Literature DB >> 9093859

Male-dependent doubly uniparental inheritance of mitochondrial DNA and female-dependent sex-ratio in the mussel Mytilus galloprovincialis.

C Saavedra1, M I Reyero, E Zouros.   

Abstract

We have investigated sex ratio and mitochondrial DNA inheritance in pair-matings involving five female and five male individuals of the Mediterranean mussel Mytilus galloprovincialis. The percentage of male progeny varied widely among families and was found to be a characteristic of the female parent and independent of the male to which it was mated. Thus sex-ratio in Mytilus appears to be independent of the nuclear genotype of the sperm. With a few exceptions, doubly uniparental inheritance (DUI) of mtDNA was observed in all families fathered by four of the five males: female and male progeny contained the mother's mtDNA (the F genome), but males contained also the father's paternal mtDNA (the M genome). Two hermaphrodite individuals found among the progeny of these crosses contained the F mitochondrial genome in the female gonad and both the F and M genomes in the male gonad. All four families fathered by the fifth male showed the standard maternal inheritance (SMI) of animal mtDNA: both female and male progeny contained only the maternal mtDNA. These observations illustrate the intimate linkage between sex and mtDNA inheritance in species with DUI and suggest different major roles for each gender. We propose a model according to which development of a male gonad requires the presence in the early germ cells of an agent associated with sperm-derived mitochondria, these mitochondria are endowed with a paternally encoded replicative advantage through which they overcome their original minority in the fertilized egg and this advantage (and, therefore, the chance of an early entrance into the germ line) is countered by a maternally encoded egg factor.

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Year:  1997        PMID: 9093859      PMCID: PMC1207877     

Source DB:  PubMed          Journal:  Genetics        ISSN: 0016-6731            Impact factor:   4.562


  11 in total

1.  Paternal inheritance of mitochondrial DNA in mice.

Authors:  U Gyllensten; D Wharton; A Josefsson; A C Wilson
Journal:  Nature       Date:  1991-07-18       Impact factor: 49.962

2.  Degree of selective constraint as an explanation of the different rates of evolution of gender-specific mitochondrial DNA lineages in the mussel mytilus.

Authors:  D T Stewart; E R Kenchington; R K Singh; E Zouros
Journal:  Genetics       Date:  1996-07       Impact factor: 4.562

3.  Heteroplasmy suggests limited biparental inheritance of Mytilus mitochondrial DNA.

Authors:  W R Hoeh; K H Blakley; W M Brown
Journal:  Science       Date:  1991-03-22       Impact factor: 47.728

Review 4.  Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution.

Authors:  C W Birky
Journal:  Proc Natl Acad Sci U S A       Date:  1995-12-05       Impact factor: 11.205

5.  An unusual type of mitochondrial DNA inheritance in the blue mussel Mytilus.

Authors:  E Zouros; A Oberhauser Ball; C Saavedra; K R Freeman
Journal:  Proc Natl Acad Sci U S A       Date:  1994-08-02       Impact factor: 11.205

6.  Incomplete maternal transmission of mitochondrial DNA in Drosophila.

Authors:  R Kondo; Y Satta; E T Matsuura; H Ishiwa; N Takahata; S I Chigusa
Journal:  Genetics       Date:  1990-11       Impact factor: 4.562

7.  Male and female mitochondrial DNA lineages in the blue mussel (Mytilus edulis) species group.

Authors:  D T Stewart; C Saavedra; R R Stanwood; A O Ball; E Zouros
Journal:  Mol Biol Evol       Date:  1995-09       Impact factor: 16.240

8.  Evolutionary relationships among the male and female mitochondrial DNA lineages in the Mytilus edulis species complex.

Authors:  P D Rawson; T J Hilbish
Journal:  Mol Biol Evol       Date:  1995-09       Impact factor: 16.240

9.  Elimination of paternal mitochondrial DNA in intraspecific crosses during early mouse embryogenesis.

Authors:  H Kaneda; J Hayashi; S Takahama; C Taya; K F Lindahl; H Yonekawa
Journal:  Proc Natl Acad Sci U S A       Date:  1995-05-09       Impact factor: 11.205

10.  A novel mitochondrial genome organization for the blue mussel, Mytilus edulis.

Authors:  R J Hoffmann; J L Boore; W M Brown
Journal:  Genetics       Date:  1992-06       Impact factor: 4.562

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  35 in total

1.  Comparing relative rates of pollen and seed gene flow in the island model using nuclear and organelle measures of population structure.

Authors:  Matthew B Hamilton; Judith R Miller
Journal:  Genetics       Date:  2002-12       Impact factor: 4.562

2.  Heteroplasmy suggests paternal co-transmission of multiple genomes and pervasive reversion of maternally into paternally transmitted genomes of mussel (Mytilus) mitochondrial DNA.

Authors:  Humberto Quesada; Heiko Stuckas; David O F Skibinski
Journal:  J Mol Evol       Date:  2003       Impact factor: 2.395

3.  Novel protein genes in animal mtDNA: a new sex determination system in freshwater mussels (Bivalvia: Unionoida)?

Authors:  Sophie Breton; Donald T Stewart; Sally Shepardson; Richard J Trdan; Arthur E Bogan; Eric G Chapman; Andrew J Ruminas; Helen Piontkivska; Walter R Hoeh
Journal:  Mol Biol Evol       Date:  2010-12-20       Impact factor: 16.240

4.  Mitochondrial DNA Introgression in the European abalone Haliotis tuberculata tuberculata: evidence for experimental mtDNA paternal inheritance and a natural hybrid sequence.

Authors:  Alain Van Wormhoudt; Valérie Roussel; Gercende Courtois; Sylvain Huchette
Journal:  Mar Biotechnol (NY)       Date:  2010-10-12       Impact factor: 3.619

5.  Early replication dynamics of sex-linked mitochondrial DNAs in the doubly uniparental inheritance species Ruditapes philippinarum (Bivalvia Veneridae).

Authors:  D Guerra; F Ghiselli; L Milani; S Breton; M Passamonti
Journal:  Heredity (Edinb)       Date:  2015-12-02       Impact factor: 3.821

6.  Comparative analysis of gender-associated complete mitochondrial genomes in marine mussels (Mytilus spp.).

Authors:  Sophie Breton; Gertraud Burger; Donald T Stewart; Pierre U Blier
Journal:  Genetics       Date:  2005-12-01       Impact factor: 4.562

7.  Evolution of a unique mitotype-specific protein-coding extension of the cytochrome c oxidase II gene in freshwater mussels (Bivalvia: Unionoida).

Authors:  Jason P Curole; Thomas D Kocher
Journal:  J Mol Evol       Date:  2005-07-28       Impact factor: 2.395

8.  No evidence for presence of maternal mitochondrial DNA in the sperm of Mytilus galloprovincialis males.

Authors:  Constantinos Venetis; Ioannis Theologidis; Eleftherios Zouros; George C Rodakis
Journal:  Proc Biol Sci       Date:  2006-10-07       Impact factor: 5.349

9.  Nuclear sex-determining genes cause large sex-ratio variation in the apple snail Pomacea canaliculata.

Authors:  Yoichi Yusa
Journal:  Genetics       Date:  2006-10-22       Impact factor: 4.562

10.  No evidence for absence of paternal mtDNA in male progeny from pair matings of the mussel Mytilus galloprovincialis.

Authors:  Ioannis Theologidis; Carlos Saavedra; Eleftherios Zouros
Journal:  Genetics       Date:  2007-04-15       Impact factor: 4.562

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