Enrichment of a LINE subfamily in a single chromosomal region
in Peromyscus
David H. Kass,
1
John A. Peppers,
2
Mary Maltbie,
2
Robert J. Baker
2
1
Department of Biology, Eastern Michigan University, Ypsilanti, Michigan 48197, USA
2
Department of Biological Sciences, Texas Tech University, Lubbock, Texas 79409, USA
Received: 15 December 1997 / Accepted: 20 February 1998
LINEs are a class of transposable elements greater than 5 kb
in length consisting of 10
4
–10
5
copies, most of which are hetero-
geneously 5' truncated (Voliva et al. 1983). These elements are
not randomly inserted in the genome, and generally correspond
to the A-T rich chromosomal G bands, as well as accumulate
on the sex chromosomes, as observed in the human (Koren-
berg and Rykowski 1988), European house mouse (Boyle et al.
1990), and deer mouse (Wichman et al. 1992; Baker and Kass
1994).
Sequence analysis of L1 elements suggests few original source
or master genes generated the numerous L1 elements (Deininger et
al. 1992). As mutations accumulate in the master gene, the more
recently diverged species would share these mutations and yield
concerted variations and hence subfamilies. LINE subfamilies
have been described by restriction endonuclease cleavage patterns
(Jubier-Maurin et al. 1985; Kass et al. 1992), sequences of 5'
motifs (Padgett et al. 1988), diagnostic nucleotides (Jurka 1989),
and stretches of sequence variability within an open reading frame
(ORF; Pascale et al. 1990; Kass et al. 1992). Two highly divergent
LINE (L1) subfamilies (L1Pm62 and L1Pm55) have been identi-
fied that coexist in the genomes of Peromyscus, exhibiting differ-
ing restriction fragment length variants (RFLVs) on Southern blots
with DNA isolated from various Peromyscus species (Kass et al.
1992). Sequences of the elements (subcloned L1-hybridizing frag-
ments from a P. maniculatus genomic library) representing these
subfamilies demonstrate 29% divergence from each other within
ORF-2, which is unusually high for intraspecific LINEs compared
with mice and rats (Martin et al. 1985; Soares et al. 1985). Com-
parisons of second and third position nucleotides by codon align-
ment between L1Pm62 and L1Pm55 support the view that these
subfamilies were derived from different source genes (Kass et al.
1992). A comparative sequence analysis of several Peromyscus
LINEs depicts L1Pm62 and L1Pm55 as relatively ‘‘old’’, predat-
ing the divergence of two recent LINE-1 lineages (Casavant et al.
1996). The lack of a conserved ORF additionally supports the
ancient origin of the L1-62 and L1-55 subfamilies (Kass et al.
1992) and is indicative of retropositional inactivity during the
course of speciation within this genus. However, the maintenance
of conserved restriction sites that follow phylogenetic trends (Kass
et al. 1992) suggests these subfamilies have more recent evolu-
tionary histories.
L1Pm55 appeared to be the oldest sequence of elements iso-
lated from P. maniculatus and branches as an off-shoot from
the other Peromyscus L1 sequences from a derived molecular
phylogeny (Casavant et al. 1996). L1Pm55 was estimated at
100 copies per haploid genome by a genomic Southern blot (Kass
et al. 1992), representing less than 1% of total LINE repeats.
The same blot demonstrated a less intense EcoRI fragment in
species of the P. leucopus (0.7 kb) and P. truei (1.7 kb) species
groups, indicative of fewer copies or high sequence divergence.
The use of alternative restriction enzymes for Southern blots also
demonstrated concerted variations, primarily at the species group
level, always with a more intense band in species of the P. manicu-
latus species group. Surprisingly, this suggests a more recent ori-
gin of this apparently retropositionally inactive subfamily. We
therefore elected to analyze the chromosomal organization of
L1Pm55 to gain insight into the evolutionary history of this enig-
matic subfamily.
Fluorescence in situ hybridization (FISH) as previously de-
scribed (Wichman et al. 1992; Baker and Kass 1994) was used to
analyze chromosomes of P. leucopus, P. maniculatus, and P. mela-
notis. The L1 hybridizing probe (pDK55) is a 1.5-kb fragment
subcloned from a P. maniculatus genomic library (Kass et al.
1992). Although two small regions within pDK55 (80 bp and a
27-bp GC-rich region) are not observed in L1Pm62 or L1 se-
quences from other mammals (Kass et al. 1992), it is highly im-
probable that the observed FISH patterns are due to homologies to
these short DNA stretches. A BLAST search of the database
(Altschul et al. 1990) identified no corresponding sequences to the
27-bp region. Various sequences located on different mouse and
human chromosomes were identified that corresponded to the 80-
bp region, and any significant sequence identities (80%) that were
observed included only various 20-bp stretches of this region. One
microgram of the clone (plasmid plus insert) was biotinylated by
nick translation, and the pDK55 probe was hybridized in the pres-
ence of sheared E. coli DNA. Hybridization under the conditions
used (Baker and Kass 1994) should detect sequences greater than
70% in similarity. The hybridized probes were detected with fluo-
rescein-conjugated avidin (Vector Labs), followed by two ampli-
fications consisting of alternate treatments of biotinylated goat
anti-avidin (Vector Labs). Digital enhancement of images and
pseudo-G banding were accomplished by using software from On-
cor Images. Repeated hybridizations for each species confirmed
the results.
The L1-55 subfamily is primarily located on a single pair of
homologous chromosomes (Fig. 1) within P. maniculatus and P.
melanotis, both of the P. maniculatus species group, and in P.
leucopus. The distinguishable FISH pattern in P. leucopus further
supports the subfamily classification of L1-55, as opposed to one
or a few aberrant element(s) strictly within the P. maniculatus
genome. The accompanying pseudo-G band spreads support the
existence of this subfamily on the same chromosome in these
species. The use of P. melanotis further denotes Chr 12 as the
residence for L1-55, based on G banding patterns (Committee for
the Standardization of Chromosomes of Peromyscus, 1994). L1-55
had not been observed by FISH in P. eremicus (data not shown),
a member of a separate subgenus (Haplomyomys) of Peromyscus,
either as a consequence of the level of divergence, low copy num-
ber, or its absence.
Several mechanisms for the non-random chromosomal ar- Correspondence to: D.H. Kass
Mammalian Genome 9, 488–490 (1998).
© Springer-Verlag New York Inc. 1998
Incorporating Mouse Genome