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Molecular & Cellular Proteomics

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Proteomic Analysis of Eggs from Mytilus edulis Females Differing in Mitochondrial DNA Transmission Mode

Angel P. Diz, Edward Dudley, Andrew Cogswell, Barry W. MacDonald, Ellen L. R. Kenchington, Eleftherios Zouros and David O. F. Skibinski
Molecular & Cellular Proteomics November 1, 2013, First published on July 18, 2013, 12 (11) 3068-3080; https://doi.org/10.1074/mcp.M113.031401
Angel P. Diz
From the ‡Institute of Life Science, College of Medicine, Swansea University, Swansea SA28PP, Wales UK; §Department of Biochemistry, Genetics and Immunology, Faculty of Biology, University of Vigo, 36310, Vigo, Spain;
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Edward Dudley
From the ‡Institute of Life Science, College of Medicine, Swansea University, Swansea SA28PP, Wales UK;
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Andrew Cogswell
¶Bedford Institute of Oceanography, Ocean and Ecosystem Science Division, Department of Fisheries and Oceans, Dartmouth, NS, Canada B2Y 4A2;
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Barry W. MacDonald
¶Bedford Institute of Oceanography, Ocean and Ecosystem Science Division, Department of Fisheries and Oceans, Dartmouth, NS, Canada B2Y 4A2;
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Ellen L. R. Kenchington
¶Bedford Institute of Oceanography, Ocean and Ecosystem Science Division, Department of Fisheries and Oceans, Dartmouth, NS, Canada B2Y 4A2;
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Eleftherios Zouros
‖Department of Biology, University of Crete, Iraklion 71409, Crete, Greece
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David O. F. Skibinski
From the ‡Institute of Life Science, College of Medicine, Swansea University, Swansea SA28PP, Wales UK;
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  • For correspondence: d.o.f.skibinski@swansea.ac.uk
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Abstract

Many bivalves have an unusual mechanism of mitochondrial DNA (mtDNA) inheritance called doubly uniparental inheritance (DUI) in which distinctly different genomes are inherited through the female (F genome) and male (M genome) lineages. In fertilized eggs that will develop into male embryos, the sperm mitochondria remain in an aggregation, which is believed to be delivered to the primordial germ cells and passed to the next generation through the sperm. In fertilized eggs that will develop into female embryos, the sperm mitochondria are dispersed throughout the developing embryo and make little if any contribution to the next generation. The frequency of embryos with the aggregated or dispersed mitochondrial type varies among females. Previous models of DUI have predicted that maternal nuclear factors cause molecular differences among unfertilized eggs from females producing embryos with predominantly dispersed or aggregated mitochondria. We test this hypothesis using females of each of the two types from a natural population. We have found small, yet detectable, differences of the predicted type at the proteome level. We also provide evidence that eggs of females giving the dispersed pattern have consistently lower expression for different proteasome subunits than eggs of females giving the aggregated pattern. These results, combined with those of an earlier study in which we used hatchery lines of Mytilus, and with a transcriptomic study in a clam that has the DUI system of mtDNA transmission, reinforce the hypothesis that the ubiquitin-proteasome system plays a key role in the mechanism of DUI and sex determination in bivalves. We also report that eggs of females giving the dispersed pattern have higher expression for arginine kinase and enolase, enzymes involved in energy production, whereas ferritin, which is involved in iron homeostasis, has lower expression. We discuss these results in the context of genetic models for DUI and suggest experimental methods for further understanding the role of these proteins in DUI.

Footnotes

  • ↵* This work was supported by a Marine Genomics Europe Network grant (European Union FP6 Contract GOCE-CT-2004-505403) and a postdoctoral fellowship to A.P.D. The work is also supported by a project grant from Ministerio de Ciencia e Innovación and Fondos Feder (project code: BFU2011–22599) A.P.D is currently funded by an “Isidro Parga Pondal” fellowship and “Grupos de Referencia Competitiva”(2010/80) from Xunta de Galicia and Fondos Feder.

  • ↵Embedded Image This article contains supplemental Fig. S1 and Tables S1 and S2.

  • Received November 28, 2012.
  • Revision received June 3, 2013.
  • © 2013 by The American Society for Biochemistry and Molecular Biology, Inc.
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Proteomic Analysis of Eggs from Mytilus edulis Females Differing in Mitochondrial DNA Transmission Mode
Angel P. Diz, Edward Dudley, Andrew Cogswell, Barry W. MacDonald, Ellen L. R. Kenchington, Eleftherios Zouros, David O. F. Skibinski
Molecular & Cellular Proteomics November 1, 2013, First published on July 18, 2013, 12 (11) 3068-3080; DOI: 10.1074/mcp.M113.031401

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Proteomic Analysis of Eggs from Mytilus edulis Females Differing in Mitochondrial DNA Transmission Mode
Angel P. Diz, Edward Dudley, Andrew Cogswell, Barry W. MacDonald, Ellen L. R. Kenchington, Eleftherios Zouros, David O. F. Skibinski
Molecular & Cellular Proteomics November 1, 2013, First published on July 18, 2013, 12 (11) 3068-3080; DOI: 10.1074/mcp.M113.031401
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Molecular & Cellular Proteomics: 12 (11)
Molecular & Cellular Proteomics
Vol. 12, Issue 11
1 Nov 2013
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