SREL Reprint #2127

 

 

 

Tissue-specific maternal and paternal mitochondrial DNA in the freshwater mussel, Anodonta grandis grandis

Hsiu-Ping Liu, Jeffry B. Mitton*

Savannah River Ecology Laboratory University of Georgia Drawer E
Aiken, SC 29802TEL: (803) 725-7095Email: liu@srel.edu


* Department of Environmental, Population, and Organismic Biology
University of Colorado Campus Box 334 Boulder, CO 80309
TEL: (303) 492-8956 Email: mitton@spot.colorado.edu

 


Until recently, inheritance of mitochondrial DNA (mtDNA) in animals was thought to be strictly maternal. Evidence for incidental paternal mtDNA leakage was obtained in hybrid crosses of mice1 and Drosophila2,3. An unusual pattern of mtDNA inheritance, i.e. double uniparental inheritance, was described in the blue mussel, Mytilus edulis4,5, and in the giant floater, Anodonta grandis grandis6. Here we report the distribution of maternal and paternal mitochondrial DNA in the giant floater, which differ from those in the blue mussel.
In the mode of double uniparental inheritance of the blue mussel, the transmission of mitochondrial types depends upon the sex. Females offspring receive predominantly maternal mtDNA and transmit the maternal type mtDNA into eggs, while males receive both maternal and paternal mtDNA and preferentially package the paternal type mtDNA into sperm. Heteroplasmy of the maternal and paternal mtDNA is commonly found in the somatic tissues of the male blue mussels5,7,8,9,10. Liu and associates did not examine somatic tissue6 and it is not known whether heteroplasmy is also a common phenomenon in male giant floater.
To determine the distribution of mitochondrial types, eight giant floaters (six males, two females) were collected from Flagler Reservoir (T9S, R50W, sections 4/5/8/9) at Kit Carson County, Colorado. Total DNA was extracted from gonadal tissue and from mantle tissue for each individual6. Five restriction enzymes, AseI, EcoRI, HaeIII, HindIII, and HinfI were used to digest the total DNA. Mitochondrial DNA fragments were detected and scored as described in Liu et al6.
For all five mtDNA restriction fragment patterns, female mussels exhibited only the maternal type mtDNA in both gonadal and somatic tissues (Figure 1). Male mussels showed predominantly the paternal type mtDNA in the gonadal tissue, but only the maternal type mtDNA in the somatic tissues (Figure 1).
Males gave a weak signal of the maternal type mtDNA in the gonadal tissue. This phenomenon was also observed in the blue mussel4. Skibinski et al. suggested that maternal type mtDNA might occasionally leak into the paternal mtDNA inheritance system. However, the weak maternal type mtDNA signal in the gonadal tissue of males might be from the surrounding somatic tissue of the gonad, and does not necessarily indicate that maternal type mtDNA are packaged into sperm.
In the blue mussel, zygotes contain approximately 104 mitochondria contributed by the egg11 and approximately five copies of mitochondria contributed by the sperm12. As males develop and grow, the paternal type mtDNA becomes codominant with the maternal type mtDNA in the somatic tissue. If the paternal type mtDNA is in females, it can not be detected by the usual detection methods4. In contrast, the maternal type is the only type of mtDNA in the somatic tissues of both males and females in the giant floater. The contrasting results suggest that the regulation of replication of mitochondria differs between the blue mussel and the giant floater.
The analysis of different tissues within individual animals is not usual in studies of mtDNA variation. Foot, mantle, adductor muscle are the tissues more commonly used in DNA analysis in bivalves7,13. If maternal type mtDNA is the predominant type mtDNA in the somatic tissues, as the giant floater, the detection of the double uniparental inheritance could be missed easily by using only somatic tissue in the DNA analysis. Thus the double uniparental inheritance might occur widely in bivalves, but may have been missed.
Acknowledgment
This work was supported by Research Grant in Malacology, and Walker Van Riper Award to H.-P. Liu. This manuscript was prepared under the contract number DE-AC09-76SROO-819 between the U.S. Department of Energy and the University of Georgia’s Savannah River Ecology Laboratory.

References
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4. Skibinski, D. O. F. et al. 1994. Nature, 368: 817-818.
5. Zouros, E. et al. 1994. Nature, 368: 818.
6. Liu, H.-P. et al. 1995. Evolution, in press.
7. Fisher, C. & Skibinski, D. O. F. 1990. Proc. R. Soc. Lond., B242: 149-156.
8. Hoeh, W. R. et al. 1990. Science, 251: 1488-1490.
9. Zouros, E. et al. 1992. Nature, 359: 412-414 (1992).
10. Zouros, E. et al. 1994. Proc. Natn. Acad. Sci. U.S.A., 91(16): 7463-7467.
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13. Banks, M. A. & Hedgecock, D. 1993. Mol. Mar. Biol. Biotech., 2(3): 129-136.

SREL Reprint #2127

Liu, H.-P. and J.B. Mitton. 1995. Tissue-specific maternal and paternal mitochondrial DNA in the freshwater mussel, Anodonta grandis grandis. The Journal of Molluscan Studies 62:393-394.

 

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