A mapping and evolutionary study of porcine sex chromosome genes
Claire R. Quilter,
Sarah C. Blott,
Alan J. Mileham,
Nabeel A. Aara,
Carole A. Sargent,
Darren K. Grin
Human Molecular Genetics Group, University of Cambridge, Department of Pathology, Tennis Court Road, Cambridge CB2 1QP, UK
Brunel University, Department of Biological Sciences, Uxbridge, Middlesex, UB8 3PH, UK
Sygen International, 2929 7
Street, Suite 130, Berkeley, California 94710, USA
Received: 18 April 2002 / Accepted: 10 July 2002
Abstract. A combination of FISH and RH mapping was used
to study the evolution of sex chromosome genes in the pig. In
total, 19 genes were identi®ed, including 3 PAR genes (STS,
KAL, PRK). The gene order of the porcine X Chromosome
(Chr) closely resembled the human X Chr (PRK/STS/KAL±
that the porcine X has undergone very little rearrangement
during evolution. For the porcine Y Chr, two linkage groups
of 10 NRY genes were found, and the following order was
UTY)±(TSPY±SMCY±UBE1Y±SRY)±CEN. This gene order
showed greater conservation with the murine Y than with the
human Y Chr. In addition, all porcine Y Chr genes mapped to
Yp, which is similar to the mouse and included EIF2s3Y and
UBE1Y, which are not present in humans. Interestingly,
complete conservation of X/Y homologous gene order was
found between the pig X and Y Chrs, indicating that the
porcine Y Chr has not undergone extensive reorganisation
with respect to the X. This suggests that the order of the
X/Y homologous genes of the porcine X and Y Chrs may
closely resemble the ancestral gene order of the eutherian sex
The majority of mammals have an X-Y chromosomal sex-
determining system. Recombination between the sex chromo-
somes occurs only at the pseudoautosomal region (PAR),
which may account for loss of function of Y Chr genes and
eventual Y Chr degradation (Graves 1995; Charlesworth
1996). The genes on the non-recombining region of the Y Chr
(NRY) fall into two categories: the former are X-Y homolo-
gous and are postulated to have evolved in order to maintain
comparable expression of housekeeping functions in males and
females, and the latter are Y-speci®c genes, which are generally
expressed in the testis and are thought to have survived on the
Y Chr by acquiring a function in male fertility (Lahn and Page
Investigations of the genes found on the sex chromosomes
are of interest with regard to the study of chromosome evo-
lution. Comparative mapping and painting studies between
humans and their most distant mammalian relatives, marsu-
pials and monotremes, have been carried out to establish
whether there is conservation of gene order between species.
These studies have shown that the eutherian X Chr can be
divided into a conserved region (XCR), consisting of the q arm
and proximal Xp, and a more recently added region (XAR)
distal to Xp11.23. XAR maps to at least two autosomal clus-
ters in marsupials and monotremes (Graves 1995, 1998).
Overall, these studies suggest that the eutherian X Chr is
conserved between species, particularly the pericentric region
and the q arm. However, this does not appear to be the case
for all taxa, as it has been shown that there is some rear-
rangement of X chromosome genes relative to the human X,
for cattle, goats, and sheep (Piumi et al. 1998; Robinson et al.
1998; Iannuzzi et al. 2000; Cribiu et al. 2001). Loci present on
the mouse X Chr have also undergone rearrangement com-
pared with the human X (Carver and Stubbs 1997).
Evolution of the Y Chr is more complicated, but it appears
to consist mainly of recently added regions (YAR) (Waters
et al. 2001). It has been shown that genes from YAR map to
the same autosomal location in marsupials as many genes from
the XAR. This suggests that an ancestral gene cluster has been
added to the sex chromosomes during the eutherian lineage
(Graves 1995, 1998; Waters et al. 2001). Only four genes are
common to marsupials and humans, representing two small Y
conserved regions (YCR): SRY and RPS4Y, which map to
human Yp close to the PAR and SMCY and RBMY, the
major copy of which map to Yq close to the heterochromatic,
block (Foster et al. 1992; Delbridge et al. 1997; Jegalian and
Page 1998; Agulnik et al. 1994; Waters et al. 2001).
Overall, the eutherian Y Chr appears to have undergone
extensive reorganization during evolution. However, a com-
prehensive study by Murphy et al. (1999) found a remarkably
conserved locus order between human and cat, which indicates
that this is not always the case. In mice, although the gene
order is largely dierent from the human Y Chr, USP9Y,
DBY, and UTY are closely linked in both (Mazeyrat et al.
1998; Aara and Mitchell 2000).
Previous studies of X and Y Chr genes therefore suggest
that the conservation of the sex chromosome genes may war-
rant further investigation for dierent mammalian orders. In
this study, we investigated Y Chr genes in the pig and some of
their X Chr homologs. The only known loci to date that have
been physically mapped to a porcine Y chromosomal arm are
SRY, the sex-determining gene, to Yp1.2-1.3 by ISH (Yang
et al. 1993), and DYZ1, a heterochromatic repeat, to the whole
of the q arm by FISH (Thomsen et al. 1992). Other genes have
been inferred to have Y copies through studies involving zoo
blots: TSPY (Jakubiczka et al. 1993); SMCY (Agulnik et al.
1994); RBMY (Ma et al. 1993); UBE1Y (Mitchell et al. 1991);
USP9Y, DBY, UTY, EIF1AY (Mazeyrat et al. 1998); EIF2s3Y
(Ehrmann et al. 1998). The porcine X has been shown to have
a high degree of synteny with the human X Chr from gene
mapping and chromosome painting studies (Fronicke et al.
1996). This is rearmed by the fact that it has a G-banding
pattern similar to the human X.
Mammalian Genome 13, 588±594 (2002).
DOI: 10.1007/s00335-002-3026 -1
The nucleotide sequence data reported in this paper have been sub-
mitted to EMBL and have been assigned the accession numbers
AJ437581, AJ437582, AJ437583 and AJ437584.
Correspondence to: C. Quilter; E-mail: firstname.lastname@example.org.