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1 Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Changping Liuzi 5, 102206 Beijing, PR China
2 Beijing Friendship Hospital, Affiliate of Capital Medical University, Beijing, PR China
3 Guizhou Center for Disease Control and Prevention, Guiyang, Guizhou Province, PR China
4 Department of Pathology, University of Georgia, Athens, GA 30602, USA
5 Department of Virology, Haartman Institute, University of Helsinki, Finland
Correspondence
Yong-Zhen Zhang
yongzhenzhang{at}sohu.com
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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GenBank accession numbers of the S, M and L segment sequences determined in this study are given in Table 1.
Two supplementary tables and a supplementary figure are available with the online version of this paper.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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; Zhang et al., 2004). The disease is caused by hantaviruses, members of the genus Hantavirus in the family Bunyaviridae (Nichol et al., 2005). The virus genome consists of three separate segments of negative-stranded RNA referred to as small (S), medium (M), and large (L) segments, which encode nucleocapsid protein (NP), two envelope glycoproteins (Gn and Gc) and viral RNA-dependent RNA polymerase (RdRP), respectively (Plyusnin et al., 1996). In contrast to other genera of the Bunyaviridae, hantaviruses are not transmitted by arthropods (Schmaljohn & Hjelle, 1997). They establish a chronic infection that causes no apparent harm to rodents of the Muridae family, which are their natural hosts (Childs et al., 1989; Hutchinson et al., 2000; Kurata et al., 1983; Li et al., 1995; Netski et al., 1999). Currently, at least 22 distinct hantavirus species have been identified worldwide; all of these hantaviruses except Thottapalayam virus (TPMV) are carried by rodents (Nichol et al., 2005). Each rodent-borne hantavirus species appears to be associated primarily with one (or a few closely related) rodent species (Nichol et al., 2005; Plyusnin & Morzunov, 2001). Most of the current data support the notion that hantaviruses have co-evolved with their respective rodent hosts during the long-term evolution of this group of viruses (Morzunov et al., 1998; Nichol et al., 2005; Plyusnin et al., 1996; Plyusnin & Morzunov, 2001).
Guizhou province is located in the south-western part of China. The province has always been one of the most seriously affected areas in China since the first hantavirus outbreak was reported in 1962 (Wang et al., 1989, 2003; Zhang et al., 2004). More than 5000 HFRS patients were reported in 1985 alone (Wang et al., 1989). Forty-five species of rodents have been found in Guizhou (Li et al., 1999) and during the past two decades, hantavirus-reactive antibodies and/or antigens have been identified in at least 12 rodent species in Guizhou (Chen et al., 1999; Wang et al., 1989, 2003). However, the mouse Apodemus agrarius has been identified as the major reservoir of hantavirus. Phylogenetic analysis of partial M and S segment sequences indicates that Hantaan virus (HTNV) displays high genetic diversity in Guizhou (Wang et al., 2000) and at least three distinct phylogroups of HTNV and one new variant of Seoul virus (SEOV) have been found to circulate in Guizhou (Zou et al., 2008). Spillover of HTNV from A. agrarius to Rattus norvegicus has been reported in Guizhou. Circumstantial evidence suggests that genetic reassortment between HTNV and SEOV has also occurred naturally during or after the spillover. In addition, Guizhou is the main constituent of the Yunnan–Guizhou plateau, which may be a significant factor in lineage isolation of Apodemus spp. (Xia, 1984; Suzuki et al., 2003). Thus, further studies of hantaviruses in Guizhou would be helpful to clarify the phylogeny of HTNV and to shed light on the prevention and control of the diseases it causes.
In the present study, we recovered the complete S and M sequences and also partial L segment sequences from the Guizhou HTNV variants isolated both in this study and previously, and compared these sequences with those of HTNV isolates reported previously in China, far-eastern Russia and South Korea. Our data indicated that there are at least four distinct phylogroups of HTNV in Guizhou. Further analysis of the S segment sequences showed that the HTNV isolates from China, far-eastern Russia and South Korea form six distinct phylogroups, which cluster into three clades. The viruses in clade I have only been found in Guizhou; these became the outgroup of clades II and III. The viruses in the second clade are found in Guizhou and mainly in far-eastern Asia (China, Russia and South Korea). The viruses in the third clade are distributed in most HFRS areas of China, including Guizhou.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Sampling and screening, and virus propagation.
Rodents were captured in HFRS endemic areas in Guizhou with snap-traps, which were set at five metre intervals and baited with peanuts (Fig. 2), between the spring of 2004 and the autumn of 2005. Lung tissue was obtained from trapped animals. Serum samples were obtained from two patients with acute HFRS, which was diagnosed by using clinical criteria and the presence of IgM antibodies to HTNV. Hantavirus-specific antigens in rat lungs were detected by indirect immunofluorescence assay (IFA), as described by Lee et al. (1978). Antigen-positive lung tissues were homogenized. The supernatants and serum samples from HFRS patients were used to inoculate Vero E6 cell monolayers as described by Lee (1999). After 2 h adsorption, the tissue suspension and the sera were removed, and maintenance medium [Dulbecco's modified Eagle medium supplemented with 2 % heat-inactivated fetal calf serum (FCS), 100 µg penicillin ml–1 and 100 µg streptomycin ml–1] was added to the cells. Cells were incubated at 37 °C with 5 % CO2 in an incubator. On day 21 post-inoculation (p.i.), cells were suspended by trypsin treatment, and part of the suspended cells was cultured with fresh Vero E6 cells. A sample of the cells was fixed onto glass slides for detection of hantavirus antigen by IFA. The four viruses that were isolated in 1986 (above) were propagated in Vero E6 cells.
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) was used for reverse transcription of the S, M, and L segments from total RNA by using avian myeloblastosis virus reverse transcriptase (Promega). The S segment was amplified by using the primers S1 and S2 (Puthavathana et al., 1992). The M segment was amplified as two overlapping fragments using two initial primer pairs, M1 and HV-MFO and HV-MRO and M4 (Shi et al., 1998; Sun et al., 2005), for the first round of amplification. In the second round of amplification, the primer pairs M1 and HMF, and HMR and M4 (Shi et al., 1998; Sun et al., 2005) were used to amplify the two fragments for HTNV. Partial L segment [nucleotides (nt) 2750–3200] sequences were amplified by using primer pair HTN-L-F1 and HTN-L-R1 for initial PCR and primer pair HTN-L-F2 and HTN-L-R2 for the second round of amplification (Klempa et al., 2006). PCR products were separated by electrophoresis and purified from gel slices by using the agarose gel DNA purification kit (TaKaRa Biotechnology) according to the manufacturer's instructions. Purified DNA fragments were cloned into the pMD18-T vector (TaKaRa Biotechnology). The ligated products were transformed into Escherichia coli JM109 competent cells. DNA sequencing was performed with the ABI-PRISM Dye Terminator Sequencing kit and an ABI 373A Genetic Analyzer. The nucleotide sequences of at least two clones from each isolate were determined.
Phylogenetic analysis.
The PHYLIP program package (version 3.65) was used to construct phylogenetic trees by using the maximum-likehood (ML) and the maximum-parsimony (MP) methods with 1000 bootstrap replicates. Alignments were prepared with CLUSTAL W (version 1.83) by first translating nucleotide sequences into amino acid sequences with DNASTAR (version 5.01). Nucleotide or amino acid identities were also calculated by using DNASTAR. The hantavirus sequences available in GenBank that are listed in Table 1 were also retrieved for analysis.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Molecular diversity and phylogenetic relationship of HTNV strains from Guizhou
Complete S and M sequences and partial L segment sequences were determined for all ten isolates, as well as for four viruses isolated previously (CGAa4MP9, CGAa4P15, CGAa1011 and CGAa1015). Phylogenetic ML trees were constructed by using the S and M segment sequences from Guizhou that were recovered in the present study and in previous studies (Table 1
; available in GenBank) (Fig 1a, strains in bold type were recovered in this study). This tree indicates that all known isolates from Guizhou, regardless of their source, belong to HTNV and could be divided into four distinct groups (S1, S2, S3 and S4). These data also suggest that the spillover of HTNV occurred naturally from A. agrarius to R. norvegicus or R. nitidus. The first group contained only one human isolate . The Guizhou viruses in the second group were divided into two distinct lineages. The Guizhou viruses in the third group could be also divided into two lineages. Phylogroup S4 comprised only viruses from Guizhou, and these viruses were further divided into two distinct lineages, suggesting a high degree of molecular diversity of HTNV in Guizhou.
In the phylogenetic tree generated from the M segment sequences (Fig. 1b), all the Guizhou isolates belonged to HTNV except the reassortants CGRn8316 and CGRn9415 (Zou et al., 2008). Analysis of the M segment sequences also divided the Guizhou HTNV variants into four groups (M1, M2, M3 and M4). However, the relationship among these variants was different from that in the phylogenetic tree based on S sequences. The S4 variants, which are distinct from the other three groups in the tree based on the S segment, clustered together with the viruses (CGAa2, CGAa75, CGRn15, CGRn45, CGRn2616, CGRn2618 and CGHu3) from S2, and comprise the group M4. These data suggest that the genetic reassortment within HTNV might have occurred naturally.
In order to gain more insights into hantavirus reassortment, partial L segment sequences (nt 2750–3200) were recovered and analysed. Similar to the phylogenetic trees based on the S and M segment sequences, all Guizhou HTNV strains were divided into four groups (L1, L2, L3 and L4) (Fig. 1c). The clustering of the Guizhou viruses in the L tree was congruent with their clustering in the M tree, but different from the clustering in the S tree. These data supported our hypothesis that genetic reassortment within HTNV occurs in nature.
Comparison of the S sequences revealed that the nucleotide divergence among all Guizhou HTNV isolates ranged from 0.1 to 16 % (see Supplementary Table S1, available in JGV Online). The amino acid divergence varied from 0.2 to 4 %. There was no significant amino acid difference among groups except between group S1 and other groups. The M segment nucleotide divergence among all Guizhou HTNV isolates varied from 0.1 to 17 %, similar to the S segment divergence, but the amino acid difference varied from 0.4 to 7 %, and was higher than that for the S segment (see Supplementary Table S2). Furthermore, the divergence among groups ranged from 10 to 17 % at the nucleotide level and from 5 to 7 % at the amino acid level, and the difference among lineage within group varied from 5 to 7 % at the nucleotide level and from 1 to 2 % at the amino acid level, respectively. These data suggest that more non-synonymous substitutions occurred in the M segment than in the S segment.
The geographical distribution of HTNV in Guizhou
Overall, HTNV strains clustered geographically in Guizhou (Fig. 2). The first group (S1) consisted of only one isolate, CGHu1, which was derived from a human and was found in Zunyi; the third group (S3) had six isolates, which were detected in Anshun and Rongjiang; and viruses of the fourth group (S4) were detected in Changshun. In contrast, the group S2 viruses were distributed widely, and were found in most of the HFRS endemic areas of the province (Cengong, Kaiyang, Shiqian, Xingyi and Zunyi). Furthermore, the viruses isolated between 2001 and 2005 also belong to group S2. These data suggest that this group has been predominant in Guizhou in recent times.
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). In the phylogenetic tree based on the S segment sequences, all HTNV isolates formed three clades (Fig. 1a). The first clade consisted of viruses (group S4) derived only from A. agrarius in Guizhou. The second clade comprised two groups (S1 and S6), derived mainly from humans, A. agrarius and A. peninsulae in north-eastern China (Sun et al., 2001; Wang et al., 2000; Zhang et al., 2007), as well as from far-eastern Russia (Lokugamage et al., 2004) and South Korea (Baek et al., 2006; Lee et al., 1978), both of which share borders with China. The third clade included three groups (S2, S3 and S5), derived mainly from A. agrarius in HFRS endemic areas of China including Guizhou. The viruses from S2 grouped together with isolates A16 from A. agrarius in Shaanxi (Yao et al., 2001a) and TJJ16 from Niviventer confucianus in Tianjin (Li et al., 2005). Interestingly, the Guizhou viruses from S3 formed a group with the isolates Z5 derived from A. agrarius (sequence can be found under GenBank accession number EF103195
[GenBank]
), Z10 derived from a human in Zhejiang (Yao et al., 2001b), A9 from A. agrarius in Jiangsu (Shi et al., 1998), which shares borders with Zhejiang, and Hu isolated from a human in Hubei (Wang et al., 2000). The group S5 in the third clade contains strains 84FLi from a human in Shaanxi, Chen4 from a human in Anhui (Liang et al., 1994), SN7 from N. confucianus in Sichuan (Yao et al., 2002) and E142 from Eothenomys eleusis in Yunnan (this sequence can be found under GenBank accession number AF288644
[GenBank]
). The tree constructed by using the MP method had the same topology as that constructed by the ML method, supported by higher bootstrap values (Supplementary Fig. S1).
In contrast to the topology of the S tree, all HTNV isolates formed seven distinct phylogroups and showed monophyletic ancestry in the tree constructed from the M segment sequences (Fig. 1b). Furthermore, strains Z5 (EF103195
[GenBank]
) and Z10 (Yao et al., 2001b) formed group M7, which was different from the other S3 viruses, although there was only weak bootstrap support for the M7 group. The tree constructed by using the MP method had a similar topology to that constructed by using the ML method (Supplementary Fig. S1). However, the viruses in group M7 clustered together with the viruses in group M3 in the MP tree.
Multiple alignments of the deduced amino acid sequences of the M and S coding region
It has previously been reported that all genetic lineages of Puumala virus (PUUV) possess specific amino acid ‘signatures’ in the NP sequences (Sironen et al., 2001). Although a high degree of nucleotide variation of the S segment is present among different groups, only a few non-synonymous substitutions were observed for the NP sequence. Furthermore, unlike PUUV, groups S3 and S5 do not possess specific amino acid ‘signatures’. The other groups possess specific amino acid ‘signatures’ such as group S1, aa 52 changes from A
V; group S2, aa 295 IV; group S4, aa 241 SG; and group S6, aa 9 RK, aa 28 AR, aa 215 IV and aa 416 VL. In addition, the following non-synonymous substitutions are shared by several groups: substitution at aa 43 (TA) is shared by group S3 strains except Z5 and Z10, nearly half of the viruses in group S2 and most of the viruses in group S6; at aa 124 (IV) by groups S1 and S6; at aa 256 (HL) by groups S1 and S4; at aa 290 (SA) by groups S1 and S3 except the strains Z5 and Z10; and at aa 290 (ST) by groups S4 and S6, and strains Z5 and Z10 from group S3.
Comparing GnGc protein sequences (encoded by the M segment) may provide clues to antigenic, as well as genetic, diversity (Schmaljohn & Hjelle, 1997). All genetic groups possess specific amino acid ‘signatures’ in the deduced GnGc protein sequence, which are displayed in bold in Fig. 3. Interestingly, groups M3 and M7 shared a total of 14 identical non-synonymous substitutions, and groups M5 and M7 also share eight identical non-synonymous substitutions, suggesting that these groups may be closely related.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Genetic analysis of S and M segments from 14 isolates showed a high degree of genetic diversity of HTNV in Guizhou. The previous phylogenetic analysis of partial M segment sequences of the isolates showed that four distinct lineages of HTNV are present in A. agrarius in Guizhou (Wang et al., 2000). Recently, we found three distinct phylogroups of HTNV in Guizhou (Zou et al., 2008). In the present study, phylogenetic analysis of S and M segment sequences indicated that HTNV isolates could be divided into four distinct phylogroups and seven distinct lineages (Fig. 1). These viruses show up to 17 % divergence at the nucleotide level and up to 7 % at the amino acid level for the M segment. Furthermore, there is evidence that genetic reassortment has occurred for group S4 viruses and viruses from group S2 (CGHu3, CGAa2, CGAa75, CGRn15, CGRn45, CGRn2616, and CGRn2618, see below for explanation). Therefore, there may be two unrecognized groups of HTNV co-circulating in the rodent population in Guizhou. In addition, the S segment sequences from group S4 viruses, which have not been found in other parts of China or far-east Asia, are distinct from those of all other known HTNV. These data may suggest that a new variant of HTNV may circulate in rodents in Guizhou. In addition, group S5 virus has been detected recently in Guizhou (data not shown). Thus, a total of six phylogroups of HTNV could be distinguished by using S and M segment sequences, which indicates a remarkably high genetic diversity of HTNV within a small geographical region (Fig. 2).
Several studies have shown that genetic reassortment can occur naturally within hantaviruses (Henderson et al., 1995; Li et al., 1995) or experimentally between hantaviruses (Razzauti et al., 2008; Rizvanov et al., 2004; Rodriguez et al., 1998). This genetic reassortment occurs more frequently between closely related strains than genetically distant hantaviruses (Henderson et al., 1995; Li et al., 1995; Khaiboullina et al., 2005; Razzauti et al., 2008). Recently, we provided evidence that genetic reassortment between HTNV and SEOV has occurred naturally in Guizhou (Zou et al., 2008). In the present study, the clustering pattern of the viruses isolated from Guizhou in the tree based on S segment sequences was in disagreement with that in the trees based on either M or partial L segment sequences. It was obvious that the viruses in group S2 could be divided into two distinct groups in the trees constructed with the M or partial L segment (Fig. 1). Particularly, all viruses in group S4 were also grouped into group M2 in the tree based on the M segment sequence, and into group L4 in the tree based on partial L segment sequences. For these viruses, their respective amino acid ‘signatures’ on the NP and the GnGc protein sequences also suggested that genetic reassortment had occurred between groups within HTNV. These data indicate that genetic reassortment has occurred within HTNV in Guizhou. In addition, phylogenetic analysis of these sequences also revealed that virus A16 isolated from A. agrarius in Shaanxi province was a reassortant (Fig. 1). Together, our results suggest that genetic reassortment of hantaviruses may be more common than expected when closely related rodent species are sympatric (Zou et al., 2008) and that it is one of the mechanisms that generate HTNV genetic diversity.
Similar to other members of the family Bunyaviridae, the hantaviral NP plays an important role in virus replication (Blakqori et al., 2003; Flick et al., 2003; Flick & Pettersson, 2001; Kaukinen et al., 2005). Glycoproteins are known to mediate cell attachment and fusion (Tsai et al., 1984; Arikawa et al., 1985; Ogino et al., 2004; Okuno et al., 1986; Tischler et al., 2005) and are presumed to be the major element involved in induction of neutralizing antibodies during hantavirus infection (Khaiboullina et al., 2005). Although the nucleotide sequences of the M and S segments of any two HTNV have approximately the same degree of divergence (Supplementary Tables S1 and S2), the amino acid sequences of the S segment are less variable than those of the M segment (Supplementary Table S2). This means that more synonymous substitutions occur for the S segment and that more non-synonymous substitutions occur for the M segment. Unlike in PUUV (Sironen et al., 2001), the small number of non-synonymous substitutions also leads to a lack of specific amino acid ‘signatures’ in the NP of each phylogenetic group of HTNV. On the other hand, phylogenetic analysis of the S segment sequences of HTNVs indicates that there are three clades with five groups (Fig. 1a), while these viruses form seven groups in the tree based on M segment sequences (Fig. 1b). Hence, comparison of deduced N protein sequences among distinct groups of hantaviruses could not provide clues to localized genetic features of each group of HTNV. However, comparision of deduced GnGc protein sequences may provide clues to the antigenic as well as genetic diversity among hantaviruses (Schmaljohn & Hjelle, 1997). Analysis of the GnGc protein sequence showed that all groups of HTNV have specific amino acid ‘signatures’ (Fig. 3). Viral glycoproteins are often associated with high levels of non-synonymous diversity and provide some of the best examples in nature of positive selection (Yang & Bielawski, 2000; Valarcher et al., 2000; Holmes et al., 2002). It has been suggested that changes in the hypervariable region might represent adaptation to host-specific characteristics of the immune response (Hughes & Friedman, 2000). Earlier studies also found that the S, M and L segments of Amur–Soochong viruses isolated from humans in China (Liang et al., 1994) and carried by Apodemus peninsulae (Liang et al., 1994; Lokugamage et al., 2004; Baek et al., 2006) diverged from hantaviruses isolated from A. agrarius by 15, 22 and 21 % at the nucleotide level and 3, 9 and 4 % at the amino acid level, respectively. Considering the co-evolution of hantaviruses with their hosts (Plyusnin & Morzunov, 2001), these data suggest that hantaviral S and M segments may face different selection pressures from their host. Therefore, analysis of the S segment may provide more information about the earliest original relationship of HTNV, but comparison of the M segment may yield more information about the adaptation of HTNV to its local host.
The current distribution of hantaviruses is the result of rodent migration and the history of virus–host co-speciation events. Different characteristics of hantaviruses have emerged as adaptations to the distinct genetic environment of their rodent hosts (Plyusnin & Morzunov, 2001). Molecular data have provided strong evidence that Apodemus mice diverged about 8–10 million years ago (Serizawa et al., 2000). The Hengduan Mountains region was hypothesized to have played an important role in the evolutionary history of Apodemus since the Pleistocene era (Liu et al., 2004). It has been proposed that the Hengduan Mountains region might be a radiation centre of the present Apodemus species (Xia, 1984; Musser et al., 1996). The Yunnan–Guizhou plateau, which connects and overlaps with the Hengduan Mountains region, is also thought to play an important role in lineage isolation in Apodemus (Suzuki et al., 2003). The second radiation of Apodemus involved the divergence of A. agrarius, A. peninsulae, Apodemus semotus and Apodemus speciosus, and these four Asian species can be treated as a monophyletic group (Serizawa et al., 2000). Furthermore, these species could be integrated into the A. agrarius group within Apodemus (Liu et al., 2004; Serizawa et al., 2000). It is suggested that the ancestral HTNV might first have migrated into Guizhou (Wang et al., 2000). In the present study, phylogenetic analysis of the S segment sequence revealed that all HTNV isolates could be divided into three clades with six distinct genetic groups. In particular, the first clade, which has been found only in Guizhou to date, was the nearest to the ancestral node separating HTNV from other hantaviruses in the tree based on S segment sequences (Fig. 1a). Furthermore, this clade became the outgroup for both viruses in clades II and III, supported by high bootstrap values (100 %). Hence, the prototype viruses of the group S4 reassortant viruses might have diversified earlier than the other two clades. These data also suggest that viruses in clades II and III have a common origin, although the bootstrap support for clade II and also for the monophyly of clades II and III was low.
Taken together, a hypothesis for the evolutionary history of HTNV is illustrated in Fig. 4 and described here. An ancestor of hantaviruses carried by Apodemus mice in the Hengduan Mountains region or the Yunnan–Guizhou plateau diversified into two groups. The first group resulted in the divergence of clade I and the second group resulted in the divergence of most HTNV carried by A. agrarius, which diversified into two clades. Clade II evolved into group S1, associated with A. agrarius, and group S6, associated with A. peninsulae. Following radiation of A. peninsulae, this latter group diversified into strain A16 in Shaanxi (Yao et al., 2001a), B78 in Shandong, H5 in Heilongjiang (Liang et al., 1994) and Amur–Soochong viruses in far-eastern Russia (Lokugamage et al., 2004) and South Korea (Baek et al., 2006). As A. agrarius and A. peninsulae are closely related (Liu et al., 2004; Serizawa et al., 2000) and often inhabit the same forest, HTNV is closely associated with both species (Zhang et al., 2007). The ancestor of clade III diversified into groups S2, S3 and S5, and then spread and further diversified following rodent migration to the north and the east. However, knowledge of the genetic diversity and geographical distribution of hantaviurses carried by Apodemus is limited and thus further studies of HTNV in Guizhou and neighbouring areas will help to clarify the phylogeny of HTNV.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Received 18 January 2008;
accepted 10 April 2008.
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