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Title: Meiosis genes in Daphnia pulexand the role of parthenogenesis in genome evolution

Abstract

Background: Thousands of parthenogenetic animal species have been described and cytogenetic manifestations of this reproductive mode are well known. However, little is understood about the molecular determinants of parthenogenesis. The Daphnia pulex genome must contain the molecular machinery for different reproductive modes: sexual (both male and female meiosis) and parthenogenetic (which is either cyclical or obligate). This feature makes D. pulex an ideal model to investigate the genetic basis of parthenogenesis and its consequences for gene and genome evolution. Here we describe the inventory of meiotic genes and their expression patterns during meiotic and parthenogenetic reproduction to help address whether parthenogenesis uses existing meiotic and mitotic machinery, or whether novel processes may be involved. Results: We report an inventory of 130 homologs representing over 40 genes encoding proteins with diverse roles in meiotic processes in the genome of D. pulex. Many genes involved in cell cycle regulation and sister chromatid cohesion are characterized by expansions in copy number. In contrast, most genes involved in DNA replication and homologous recombination are present as single copies. Notably, RECQ2 (which suppresses homologous recombination) is present in multiple copies while DMC1 is the only gene in our inventory that is absent in the Daphniamore » genome. Expression patterns for 44 gene copies were similar during meiosis versus parthenogenesis, although several genes displayed marked differences in expression level in germline and somatic tissues. Conclusion: We propose that expansions in meiotic gene families in D. pulex may be associated with parthenogenesis. Taking into account our findings, we provide a mechanistic model of parthenogenesis, highlighting steps that must differ from meiosis including sister chromatid cohesion and kinetochore attachment.« less

Authors:
 [1];  [1];  [2]
  1. Univ. of Iowa, Iowa City, IA (United States). Dept. of Biology. Roy J. Carver Center for Comparative Genomics
  2. Indiana Univ., Bloomington, IN (United States). Dept. of Biology. The Center forGenomics and Bioinformatics
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Univ. of California, San Diego, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
OSTI Identifier:
1626385
Grant/Contract Number:  
AC02-05CH11231; W-7405-ENG-36; W-7405-ENG-48
Resource Type:
Accepted Manuscript
Journal Name:
BMC Evolutionary Biology (Online)
Additional Journal Information:
Journal Name: BMC Evolutionary Biology (Online); Journal Volume: 9; Journal Issue: 1; Journal ID: ISSN 1471-2148
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Evolutionary Biology; Genetics & Heredity

Citation Formats

Schurko, Andrew M., Logsdon, John M., and Eads, Brian D. Meiosis genes in Daphnia pulexand the role of parthenogenesis in genome evolution. United States: N. p., 2009. Web. doi:10.1186/1471-2148-9-78.
Schurko, Andrew M., Logsdon, John M., & Eads, Brian D. Meiosis genes in Daphnia pulexand the role of parthenogenesis in genome evolution. United States. https://doi.org/10.1186/1471-2148-9-78
Schurko, Andrew M., Logsdon, John M., and Eads, Brian D. Tue . "Meiosis genes in Daphnia pulexand the role of parthenogenesis in genome evolution". United States. https://doi.org/10.1186/1471-2148-9-78. https://www.osti.gov/servlets/purl/1626385.
@article{osti_1626385,
title = {Meiosis genes in Daphnia pulexand the role of parthenogenesis in genome evolution},
author = {Schurko, Andrew M. and Logsdon, John M. and Eads, Brian D.},
abstractNote = {Background: Thousands of parthenogenetic animal species have been described and cytogenetic manifestations of this reproductive mode are well known. However, little is understood about the molecular determinants of parthenogenesis. The Daphnia pulex genome must contain the molecular machinery for different reproductive modes: sexual (both male and female meiosis) and parthenogenetic (which is either cyclical or obligate). This feature makes D. pulex an ideal model to investigate the genetic basis of parthenogenesis and its consequences for gene and genome evolution. Here we describe the inventory of meiotic genes and their expression patterns during meiotic and parthenogenetic reproduction to help address whether parthenogenesis uses existing meiotic and mitotic machinery, or whether novel processes may be involved. Results: We report an inventory of 130 homologs representing over 40 genes encoding proteins with diverse roles in meiotic processes in the genome of D. pulex. Many genes involved in cell cycle regulation and sister chromatid cohesion are characterized by expansions in copy number. In contrast, most genes involved in DNA replication and homologous recombination are present as single copies. Notably, RECQ2 (which suppresses homologous recombination) is present in multiple copies while DMC1 is the only gene in our inventory that is absent in the Daphnia genome. Expression patterns for 44 gene copies were similar during meiosis versus parthenogenesis, although several genes displayed marked differences in expression level in germline and somatic tissues. Conclusion: We propose that expansions in meiotic gene families in D. pulex may be associated with parthenogenesis. Taking into account our findings, we provide a mechanistic model of parthenogenesis, highlighting steps that must differ from meiosis including sister chromatid cohesion and kinetochore attachment.},
doi = {10.1186/1471-2148-9-78},
journal = {BMC Evolutionary Biology (Online)},
number = 1,
volume = 9,
place = {United States},
year = {Tue Apr 21 00:00:00 EDT 2009},
month = {Tue Apr 21 00:00:00 EDT 2009}
}

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The Smc5–Smc6 complex and SUMO modification of Rad52 regulates recombinational repair at the ribosomal gene locus
journal, July 2007

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Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over
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Cyclin-dependent kinase 2 is essential for meiosis but not for mitotic cell division in mice
journal, August 2003

  • Ortega, Sagrario; Prieto, Ignacio; Odajima, Junko
  • Nature Genetics, Vol. 35, Issue 1
  • DOI: 10.1038/ng1232

Homologous chromosome interactions in meiosis: diversity amidst conservation
journal, June 2005

  • Gerton, Jennifer L.; Hawley, R. Scott
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  • DOI: 10.1038/nrg1614

Meiosis: cell-cycle controls shuffle and deal
journal, December 2004

  • Marston, Adèle L.; Amon, Angelika
  • Nature Reviews Molecular Cell Biology, Vol. 5, Issue 12
  • DOI: 10.1038/nrm1526

The Hop2 and Mnd1 proteins act in concert with Rad51 and Dmc1 in meiotic recombination
journal, April 2005

  • Petukhova, Galina V.; Pezza, Roberto J.; Vanevski, Filip
  • Nature Structural & Molecular Biology, Vol. 12, Issue 5
  • DOI: 10.1038/nsmb923

Diverse, endemic and polyphyletic clones in mixed populations of a freshwater snail (Potamopyrgus antipodarum)
journal, May 1995


Ameiotic recombination in asexual lineages of Daphnia
journal, November 2006

  • Omilian, A. R.; Cristescu, M. E. A.; Dudycha, J. L.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 49
  • DOI: 10.1073/pnas.0606435103

Restoration of mismatch repair to nuclear extracts of H6 colorectal tumor cells by a heterodimer of human MutL homologs.
journal, March 1995

  • Li, G. M.; Modrich, P.
  • Proceedings of the National Academy of Sciences, Vol. 92, Issue 6
  • DOI: 10.1073/pnas.92.6.1950

Functional specificity of MutL homologs in yeast: Evidence for three Mlh1-based heterocomplexes with distinct roles during meiosis in recombination and mismatch correction
journal, November 1999

  • Wang, T. -F.; Kleckner, N.; Hunter, N.
  • Proceedings of the National Academy of Sciences, Vol. 96, Issue 24
  • DOI: 10.1073/pnas.96.24.13914

Tid1/Rdh54 promotes colocalization of Rad51 and Dmc1 during meiotic recombination
journal, September 2000

  • Shinohara, M.; Gasior, S. L.; Bishop, D. K.
  • Proceedings of the National Academy of Sciences, Vol. 97, Issue 20
  • DOI: 10.1073/pnas.97.20.10814

Identification of hMutLβ, a Heterodimer of hMLH1 and hPMS1
journal, November 1999

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