Mitochondrial DNA misinformation

Jim Cummins cummins at possum.murdoch.edu.au
Tue Oct 3 19:38:27 EST 1995


Margaret Martens <dr._margaret_martens at FTDETRCK-CCMAIL.ARMY.MIL> wrote:


> Article: bionet.cellbiol.2053
> Message-ID: <9509028126.AA812656527 at ftdetrck-ccmail.army.mil>
> From: dr._margaret_martens at FTDETRCK-CCMAIL.ARMY.MIL
> Date: 2 Oct 1995 12:19:05 -0700

>       Mitochondria themselves come from your mother because during
>       fertilization the only thing that the sperm contributes to the embryo
>       is its DNA.  The egg donates all other structures including
>       mitochondria, which replicate by division.  Thus, initially all the
>       mitochondria come from the mother.  However, as mitochondrial proteins
>       are encoded by both nuclear and mitochondrial DNA, defects in
>       mitochondrial structure/function can be inherited via the classical
>       Mendelian pattern of inheritance (mutation in nuclear genes) or
>       maternally (mutation in mitochondrial genes).

Sorry, this is just plain wrong, yet it persists in many texts.  Sperm definitely carry mitochondria into the egg.  There is a low albeit measurable level of paternal inheritance on mt DNA.  One of Allan Wilson's last papers actually measured the rate of paternal inheritance of mitochondria in lab mice,
and found it to be around 10^-4 (Nature 352: 255-257 1991).

 In some organisms (eg conifers) paternal inheritance is the rule.

Typical published misinformation is as follows:

"At fertilization the mother's egg contains many mitochondria (and lots of
mtDNA) while the father's sperm dos not contribute its mitochondria to the
embryo presumably leaving them behind in its discarded tail"  Pat Shipman
"The Evolution of Racism" Simon and Schuster NY 1994 p269.

And, even accompanied by a cartoon showing the "discarded" sperm tail,  from
Roger Lewin (who surely must know better!) we get the following:

"..when the sperm fertilizes the egg, it leves behind all its mitochondria:
the developing fetus therefore inherits mitochondria only from the mother's
egg"

Lewin R "Human Evolution" 1993 Blackwell p 155

Now leaving aside the African Eve polemics, this is just plain WRONG.  The
only mammal in which I'm aware the sperm tail gets excluded (because of its
size) is the Chinese Hamster.  In all others that have been studied
(including human embryos) the tail including centriole and mitochondria are
indeed incorporated and can be indentified for several cleavage stages.
Indeed in ICSI for male infertility we deliberately inject the whole sperm into the oocyte.

The reasons for maternal inheritance of mtDNA are complex and,
incidentally, *not* universal-there are several exceptions including
Conifers and mussels.  However it is not because of exclusion of
mitochondria.   There may be dilution effects, destruction of the midpiece
or inactivation of mtDNA and at last count the jury's out on the real mechanism.  The bottom line is that there always remains the possibility of
slow "leakage" of paternal mtDNA, and any hypothesis of human origins must
take this slippage into account.  Hurst's paper goes into the possible
reasons for uniparental inheritance of cytoplasmic genes, and is a
wonderful comparative account.

References:-

Cummins, J.M., Fleming, A.D., Crozet, N., Kosower, N.S., Kuehl, T.J., and
Yanagimachi, R. (1986). Labelling of living mammalian spermatozoa with the
fluorescent thiol alkylating agent, Monobromobimane (MB):  fate of labelled
sperm components in the embryo and developmental capacity. J Exp Zool.,
237, 383-390.

Hurst, L.D. (1992). Intragenomic conflict as an evolutionary force. Proc
Roy Soc Lond B., 248, 135-140.

Shalgi, R., Magnus, A., Jones, R., and Phillips, D.M. (1994). Fate of sperm
organelles during early embryogenesis in the rat. Mol Reprod Devel., 37,
264-271.

Simerly, C.R., Hecht, N.B., Goldberg, E., and Schatten, G. (1993). Tracing
the incorporation of the sperm tail in the mouse zygote and early embryo
using an anti-testicular alpha-tubulin antibody. Dev Biol., 158, 536-48.

Sathananthan, A.H. (1991). Inheritance of paternal centrioles and male
infertility. Singapore:

Sathananthan, A.H. (1992). Centriole behaviour during fertilization in
humans. Seattle, Washington:

Sathananthan, A.H., Kola, I., Osborne, J., Trounson, A.O., Ng, S.C.,
Bongso, A., and Ratnam, S.S. (1991). Centrioles in the beginning of human
development. Proc Natl Acad Sci, USA., 88, 4806-4810.


Jim Cummins, Associate Professor in Veterinary Anatomy,
Murdoch University, Western Australia 6150.
TEL +61-9-360 2668 FAX +61-9-310 4144
<cummins at possum.murdoch.edu.au>





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