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
Aiken, SC 29802TEL: (803) 725-7095Email: firstname.lastname@example.org
* Department of Environmental, Population, and
University of Colorado Campus Box 334 Boulder, CO 80309
TEL: (303) 492-8956 Email: email@example.com
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.
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
Georgias Savannah River Ecology Laboratory.
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3. Kondo, R. et al. 1992. Genet. Res., Camb., 59: 81-84.
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.,
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.,
11. Billett, F. S. 1979. Cambridge University Press, London.
12. Longo, F. J. & Dornfield, E. J. 1967. J. Ultra. Res., 20:
13. Banks, M. A. & Hedgecock, D. 1993. Mol. Mar. Biol.
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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.
To request a reprint