Mol. Biol. Evol. 15(5):611–612. 1998
1998 by the Society for Molecular Biology and Evolution. ISSN: 0737-4038
Letter to the Editor
L1 Repeat Is a Basic Unit of Heterochromatin Satellites in Cetaceans
Vladimir V. Kapitonov,* Gerald P. Holmquist,† and Jerzy Jurka*
*Genetic Information Research Institute, Palo Alto, California; and †Department of Biology, Beckman Institute of the City of
Hope, Duarte, California
. 1.—Alignment of dolphin satellite monomer and L1 consen-
sus sequence. The top sequence is the satellite monomer (GenBank
sequence M36451; opposite orientation) and the bottom sequence is
the L1MA9 consensus sequence (Smit et al. 1995) (positions 81–685;
RepBase Update: http://www.girinst.org). Numbering refers to satellite
sequence positions. Identical nucleotides are indicated by asterisks,
transversions by dots, transitions by colons, and alignment gaps by
Mammalian heterochromatin, pericentric, telomer-
ic, or intercalary, is usually composed of long arrays of
tandemly repeated DNA sequences called satellites,
which contribute up to 15%–30% of the entire genome.
Rapid divergence of heterochromatin satellites, some-
times between closely related species, raises the funda-
mental question of whether satellite monomers rapidly
evolve from the preexisting pool of satellites or some
of them are recruited from nonsatellite DNA. Previous
analyses of sequence periodicities indicate that alphoid
satellites might have evolved from smaller heptanucleo-
tide units (Zaitsev and Rogaev 1986), which suggests
continuous evolution of satellites from the preexisting
satellites. The alternative model is that individual sat-
ellite units can be recruited from a wide spectrum of
nonsatellite DNA and propagated into satellites by un-
equal crossing over (Smith 1976). This model is rooted
in the fact that no stringent functional requirements
seem to be imposed on individual satellite units, and
many DNA fragments, particularly abundant inter-
spersed repeats, should occasionally be expanded into
satellites. However, to date, no evidence of such events
has been recorded. In this correspondence, we report
that the so-called ‘‘common satellite’’ in cetaceans orig-
inated by ampliﬁcation of a DNA fragment which in-
cludes the L1 interspersed repetitive element (Boeke
The common cetacean satellites, constituting about
15% of all cetacean genomes, of both odontocetes
(toothed whales) and mysticetes (whalebone whales)
were ﬁrst used to prove a monophyletic origin of the
Cetacea at the DNA level (Arnason, Hoglund, and Wid-
egren 1984). These satellites are predominantly located
in most interstitial and terminal heterochromatin C-
bands. The monomeric repeat is
1,760 bp long in all
cetaceans except dolphins, where its length is
bp (Arnason, Gretarsdottir, and Widegren 1992; Gre-
tarsdottir and Arnason 1992). There is no reported sat-
ellite DNA similar to the common cetacean satellite in
other mammalian species.
We have found that a 540-bp DNA fragment of the
common cetacean satellite monomer is 63% similar to
-terminal portion of the mammalian L1 (LINE-1)
retrotransposon (ﬁgs. 1 and 2). This is also the ﬁrst se-
quence record of the L1 retroelement in the genome of
marine mammals. In addition to the nucleotide similar-
ity, we have found protein sequence similarity to the
Key words: LINE1 elements, retrotransposons and satellite DNA,
heterochromatin evolution, unequal crossing over, marine mammals.
Address for correspondence and reprints: Jerzy Jurka, Genetic In-
formation Research Institute, 440 Page Mill Road, Palo Alto, Califor-
nia 94306. E-mail: firstname.lastname@example.org.
beginning and end of the L1 ORF2-encoded protein se-
quence in mammals (ﬁg. 2). The distance between the
homologous patterns corresponds to the size of the basic
satellite unit (
1,580 bp). The most likely interpretation
of these facts is that the entire unit was derived from an
L1-ORF2 fragment which underwent extensive internal
deletions and other mutational events. Given the 80%
similarity between dolphin and whale satellites, it is rea-
sonable to assume a common origin of satellites in both
species from a rearranged L1 fragment.
Generally, infrequent insertions of retroelements
constitute only a tiny fraction of C-band-positive regions
of mammalian heterochromatin (Bickmore and Craif
1997, p. 164). Recently, the presence of separate clusters
612 Kapitonov et al.
. 2—Schematic structure of the dolphin satellite DNA from heterochromatin C-bands. The satellite monomer is represented by an arrow
(GenBank accession number M36451; opposite orientation). The 3
region of the monomer (540 bp; gray in the ﬁgure) is 63% similar at the
nucleotide level to the mammalian L1 non-LTR retrotransposon, L1MA9 subfamily. The hatched areas indicate signiﬁcant protein similarity to
the L1 ORF2 protein (PIR accession number S65824; BLASTX P value is 10
of retrotransposons in invertebrate and plant alpha-het-
erochromatin has been reported (Carmena and Gonzalez
1995; Pimpinelli et al. 1995; Pearce et al. 1996; Terri-
noni et al. 1997). It has been proposed that they could
be stable structural components of heterochromatin
(Pimpinelli et al. 1995) or telomeric elements partici-
pating in the compensation of the systematic chromo-
some shortening (Pardue et al. 1996). However, as in-
dicated before (Lohe and Hilliker 1995), there are no
reported data demonstrating that retroelements may
serve as the basic core of satellite monomers, and there
are no reported relationships between retrotransposons
and heterochromatin satellite formation.
The major aspect of our ﬁnding is that it revives
the Smith (1976) mechanism of unequal crossing over,
which predicts that if an individual sequence of the sat-
ellite monomer is to some extent arbitrary, then common
interspersed repeats should occasionally be found ﬁxed
in alpha-heterochromatin. Since none were found before
our ﬁnding, this prediction lacked evidence, and the role
of the Smith mechanism in satellite evolution remained
We thank anonymous reviewers for their useful
suggestions. This work was supported by grant P41
LM06252 from the National Institutes of Health.
, U., S. G
, and B. W
Mysticete (baleen whale) relationships based upon the se-
quence of the common cetacean DNA satellite. Mol. Biol.
, U., M. H
, and B. W
. 1984. Con-
servation of highly repetitive DNA in cetaceans. Chromo-
, W., and G. C
. 1997. Chromosome bands: pat-
terns in the genome. R. G. Landes, Austin, Tex.
, J. D. 1997. LINEs and Alus—the polyA connection.
Nat. Genet. 16:6–7.
, M., and C. G
. 1995. Transposable elements
map in a conserved pattern of distribution extending from
beta-heterochromatin to centromeres in Drosophila mela-
nogaster. Chromosoma 103:676–684.
, S., and U. A
. 1992. Evolution of the
common cetacean highly repetitive DNA component and
the systematic position of Orcaella brevirostris. J. Mol.
, A. R., and A. J. H
. 1995. Return of the H-word
(heterochromatin). Curr. Opin. Genet. Dev. 5:746–755.
, M. L., O. N. D
, and K. L. T
. 1996. Drosophila telomeres:
new views on chromosome evolution. Trends Genet. 12:48–
, S. R., U. P
, and A. K
. 1996. The
Ty 1-copia group retrotransposons of Allium cepa are dis-
tributed throughout the chromosomes but are enriched in
the terminal heterochromatin. Chromosome Res. 4:357–
, S., M. B
, and M.
. 1995. Transposable elements are stable structural
components of Drosophila melanogaster heterochromatin.
Proc. Natl. Acad. Sci. USA 92:3804–3808.
, A. F. A., G. T
, and J. J
Ancestral, mammalian-wide subfamilies of LINE-1 repeti-
tive sequences. J. Mol. Biol. 246:401–417.
, G. P. 1976. Evolution of repeated DNA sequences by
unequal crossover. Science 191:528–535.
, A., C. D
, and N. J
1997. Intragenomic distribution and stability of transposable
elements in euchromatin and heterochromatin of Drosoph-
ila melanogaster: non-LTR retrotransposon. J. Mol. Evol.
, I. Z., and E. I. R
. 1986. Structural analysis of
alphoid DNA of primates. I. Heterogeneity of nucleotide
sequence of alphoid repeats in human DNA. Mol. Biol.
, reviewing editor
Accepted January 16, 1998