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

Schurko, Andrew M.; Logsdon, John M.; Eads, Brian D.

doi:10.1186/1471-2148-9-78

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

Journal Article · Tue Apr 21 00:00:00 EDT 2009 · BMC Evolutionary Biology (Online)

DOI:https://doi.org/10.1186/1471-2148-9-78· OSTI ID:1626385

Schurko, Andrew M. ^[1]; Logsdon, John M. ^[1]; Eads, Brian D. ^[2]

Univ. of Iowa, Iowa City, IA (United States). Dept. of Biology. Roy J. Carver Center for Comparative Genomics
Indiana Univ., Bloomington, IN (United States). Dept. of Biology. The Center forGenomics and Bioinformatics

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.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Univ. of California, San Diego, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC02-05CH11231; W-7405-ENG-36; W-7405-ENG-48

OSTI ID:: 1626385

Journal Information:: BMC Evolutionary Biology (Online), Vol. 9, Issue 1; ISSN 1471-2148

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

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Meiosis-Specific DNA Double-Strand Breaks Are Catalyzed by Spo11, a Member of a Widely Conserved Protein Family Keeney, Scott; Giroux, Craig N.; Kleckner, Nancy Cell, Vol. 88, Issue 3 https://doi.org/10.1016/s0092-8674(00)81876-0	journal	February 1997
Meiosis: polo, FEAR and the art of dividing reductionally Cohen-Fix, Orna Current Biology, Vol. 13, Issue 15 https://doi.org/10.1016/s0960-9822(03)00526-8	journal	August 2003
The Rad51 and Dmc1 recombinases: a non-identical twin relationship Masson, Jean-Yves; West, Stephen C. Trends in Biochemical Sciences, Vol. 26, Issue 2 https://doi.org/10.1016/s0968-0004(00)01742-4	journal	February 2001
The Hop2 Protein Has a Direct Role in Promoting Interhomolog Interactions during Mouse Meiosis Petukhova, Galina V.; Romanienko, Peter J.; Camerini-Otero, R. Daniel Developmental Cell, Vol. 5, Issue 6 https://doi.org/10.1016/s1534-5807(03)00369-1	journal	December 2003
Sister chromatid cohesion: the cohesin cleavage model does not ring true Guacci, Vincent Genes to Cells, Vol. 0, Issue 0 https://doi.org/10.1111/j.1365-2443.2007.01093.x	journal	June 2007
Novel Meiosis-Specific Isoform of Mammalian SMC1 Revenkova, E.; Eijpe, M.; Heyting, C. Molecular and Cellular Biology, Vol. 21, Issue 20 https://doi.org/10.1128/mcb.21.20.6984-6998.2001	journal	October 2001
Differential Contributions of Mammalian Rad54 Paralogs to Recombination, DNA Damage Repair, and Meiosis Wesoly, Joanna; Agarwal, Sheba; Sigurdsson, Stefan Molecular and Cellular Biology, Vol. 26, Issue 3 https://doi.org/10.1128/mcb.26.3.976-989.2006	journal	February 2006
Eukaryotic MCM Proteins: Beyond Replication Initiation Forsburg, S. L. Microbiology and Molecular Biology Reviews, Vol. 68, Issue 1 https://doi.org/10.1128/mmbr.68.1.109-131.2004	journal	March 2004
Expression of the MutL Homologue hMLH3 in Human Cells and its Role in DNA Mismatch Repair Cannavo, Elda; Marra, Giancarlo; Sabates-Bellver, Jacob Cancer Research, Vol. 65, Issue 23 https://doi.org/10.1158/0008-5472.can-05-2528	journal	December 2005
MicroRNA-25 Exerts an Oncogenic Function by Regulating the Ubiquitin Ligase Fbxw7 in Hepatocellular Carcinoma El-mezayen, Hatem; Yamamura, Kensuke; Yusa, Toshihiko Annals of Surgical Oncology, Vol. 28, Issue 12 https://doi.org/10.1245/s10434-021-09778-2	journal	April 2021

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Abortive meiosis in the oogenesis of parthenogenetic Daphnia pulex Hiruta, Chizue; Nishida, Chizuko; Tochinai, Shin Chromosome Research, Vol. 18, Issue 7 https://doi.org/10.1007/s10577-010-9159-2	journal	October 2010
Daphnia as an Emerging Epigenetic Model Organism Harris, Kami D. M.; Bartlett, Nicholas J.; Lloyd, Vett K. Genetics Research International, Vol. 2012 https://doi.org/10.1155/2012/147892	journal	January 2012
Targeted gene disruption by use of CRISPR/Cas9 ribonucleoprotein complexes in the water flea Daphnia pulex Hiruta, Chizue; Kakui, Keiichi; Tollefsen, Knut E. Genes to Cells, Vol. 23, Issue 6 https://doi.org/10.1111/gtc.12589	journal	May 2018
The evolution of meiotic sex and its alternatives Mirzaghaderi, Ghader; Hörandl, Elvira Proceedings of the Royal Society B: Biological Sciences, Vol. 283, Issue 1838 https://doi.org/10.1098/rspb.2016.1221	journal	September 2016
The water flea Daphnia - a 'new' model system for ecology and evolution? Stollewerk, Angelika Journal of Biology, Vol. 9, Issue 2 https://doi.org/10.1186/jbiol212	journal	January 2010
Sex in crowded places: population density regulates reproductive strategy Haltiner, Linda; Hänggi, Corinne; Spaak, Piet Hydrobiologia, Vol. 847, Issue 7 https://doi.org/10.1007/s10750-019-04143-7	journal	December 2019
Clonal expansion behind a marine diatom bloom Ruggiero, Maria Valeria; D'Alelio, Domenico; Ferrante, Maria Immacolata The ISME Journal, Vol. 12, Issue 2 https://doi.org/10.1038/ismej.2017.181	journal	November 2017
Identification of the meiotic toolkit in diatoms and exploration of meiosis-specific SPO11 and RAD51 homologs in the sexual species Pseudo-nitzschia multistriata and Seminavis robusta Patil, Shrikant; Moeys, Sara; von Dassow, Peter BMC Genomics, Vol. 16, Issue 1 https://doi.org/10.1186/s12864-015-1983-5	journal	November 2015
Male meiosis in Crustacea: synapsis, recombination, epigenetics and fertility in Daphnia magna Gómez, Rocío; Van Damme, Kay; Gosálvez, Jaime Chromosoma, Vol. 125, Issue 4 https://doi.org/10.1007/s00412-015-0558-1	journal	December 2015
The boule gene is essential for spermatogenesis of haploid insect male Sekiné, Kazuki; Furusawa, Tadashi; Hatakeyama, Masatsugu Developmental Biology, Vol. 399, Issue 1 https://doi.org/10.1016/j.ydbio.2014.12.027	journal	March 2015
The Epigenetic Repertoire of Daphnia magna Includes Modified Histones Robichaud, Nicole F.; Sassine, Jeanette; Beaton, Margaret J. Genetics Research International, Vol. 2012 https://doi.org/10.1155/2012/174860	journal	January 2012
Evolutionary study of duplications of the miRNA machinery in aphids associated with striking rate acceleration and changes in expression profiles Ortiz-Rivas, Benjamín; Jaubert-Possamai, Stéphanie; Tanguy, Sylvie BMC Evolutionary Biology, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2148-12-216	journal	November 2012
Not just another genome Tautz, Diethard BMC Biology, Vol. 9, Issue 1 https://doi.org/10.1186/1741-7007-9-8	journal	February 2011
Expansion of Genes Encoding piRNA-Associated Argonaute Proteins in the Pea Aphid: Diversification of Expression Profiles in Different Plastic Morphs Lu, Hsiao-ling; Tanguy, Sylvie; Rispe, Claude PLoS ONE, Vol. 6, Issue 12 https://doi.org/10.1371/journal.pone.0028051	journal	December 2011
Gene Expression Analysis of Parthenogenetic Embryonic Development of the Pea Aphid, Acyrthosiphon pisum, Suggests That Aphid Parthenogenesis Evolved from Meiotic Oogenesis Srinivasan, Dayalan G.; Abdelhady, Ahmed; Stern, David L. PLoS ONE, Vol. 9, Issue 12 https://doi.org/10.1371/journal.pone.0115099	journal	December 2014

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