume 26 August 15, 2015 http://www.molbiolcell.org/content/suppl/2015/06/14/mbc.E14-12-1637v1.DC1.html 2913 the myosin regulatory light chain, Mlc1, via interactions with the IQ primarily to promote proper spindle function and chromosome seg- domains (Boyne et al., 2000; Shannon and Li, 2000). Iqg1 recruit- regation. After chromosome segregation is completed, the MEN ment to the ring is restricted to mitosis even though Mlc1 localizes triggers widespread release of Cdc14 to the cytoplasm (Queralt and to the bud neck earlier in the cell cycle (Boyne et al., 2000; Shannon Uhlmann, 2008; Uhlmann et al., 2011). Although many Cdc14 target and Li, 2000). Iqg1 binds F-actin via the CHD and recruits F-actin to proteins required for mitotic exit and other mitotic events are well the bud neck during anaphase/telophase of mitosis, which com- characterized, a direct role for Cdc14 in regulating actomyosin ring pletes actomyosin ring assembly (Shannon and Li, 1999). The C- assembly has not previously been described. terminus of Iqg1, containing both the GRD and RGCt domains, in- In the yeast Candida albicans, the Igq1 homologue is phosphor- teracts with the GTPase Tem1 and is required for contraction of the ylated in vitro by the cyclin-dependent kinase Cdk1. Mutation of 15 actomyosin ring (Shannon and Li, 1999). Tem1 is part of the mitotic minimal Cdk1 consensus sites (S/T-P) in Iqg1 flanking the CHD re- exit network (MEN), and temperature-sensitive alleles of Tem1 and sulted in premature assembly and delayed disassembly of the acto- other MEN proteins cause mitotic arrest in late anaphase before myosin ring, resulting in cytokinesis defects (Li et al., 2008). Budding cytokinesis (Jaspersen et al., 1998; McCollum and Gould, 2001). yeast Iqg1 is phosphorylated in vivo by Cdk1 (Holt et al., 2009), and The MEN, a signaling cascade that leads to the full release and a recent report demonstrated that loss of various combinations of activity of the phosphatase Cdc14, regulates mitotic exit, cytokine- N-terminal Cdk1 sites caused premature recruitment of Iqg1 and sis, and septation in budding yeast (Bardin and Amon, 2001; Meit- actin filaments to the contractile ring (Naylor and Morgan, 2014). inger et al., 2012). The MEN brings about exit from mitosis by inac- Although there are 20 minimal consensus Cdk sites (S/T-P) in bud- tivating the mitotic cyclin-dependent kinase 1 (Cdk1). Cdk1, or ding yeast Iqg1, only 4 match the strict Cdk consensus motif S/T-P- Cdc28-Clb2 in budding yeast, is inactivated during anaphase via x-R/K, and these are all adjacent to the CHD near the Iqg1 N-termi- two partially redundant methods: inhibition of its kinase activity by nus. Recently, Cdc14 was shown to possess specificity for the Sic1 and degradation of the mitotic cyclin Clb2 by the APCCdh1 com- phosphoserine subset of the perfect Cdk consensus sites, and 3 of plex (Jaspersen et al., 1998; Visintin et al., 1998). Both Sic1 and the CHD-flanking Cdk consensus sites also match the consensus for Cdh1 become active once dephosphorylated by the MEN compo- dephosphorylation by Cdc14 (Bremmer et al., 2012; Eissler et al., nent Cdc14, leading to inhibition of Cdk1 activity (Visintin et al., 2014). We hypothesized that dephosphorylation of these Cdk sites 1998). When Cdk1 activity drops, MEN proteins Cdc15, Dbf2-Mob1, by Cdc14 is important for controlling Iqg1 function in cytokinesis. In Dbf20-Mob1, and Cdc14 all accumulate to the bud neck by an un- this study we present genetic, cell biological, and biochemical evi- known mechanism, where they are positioned to regulate cytokine- dence supporting this hypothesis and demonstrate that dephos- sis and septation (Bembenek et al., 2005; Meitinger et al., 2012). phorylation of Iqg1 by Cdc14 is required for normal assembly of Although Cdk1 must be inactivated in order for actomyosin ring Iqg1 and F-actin in the contractile ring, providing insight into the assembly and contraction to occur, the MEN has a role in promoting mechanism of temporal regulation of cytokinesis.
Load more

Recommended publications
  • Sample Thesis Title with a Concise and Accurate
    DISTINCT FUNCTIONS FOR THE HIGHLY RELATED PP2A B55 REGULATORY SUBUNITS (Bα AND Bδ) IN CELL CYCLE REGULATION AND TUMOURIGENESIS by Dominik Sommerfeld B.Sc., The University of British Columbia, 2009 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY in THE FACULTY OF GRADUATE AND POSTDOCTORAL STUDIES (Experimental Medicine) THE UNIVERSITY OF BRITISH COLUMBIA (Vancouver) August 2018 © Dominik Sommerfeld, 2018 The following individuals certify that they have read, and recommend to the Faculty of Graduate and Postdoctoral Studies for acceptance, the dissertation entitled: Distinct functions for the highly related PP2A B55 regulatory subunits (Bα and Bδ) in cell cycle regulation and tumourigenesis submitted by Dominik Sommerfeld in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Experimental Medicine Examining Committee: Catherine Pallen, Ph.D. Supervisor Christopher Maxwell, Ph.D. Supervisory Committee Member Gregg Morin, Ph.D. Supervisory Committee Member Stephan Taubert, Ph.D. University Examiner Calvin Roskelley, Ph.D. University Examiner Additional Supervisory Committee Members: Samuel Aparicio, Ph.D. Supervisory Committee Member ii Abstract Progression through the phases of the cell cycle (G1, S, G2, and mitosis) is largely driven by the coordinated activities of protein kinases and phosphatases, which orchestrate the phase-specific phosphorylation of proteins. Protein Phosphatase 2A (PP2A) – a heterotrimeric holoenzyme complex composed of a scaffold (A), catalytic (C), and variable regulatory (B) subunit – has emerged as an essential cell cycle regulator. Specifically, PP2A complexes containing the B55 family of regulatory subunits (PP2A-B55) have been implicated in the control of various cell cycle phases. My studies investigated isoform-specific roles of the two highly related and abundantly expressed B55 subunits, Bα and Bδ, in the regulation of G1, S, G2 phase and mitotic progression.
    [Show full text]
  • Characterization of a Novel Chromatin―Induced Mechanism
    Rockefeller University Digital Commons @ RU Student Theses and Dissertations 2010 Characterization of a Novel Chromatinâ€Induced Mechanism that Couples Microtubule Disassembly and Nuclear Reâ€Formation Eileen Madeleine Woo Follow this and additional works at: http://digitalcommons.rockefeller.edu/ student_theses_and_dissertations Part of the Life Sciences Commons Recommended Citation Woo, Eileen Madeleine, "Characterization of a Novel Chromatinâ€Induced Mechanism that Couples Microtubule Disassembly and Nuclear Reâ€Formation" (2010). Student Theses and Dissertations. Paper 88. This Thesis is brought to you for free and open access by Digital Commons @ RU. It has been accepted for inclusion in Student Theses and Dissertations by an authorized administrator of Digital Commons @ RU. For more information, please contact [email protected]. CHARACTERIZATION OF A NOVEL CHROMATIN‐ INDUCED MECHANISM THAT COUPLES MICROTUBULE DISASSEMBLY AND NUCLEAR RE‐FORMATION A Thesis Presented to the Faculty of The Rockefeller University in Partial Fulfillment of the Requirements for the degree of Doctor of Philosophy by Eileen Madeleine Woo June 2010 © Copyright by Eileen M. Woo 2010 CHARACTERIZATION OF A NOVEL CHROMATIN‐INDUCED MECHANISM THAT COUPLES MICROTUBULE DISASSEMBLY AND NUCLEAR RE‐FORMATION Eileen M. Woo, Ph.D. The Rockefeller University 2010 Upon completion of mitosis, the disassembly of spindle components and reassembly of nuclear structures occur simultaneously around chromatin. Previous studies have suggested that an important step in this process is the inactivation of the Aurora B kinase by the Triple A‐ATPase Cdc48/p97, which physically extracts the protein from chromatin at anaphase. Aurora B is the catalytic subunit of the Chromosome Passenger Complex (CPC), which promotes microtubule polymerization and spindle formation from mitotic chromosomes.
    [Show full text]
  • The Multiple Roles of the Cdc14 Phosphatase in Cell Cycle Control
    International Journal of Molecular Sciences Review The Multiple Roles of the Cdc14 Phosphatase in Cell Cycle Control Javier Manzano-López and Fernando Monje-Casas * Centro Andaluz de Biología Molecular y Medicina Regenerativa (CABIMER), Spanish National Research Council (CSIC)—University of Seville—University Pablo de Olavide, 41092 Sevilla, Spain; [email protected] * Correspondence: [email protected] Received: 31 December 2019; Accepted: 20 January 2020; Published: 21 January 2020 Abstract: The Cdc14 phosphatase is a key regulator of mitosis in the budding yeast Saccharomyces cerevisiae. Cdc14 was initially described as playing an essential role in the control of cell cycle progression by promoting mitotic exit on the basis of its capacity to counteract the activity of the cyclin-dependent kinase Cdc28/Cdk1. A compiling body of evidence, however, has later demonstrated that this phosphatase plays other multiple roles in the regulation of mitosis at different cell cycle stages. Here, we summarize our current knowledge about the pivotal role of Cdc14 in cell cycle control, with a special focus in the most recently uncovered functions of the phosphatase. Keywords: Cdc14; phosphatase; mitotic exit; genome stability; nucleolus; autophagy; cytokinesis 1. Introduction The cell cycle comprises a series of processes that ensure the duplication of the genome and the cellular content, as well as their safe partitioning between the two newly generated daughter cells. Among other mechanisms, the coordination between these events is safeguarded by an accurate balance between kinases and phosphatases that regulate the phosphorylation status of the proteins that control the progression through mitosis. In the budding yeast Saccharomyces cerevisiae, the Cdc14 phosphatase, originally described in the pioneer screening carried out by Hartwell et al.
    [Show full text]
  • A Defect of Kap104 Alleviates the Requirement of Mitotic Exit Network Gene Functions in Saccharomyces Cerevisiae
    Copyright 2002 by the Genetics Society of America A Defect of Kap104 Alleviates the Requirement of Mitotic Exit Network Gene Functions in Saccharomyces cerevisiae Kazuhide Asakawa and Akio Toh-e1 Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Hongo, Tokyo 113-0033, Japan Manuscript received June 11, 2002 Accepted for publication September 9, 2002 ABSTRACT A subgroup of the karyopherin ␤ (also called importin ␤) protein that includes budding yeast Kap104 and human transportin/karyopherin ␤2 is reported to function as a receptor for the transport of mRNA- binding proteins into the nucleus. We identified KAP104 as a responsible gene for a suppressor mutation of cdc15-2. We found that the kap104-E604K mutation suppressed the temperature-sensitive growth of cdc15-2 cells by promoting the exit from mitosis and suppressed the temperature sensitivity of various mitotic- exit mutations. The cytokinesis defect of these mitotic-exit mutants was not suppressed by kap104-E604K. Furthermore, the kap104-E604K mutation delays entry into DNA synthesis even at a permissive temperature. In cdc15-2 kap104-E604K cells, SWI5 and SIC1, but not CDH1, became essential at a high temperature, suggesting that the kap104-E604K mutation promotes mitotic exit via the Swi5-Sic1 pathway. Interestingly, SPO12, which is involved in the release of Cdc14 from the nucleolus during early anaphase, also became essential in cdc15-2 kap104-E604K cells at a high temperature. The kap104-E604K mutation caused a partial delocalization of Cdc14 from the nucleolus during interphase. This delocalization of Cdc14 was suppressed by the deletion of SPO12. These results suggest that a mutation in Kap104 stimulates exit from mitosis through the activation of Cdc14 and implies a novel role for Kap104 in cell-cycle progression in budding yeast.
    [Show full text]
  • Functions of the Cdc14-Family Phosphatase Clp1p in the Cell Cycle Regulation of Schizosaccharomyces Pombe: a Dissertation
    University of Massachusetts Medical School eScholarship@UMMS GSBS Dissertations and Theses Graduate School of Biomedical Sciences 2005-05-20 Functions of the Cdc14-Family Phosphatase Clp1p in the Cell Cycle Regulation of Schizosaccharomyces pombe: A Dissertation Susanne Trautmann University of Massachusetts Medical School Let us know how access to this document benefits ou.y Follow this and additional works at: https://escholarship.umassmed.edu/gsbs_diss Part of the Enzymes and Coenzymes Commons, and the Fungi Commons Repository Citation Trautmann S. (2005). Functions of the Cdc14-Family Phosphatase Clp1p in the Cell Cycle Regulation of Schizosaccharomyces pombe: A Dissertation. GSBS Dissertations and Theses. https://doi.org/10.13028/ 8qvh-7e50. Retrieved from https://escholarship.umassmed.edu/gsbs_diss/10 This material is brought to you by eScholarship@UMMS. It has been accepted for inclusion in GSBS Dissertations and Theses by an authorized administrator of eScholarship@UMMS. For more information, please contact [email protected]. Functions of the Cdc14-family Phosphatase Clplp in the Cell Cycle Regulation of Schizosaccharomyces pombe A Dissertation Presented SUSANNE TRAUTMANN Submitted to the Faculty of the University of Massachusetts Graduate School of Biomedical Sciences, Worcester in partial fulfilment of the requirements for the degree of DOCTOR OF PHILOSOPHY MAY 20, 2005 MOLECULAR GENETICS AND MICROBIOLOGY Interdisciplinary Graduate Program COPYRIGHT INFORMATION Parts of chapters , III and appendix A have appeared in separate publications: Trautmann. S. , Wolfe, B.A. , Jorgensen, P. , Tyers, M. , Gould, K.L. , and McCollum, D. (2001). Fission yeast Clp1p phosphatase regulates G2/M transition and coordination of cytokinesis with cell cycle progression. CUff Bioi 11 , 931-940.
    [Show full text]
  • At the Interface Between Signaling and Executing Anaphase—Cdc14 and the FEAR Network
    Downloaded from genesdev.cshlp.org on October 2, 2021 - Published by Cold Spring Harbor Laboratory Press REVIEW At the interface between signaling and executing anaphase—Cdc14 and the FEAR network Damien D’Amours and Angelika Amon1 Center for Cancer Research, Howard Hughes Medical Institute, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA Anaphase is the stage of the cell cycle when the dupli- known functions depend on its phosphatase activity. In cated genome is separated to opposite poles of the cell. recent years, it has been shown that this phosphatase is The irreversible nature of this event confers a unique required for the execution of multiple anaphase events, burden on the cell and it is therefore not surprising that with its most prominent function being the inactivation the regulation of this cell cycle stage is complex. In bud- of cyclin-dependent kinases (CDKs) during exit from mi- ding yeast, a signaling network known as the Cdc four- tosis (Visintin et al. 1998; Jaspersen et al. 1998). teen early anaphase release (FEAR) network and its ef- Cdc14 activity is tightly regulated. The phosphatase is fector, the protein phosphatase Cdc14, play a key role in bound to an inhibitor, Cfi1/Net1, which keeps it inac- the coordination of the multiple events that occur during tive in the nucleolus for most of the cell cycle. However, anaphase, such as partitioning of the DNA, regulation of from early anaphase until telophase, the interaction be- spindle stability, activation of microtubule forces, and tween the two proteins is lost and Cdc14 becomes ac- initiation of mitotic exit.
    [Show full text]
  • Cell Cycle.Pdf
    TMTM METHODSMETHODS ININ MOLECULAR BIOLOGY Volume 296 Cell Cycle Control Mechanisms and Protocols Edited by Tim Humphrey Gavin Brooks The Budding and Fission Yeasts 3 1 Cell Cycle Molecules and Mechanisms of the Budding and Fission Yeasts Tim Humphrey and Amanda Pearce Summary The cell cycles of the budding yeast Saccharomyces cerevisiae and the fission yeast, Schizosaccharomyces pombe are currently the best understood of all eukaryotes. Studies in these two evolutionarily divergent organisms have identified common control mechanisms, which have provided paradigms for our understanding of the eukaryotic cell cycle. This chapter provides an overview of our current knowledge of the molecules and mechanisms that regulate the mitotic cell cycle in these two yeasts. Key Words Cell cycle; Saccharomyces cerevisiae; Schizosaccharomyces pombe; fission yeast; bud- ding yeast; review. 1. Introduction The eukaryotic cell cycle can be considered as two distinct events, DNA replication (S-phase) and mitosis (M-phase), separated temporally by gaps known as G1 and G2. These events must be regulated to ensure that they occur in the correct order with respect to each other and that they occur only once per cell cycle. Moreover, these discontinuous events must be coordinated with continuous events such as cell growth, in order to maintain normal cell size (reviewed in ref. 1). Significant advances in understanding such cell cycle controls have arisen from the study of these yeasts. The use of yeast as a model system for studying the cell cycle provides a number of advan- tages: yeasts are single-celled, rapidly dividing eukaryotes that can exist in the haploid form.
    [Show full text]
  • 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.
    [Show full text]
  • PDF) If You Wish to Cite from It
    University of Groningen Genome sequencing and analysis of the filamentous fungus Penicillium chrysogenum van den Berg, Marco A.; Albang, Richard; Albermann, Kaj; Badger, Jonathan H.; Daran, Jean-Marc; Driessen, Arnold J. M.; Garcia-Estrada, Carlos; Fedorova, Natalie D.; Harris, Diana M.; Heijne, Wilbert H. M. Published in: Nature Biotechnology DOI: 10.1038/nbt.1498 IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below. Document Version Publisher's PDF, also known as Version of record Publication date: 2008 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): van den Berg, M. A., Albang, R., Albermann, K., Badger, J. H., Daran, J-M., Driessen, A. J. M., Garcia- Estrada, C., Fedorova, N. D., Harris, D. M., Heijne, W. H. M., Joardar, V., Kiel, J. A. K. W., Kovalchuk, A., Martin, J. F., Nierman, W. C., Nijland, J. G., Pronk, J. T., Roubos, J. A., van der Klei, I. J., ... Bovenberg, R. A. L. (2008). Genome sequencing and analysis of the filamentous fungus Penicillium chrysogenum. Nature Biotechnology, 26(10), 1161-1168. https://doi.org/10.1038/nbt.1498 Copyright Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons). The publication may also be distributed here under the terms of Article 25fa of the Dutch Copyright Act, indicated by the “Taverne” license.
    [Show full text]