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Journal of Virology, February 2001, p. 2002-2009, Vol. 75, No. 4
0022-538X/01/$04.00+0 DOI: 10.1128/JVI.75.4.2002-2009.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Evolution and Characterization of Tetraonine Endogenous
Retrovirus: a New Virus Related to Avian Sarcoma and Leukosis
Viruses
Derek E.
Dimcheff,*
Mallika
Krishnan, and
David
P.
Mindell
Department of Biology and Museum of Zoology,
University of Michigan, Ann Arbor, Michigan 48109-1079
Received 7 August 2000/Accepted 9 November 2000
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ABSTRACT |
In a previous study, we found avian sarcoma and leukosis virus
(ASLV) gag genes in 19 species of birds in the order
Galliformes including all grouse and ptarmigan (Tetraoninae) surveyed.
Our data suggested that retroviruses had been transmitted horizontally among some host species. To further investigate these elements, we
sequenced a replication-defective retrovirus, here named tetraonine endogenous retrovirus (TERV), from Bonasa umbellus (ruffed
grouse). This is the first report of a complete, replication-defective ASLV provirus sequence from any bird other than the domestic chicken. We found a replication-defective proviral sequence consisting of
putative Gag and Env proteins flanked by long terminal repeats. Reverse
transcription-PCR analysis showed that retroviral gag sequences closely related to TERV are transcribed, supporting the
hypothesis that TERV is an active endogenous retrovirus. Phylogenetic analyses suggest that TERV may have arisen via recombination between different retroviral lineages infecting birds. Southern blotting using
gag probes showed that TERV occurs in tetraonines but not in chickens or ducks, suggesting that integration occurred after the
earliest phasianid divergences but prior to the radiation of tetraonine birds.
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TEXT |
Endogenous retroviruses have been
found in all vertebrate hosts examined. These viruses are integrated
into host genomes at multiple locations and are usually transmitted
vertically via the germline. The most extensively studied endogenous
avian retroviruses are found in the genome of the domestic chicken and
belong to the avian sarcoma and leukosis virus (ASLV), or
alpharetrovirus, genus. Endogenous ASLVs include Rous associated
virus-0 (RAV-0), endogenous avian retroviruses (EAVs), and avian
retrotransposons from chickens (ART-CH). RAV-0 is thought to represent
a recently integrated endogenous virus, because its provirus DNA
sequence is highly conserved relative to those of exogenous ASLVs such as Rous sarcoma virus (RSV). EAV-0 elements are thought to be older
integrations of avian retroviruses, because they are less similar to
exogenous viruses and their phylogeny closely reflects host phylogeny
(5, 19). The number of known EAVs is increasing and
includes recently identified EAV-HP and ev/J, which are apparently the
same endogenous virus described independently (20, 21). ART-CH elements have deletions in all retroviral genes, but they retain
cis-acting sequences necessary for retrotransposition
(11, 17).
Recently, we showed that endogenous ASLVs are found in three families
of galliform (fowl-like) birds, and, in some cases, the phylogenetic
patterns observed for virus genes were incongruent with host phylogeny
(8). Our findings are beginning to elucidate the ancient
evolutionary association between retroviruses and birds, and they
suggest the possibility of more-recent horizontal transmission of
endogenous viruses between avian hosts as well.
In this report we describe a new avian proviral genome, obtained from a
genomic library of Bonasa umbellus (ruffed grouse), called
tetraonine endogenous retrovirus (TERV). Tetraonines are a subfamily of
galliform birds consisting of grouse and ptarmigan. This is the first
report of a complete, replication-defective ASLV provirus sequence from
a bird other than the domestic chicken. We compare the structure of
TERV to those of published avian retroviruses in order to investigate
its function and evolution. Southern blot and reverse transcription-PCR
(RT-PCR) analyses are used to document the distribution and expression
of TERV-related viruses in galliform birds. We hypothesize that TERV is
an active, endogenous retrovirus formed through recombination between
endogenous retroviral lineages.
Generation of grouse 
bacteriophage genomic library and
characterization of provirus structure.
A B. umbellus
lambda genomic library was constructed using a Lambda FIX
II/XhoI partial-fill-in vector kit (Stratagene, La Jolla,
Calif.). This library was screened by lifting plaques onto nylon
membranes and probing with a 32P-labeled gag
probe. This probe was amplified by PCR using GAG.F1 and GAG.R1 primers
(Fig. 1) and standard PCR conditions as
previously described (8). After gel purification of PCR
products, 
25 ng of probe DNA was radiolabeled using
[
-32P]dATP (3,000 Ci/mmol; Amersham Pharmacia
Biotech), 6 U of Klenow fragments, and random primers. Positive plaques
were grown in liquid culture, and recombinant phage DNA was isolated
using standard protocols (22). Provirus-positive phage DNA
was randomly fragmented and subcloned into pZero vector (Stratagene).
Plasmid DNA was isolated from positive colonies using a QIAprep spin
miniprep kit (Qiagen) and sequenced using universal primers as
previously described (8). The sequence was edited, and
contigs were assembled, using Sequencher (Gene Codes Corp.). Published
ASLV Sequences are listed with GenBank accession numbers in Table
1.
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FIG. 1.
Comparison of RSV (A) and TERV (B) genome and packaging
signal ( ) secondary structures (3, 23). The RSV genome
is not drawn to scale. The first 342 nucleotides (shaded region) of
TERV gag are highly conserved relative to published ASLVs.
The nucleotide similarity ranges from 80 (EAV-HP) to 97% (B. umbellus ASLV). The matrix (MA) region of Gag is indicated above
coding regions. Hatched boxes, three regions in TERV with the greatest
similarity (29 to 59%) to those of EAV-HP (20, 21). The
single line between TERV gag and env denotes an
apparent noncoding sequence. Primers GAG.F1 and GAG.R1
(8), used to amplify the probe for genomic library
screens, are shown below RSV. Predicted secondary structures of the
retroviral packaging sequence were modeled using Mfold (4,
32). Nucleotide positions listed are relative to the 5' end of
the packaging sequence (Fig. 2, M). Major stem-loop structures are
identified using the notation of Banks et al. (3). The RSV
secondary structure is based on a consensus of 20 previously published
ASLV packaging sequences. This structure is identical to the structure
published by Banks and Linial (2).
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The DNA insert of one recombinant lambda was sequenced to reveal a
replication-defective retroviral sequence of 3,711 bp,
which we call
TERV (Fig.
2). Host
flanking sequences at the 5'
and 3' ends of TERV (1,439 and 733 kb,
respectively) were found
to be not similar to any sequences in GenBank
using BLAST (
1).
The TERV provirus genome structure was
similar to those of other
defective avian retroviruses such as Fujinami
sarcoma virus, EAV-HP,
and ART-CH (
11,
20,
21,
24). The
TERV protein coding sequence
was flanked by long terminal repeats
(LTRs), and these in turn
were flanked by 5-bp direct repeats
(5'-ATCAG-3'). The terminal
nucleotides of the provirus were
5'-TG...CA-3' and were part of
imperfect indirect repeats (Fig.
2).
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FIG. 2.
Complete nucleotide sequence of a TERV provirus
including the host flanking sequence. The complete provirus is 3,711 bp
in length. Direct repeats (5 bp) flanking the provirus are shaded, and
major LTR regions are indicated. The repeat region (R),
tRNATrp PBS, and PPT are underlined. The TATA box and
polyadenylation signal are boxed. Translations of Gag and Env proteins
are below the nucleotide sequence. Downward arrow, junction between the
highly conserved gag sequence (5') and regions of low
conservation (3'). The shaded region in Gag corresponds to a region
possibly homologous to the L domain (PPPPY) in ASLVs. Double
underlining, putative packaging sequences (M and direct repeat 1).
Only one copy of RSV-related direct repeat 1 was found in TERV. Primer
sequences described in the text are underlined, and the primer names
are indicated. ProbeMatrix and
Probeenv, fragments representing probes used for
Southern hybridization.
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We compared TERV untranslated region (UTR) sequences to retrovirus UTR
sequences of known function to identify potentially
functionally
homologous regions. The 3' boundary of the 5' LTR
was distinguished by
a sequence highly conserved relative to those
of other avian retrovirus
tRNA
Trp primer binding sites (PBS) (initiation of
minus-strand synthesis).
The 5' boundary of the 3' LTR was
distinguished by the polypurine
tract sequence (PPT) (initiation of
plus-strand synthesis). Based
on these boundaries, host flanking direct
repeat sequences, and
sequence conservation with other ASLV R regions,
identical LTRs
of 376 bp were defined. The typical proviral LTR
structure (5'-U3-R-U5-3')
was found, and lengths for the U3, R, and U5
regions were 266,
21, and 89 bp, respectively. These LTRs were longer
than LTRs
from RSV (327 bp) (
23), EAV-HP (315 bp)
(
20,
21), EAV-0
(243 bp) (
5,
6), and RAV-0
(277) (
13) but slightly shorter
than ART-CH
LTRs (388 bp) (
17).
The TERV U3 sequence was most similar to that of RAV-0, particularly at
conserved motifs that function in retrovirus transcription.
Putative
transcription factors were identified by searching on-line
database
TRANSFAC, specifying a threshold score of 85 (
12),
and by
comparative sequence analysis with known transcriptional
regulatory
sequences from ASLVs. The 5'-most enhancer binding
element was similar
to an IK-2 element (position
221), which
is bound by a transcription
factor isolated from mice (
10).
The next sequence, a
EFI binding element, was located at
194
in relation to the
transcription start site. It is thought that
protein
EFI is an
embryonic gene regulator in chickens (
9).
These two
elements were not known from other avian retrovirus
LTRs; thus further
characterization is necessary as these elements
show limited similarity
to the consensus sequences. At position
165 there was a putative
serum response element (SRE) (
27,
28) that was highly
conserved relative to the SRE found in RAV-0
(
31). Within
this element there was a CArG box, defined as
5'-CC(A/T)
6GG-3'.
This sequence was followed by an inverted
CCAAT box at
132 also
found in RAV-0 and RSV. The CCAAT box was in
the middle of putative
NF-Y and C/EBP binding sites. Finally, another
SRE was located
at
75.
The U3 region of TERV was highly conserved relative to those of other
ASLVs, starting with the TATA box located at position
24, followed by
a polyadenylation signal just upstream of the
repeat region (R). The R
and U5 regions of TERV had the greatest
sequence similarity to those of
RAV-0 at 91 and 89%, respectively,
and had 82 and 86% similarity,
respectively, to those of RSV (Table
2).
The tRNA
Trp PBS were identical across all avian
retroviruses mentioned in
this report with the exception of that of
EAV-0, which had an
additional cytosine residue (Table
2).
Analysis of putative Gag and Env proteins.
Two open reading
frames (ORFs) that had sequence similarity to those of published ASLVs
were found. The N-terminal 123 amino acids encoded by the first ORF had
88% identity to RSV and 95 to 97% identity to previously published
B. umbellus Gag sequences corresponding to the M domain of
the matrix region (Fig. 1). The remaining 460 amino acids had 29 to
59% identity with those of ASLV Gag proteins in three regions, each
separated by sequences that showed no significant sequence similarity
to published ASLV amino acid sequences in GenBank (Fig. 1). The regions
of EAV-HP had the highest similarity to these regions, slightly higher
than published regions of B. umbellus ASLV. One other region
of amino acid similarity to Gag begins at P240 and is a
proline-rich region (PSAPSAPPPAP) possibly homologous to the L domain
(PPPPY) found in all ASLVs, which functions in virus assembly
(30).
A second ORF, located 360 bp downstream of the
gag gene,
encoded 106 amino acids that had 29 to 40% identity to Gag of ASLV
and
murine leukemia virus and porcine endogenous retrovirus Env
based on
BLAST search results (Fig.
1). The putative ORF corresponded
to the
carboxyl terminus of the transmembrane region of Env. This
Env-related
ORF was just upstream of a 110-bp sequence with 89%
identity to those
of exogenous ASLVs, which corresponds to the
direct repeat 1 sequence
found in all ASLV genomes studied, including
replication-defective
transforming avian
retroviruses.
Analysis of gag gene transcription.
Sequence
analysis suggests that TERV is capable of transcription. To determine
if gag sequences were transcribed, total RNA was extracted
from heart muscle of one adult B. umbellus animal and whole
8-day-old Phasianus colchicus and Colinus
virginianus embryos using Trizol reagent (Gibco Life Technologies)
according to the manufacturer's protocol. RNA extract was treated with
5 U of DNase I, amplification grade (Gibco Life Technologies), to eliminate DNA contamination according to the manufacturer's protocol. RT-PCR was performed on DNase-treated total RNA using a Titan one-tube
RT-PCR kit (Roche) and two sets of primers at an annealing temperature
of 55°C. Primers GAG.F1 and GAG.R1 (8) are general gag primers, while GC2128F and GC2604R (Fig. 2) are specific
to TERV gag. Chicken 
-actin primers were used as a
positive control for RNA. These primers (-actinF
[5'-AATGAGAGGTTCAGGTGCCC-3'] and -actinR
[5'-ATCACAGGGGTGTGGGTGTT-3']) amplify a 410-bp fragment. RT-PCR products were verified by DNA sequence analysis as described previously (8). PCR using GAG.F1 and GAG.R1 primers was
performed on DNase-treated and untreated samples to verify that DNA
contamination was eliminated.
RT-PCR using GAG.F1 and GAG.R1 primers on DNase-treated samples
resulted in products from all three birds as did PCR analysis
of
non-DNase-treated samples (Fig.
3). Size
variation in amplicons
is consistent with results obtained in our
previous study of avian
retroviral
gag sequences
(
8). Sequence analysis of the RT-PCR
product from
Phasianus suggested that these primers amplified
nontarget
transcripts, whereas sequence analysis confirmed that
gag
transcripts were amplified from
Bonasa and
Colinus. RT-PCR
using TERV-specific primers (GC2128F and
GC2604R) resulted in
amplification in all three birds. The product from
B. umbellus was 475 bp, the size predicted from TERV, while
the predominant
products from
Phasianus and
Colinus were 200 to 300 bp larger
(Fig.
3). These RT-PCR
products were sequenced, and all were verified
as
gag
sequences.
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FIG. 3.
RT-PCR analysis of total RNA isolated from heart muscle
for an adult B. umbellus animal (BOUM) and 8-day-old embryos
of P. colchicus (PHCO) and C. virginianus
(COVI). (A) RT-PCR on total RNA. Lane 1, 100-bp ladder (Promega); lanes
2 to 5, primers GAG.F1 and GAG.R1; lanes 6 to 9, primers GC2128F and
GC2604R. (B) RT-PCR using -actin primers (lanes 2 to 5) and PCR
using primers GAG.F1 and GAG.R1 on DNase-treated RNA extracts (lanes 6 to 9). (C) PCR on non-DNase-treated samples using primers GAG.F1 and
GAG.R1.
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Normally, following transcription, two copies of the retroviral RNA
genome are incorporated into viral particles. This packaging
process
involves the recognition and binding of sequence
on
the RNA genome
by viral proteins. In ASLVs, a 160-nucleotide sequence
has been
identified as the minimal packaging signal (M
) in the
leader region
between the PBS and the Gag initiation codon (
3).
TERV
contained a sequence highly conserved relative to avian retrovirus
M
s located between the primer binding site and the
gag
initiation
codon. TERV M
had a similarity of 78.2% to a consensus
alignment
(
2) of 20 exogenous and endogenous avian
retrovirus packaging
sequences. EAV-HP and ART-CH did not have the same
level of conservation
in the packaging signal. The sequences between
the PBS and the
gag initiation codon in ART-CH and EAV-HP
are about 100 bp shorter
than those in TERV and other
ASLVs.
It appears that the secondary structure of M
plays a significant
role in efficient packaging (
2). TERV and the ASLV
consensus
packaging sequence were analyzed using the Mfold program
(version
3.0) to model the most-stable secondary structures (
4,
16).
The lowest free energies were
61.02 kcal/mol for the
secondary
structure of TERV and
56.82 kcal/mol for the folding of a
consensus
sequence of 20 ASLV packaging signals (Fig.
1). The two
modeled
structures were remarkably similar. TERV M
had the two major
stem-loop regions O3 and L3 and the three minor stem-loops O3SLa,
O3SLb, and O3SLc previously identified by Banks and Linial
(
2).
In ART-CH and EAV-HP the most-stable secondary
structures for
sequences that correspond to M
were not similar to
those of RSV,
the consensus of ASLVs, or TERV when folded with Mfold
(not
shown).
Our previous work showing that some ASLV phylogenetic relationships
reflect overlapping host species ranges rather than host
species
phylogeny (
8) suggests that horizontal transmission
of
ASLVs has occurred in the past. Here we have demonstrated that
TERV is
transcribed and contains sequences required for packaging
and
retrotransposition. We have no direct evidence regarding the
means by
which TERV or other tetraonine ASLVs move between host
species;
however, one possible mechanism is hybridization among
host species,
which is known to occur naturally between some tetraonines
(
14). Alternatively, TERVs could have been transmitted
horizontally
if they were transcribed and packaged with
replication-competent
retroviruses.
Phylogeny and recombination.
To explore the relationship of
TERV and other endogenous and exogenous ASLVs, we conducted
phylogenetic analyses using three regions of TERV. Sequence alignments
corresponding to various regions of TERV and ASLVs were performed using
Clustal X (26). Phylogenetic analyses were performed using
maximum parsimony (MP) as implemented in PAUP* (25).
Branch-and-bound MP analyses were conducted, and bootstrap values were
determined using 100 replicate searches.
The first region examined corresponds to the matrix gene of
gag. MP analysis using this region (342 nucleotides) yielded
one
tree composed of three major groups (Fig.
4A). The first group
consisted of
endogenous and exogenous viruses isolated from birds
in the genus
Gallus, including the domestic chicken (
Gallus
gallus).
The second group consisted of presumably endogenous
proviruses
from grouse and ptarmigan (Tetraoninae), and the third group
consisted
of endogenous viruses EAV-HP and ART-CH. TERV was the sister
taxon
to ASLV, whose
gag gene was previously sequenced from
B. umbellus.
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FIG. 4.
Phylogenetic analyses of gag and UTR
sequences. Unrooted MP trees were constructed using the
branch-and-bound option in PAUP* (25). Bootstrap
values along branches were calculated using 100 random-addition
replicate searches. COVI, C. virginianus ASLV; PHCO,
P. colchicus ASLV; LALA, Lagopus
lagopus ASLV; BOUM, B. umbellus ASLV; GAVA, G. varius ASLV; FuSV, Fujinami sarcoma virus; AMV, avian
myeloblastosis virus; Y73, avian sarcoma virus Y73. Branch lengths are
proportional to inferred amounts of evolutionary change. (A)
Relationship of 10 previously published ASLV and TERV sequences based
on 342 nucleotide sites from the matrix region of the gag
gene. (B) One of two equally parsimonious trees for the relationship of
11 published ASLVs and TERV based on the more-divergent amino acid
region of Gag downstream from the region analyzed in panel A. The two
equally parsimonious trees differ only in the placement of GAVA. (C)
Phylogeny of eight previously published UTR sequences and TERV.
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The second region corresponded to the remaining sequence in TERV Gag
adjacent to the highly conserved matrix region. Only
short stretches of
amino acids could be aligned to other ASLV
Gag proteins, resulting in a
data set with 125 parsimony-informative
characters. Two equally
parsimonious trees that differed only
in the placement of
Gallus
varius ASLV were found (Fig.
4B). Interestingly,
TERV and the
other
B. umbellus ASLV sequences were not sister
taxa based
on this portion of the
gag gene. Instead, TERV is located
between an EAV-HP/ART-CH group and a group containing the remaining
ASLVs.
The third region analyzed was aligned with eight published avian
retrovirus UTR sequences. This phylogeny (Fig.
4C) showed
relationships
similar to those from the tree shown in Fig.
4A.
We found that EAV-HP
and ART-CH formed a group that was sister
to EAV-0 (EAV-0 was not
included in
gag phylogeny). TERV was most
closely related to
endogenous avian retrovirus RAV-0. No UTR sequences
from other
tetraonine retroviruses were available for
comparison.
Recombination within the
gag gene of RSV can occur with a
relatively high frequency (
15). Incongruent trees
from our phylogenetic
analyses suggest the possibility that TERV
was formed by recombination
between retroviruses. One
recombination point may occur near amino
acid 123, where the similarity
of TERV Gag to
B. umbellus Gag
drops drastically from 97 to
around 40%. Phylogenetic analysis
illustrates that this downstream
region of TERV Gag is not sister
to those of other tetraonine ASLVs,
RAV-0, or exogenous ASLVs
(Fig.
4B). Phylogenetic analysis and amino
acid identity of a
short region of Env (transmembrane region) suggest a
relationship
that is also incongruent with UTR and 5'
gag phylogenies (not
shown). These findings are
compatible with the interpretation
that TERV was formed by
recombination, although the parental sequences
for divergent regions of
TERV have yet to be discovered. An alternative
explanation to
recombination is that highly divergent regions
of TERV result from
differing selective pressures on the viral
genome. We are examining
additional complete tetraonine retrovirus
genomes to investigate this
possibility.
Distribution of TERV-related sequences.
To determine the
distribution of TERV-related sequences, genomic DNA was isolated from
six galliform species and one anseriform (Aythya americana)
using standard protocols. Roughly 3 µg of genomic DNA was digested to
completion with HindIII, electrophoresed in a 1.0%
agarose gel, and blotted overnight onto a positively charged nylon
membrane (Hybond-XL; Amersham Pharmacia Biotech). Two different probes,
probematrix and probeenv, were
amplified by PCR from TERV-lambda DNA. These probes corresponded to a
region of matrix (GC2128F and GC2604R) and a divergent region similar
to that in which env is located (GC3877F and GC4332R) (Fig.
2). Hybridization was performed at 65°C in standard buffer overnight
with probematrix first, followed by
probeenv. The nylon membrane was washed in
several steps with decreasing salt and sodium dodecyl sulfate (SDS)
concentrations, down to 0.5× SSPE (1× SSPE is 0.18 M NaCl, 10 mM
NaH2 PO4, and 1 mM EDTA [pH 7.7]) and 0.1%
SDS, and increasing temperature to 65°C. Prior to being probed
with probeenv, the membrane was stripped
by washing with 0.1% SDS at 100°C for 30 min and exposed to film for
1 week to verify that all of probematrix was removed.
Results of Southern analysis at high stringency using both probes were
positive for the five grouse and ptarmigan tested and
negative for a
domestic chicken and a redhead (Fig.
5).
Genomic
DNA from two
B. umbellus individuals was analyzed
and had almost
identical banding patterns. Both probes showed complex
hybridization
patterns consistent with the idea that TERV integrated in
multiple
locations within the bird genome.
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FIG. 5.
Southern blot analysis of
HindIII-digested avian genomic DNA using TERV
probematrix and probeenv.
Hybridization was performed at 65°C, and the filter was washed
with salt-SDS solution at concentrations as low as 0.5×
SSPE-0.5% SDS at 65°C. (A) Probematrix. (B)
Probeenv. Lanes 1 and 2, B. umbellus
(ruffed grouse); lanes 3, Bonasa bonasia (hazel grouse);
lanes 4, Lagopus lagopus (willow ptarmigan); lanes 5, Lagopus leucurus (white-tailed ptarmigan); lanes 6, Dendragapus falcipennis (Siberian grouse); lanes 7, Anseriformes (Aythya americana [redhead]); lanes 8, G. gallus (domestic chicken). This shows the presence of
TERV or closely related elements in all tetraonine birds surveyed.
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Divergence date estimates from fossils suggest that tetraonines
separated from their putative closest extant relative (
Meleagris gallopavo [turkey]) in the mid-Miocene (15 to 20 million years
ago), while modern tetraonines seem to have been present for at
least 1 million years (
7,
29). If our limited sampling of
birds is
representative, TERV could have integrated into the genome
of a
tetraonine sometime during the past 15 million years. Future
surveys,
including more Galliformes as well as birds from additional
avian
orders, are needed for more-reliable estimates of TERV age
and relative
timing of integration into host species genomes.
The 100% identity
between TERV LTRs suggests that TERV was active
quite recently,
although this activity may have been restricted
within the
genome.
Nucleotide sequence accession number.
The TERV sequence
obtained in this study has been assigned GenBank accession no.
AF289082.
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ACKNOWLEDGMENTS |
This work was supported by University of Michigan graduate student
block grant funds to D.E.D. and M.K.
We thank Michael Frohlich, David Parker, and Vici Blanc for excellent
technical assistance and Sergei Drovetski of the University of
Washington Burke Museum for providing some tissue samples used in this study.
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FOOTNOTES |
*
Corresponding author. Present address: Rocky Mountain
Laboratories, 903 S. 4th St., Hamilton, MT 59840. Phone: (406)
363-9359. Fax: (406) 363-9286. E-mail: ddimcheff{at}nih.gov.
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Journal of Virology, February 2001, p. 2002-2009, Vol. 75, No. 4
0022-538X/01/$04.00+0 DOI: 10.1128/JVI.75.4.2002-2009.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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