* Department of Horticulture, University of Wisconsin-Madison; Research Institute for Bioresources, Okayama University, Kurashiki, Japan;
Institute of Plant Molecular Biology, Ceske Budejovice, Czech Republic;
Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China; and || The Institute for Genomic Research, Rockville, Maryland
Correspondence: E-mail: jjiang1{at}wisc.edu.
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Abstract |
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Key Words: bacterial artificial chromosomes centromeric retrotransposon long terminal repeats rice
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Introduction |
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Retrotransposons demonstrate different distribution patterns in plant genomes. Some retrotransposons are dispersed throughout plant genomes (Heslop-Harrison et al. 1997; Mroczek and Dawe 2003), whereas others are highly enriched in distinct chromosomal domains (Jiang et al. 2002, Jiang et al. 2003; Mroczek and Dawe 2003). These distribution patterns are likely caused by different targeting specificities of the retrotransposons. Recent studies in Saccharomyces cerevisiae have shed light on the mechanisms of retrotransposon insertion specificity (Sandmeyer 2003; Bushman 2004). For example, the Ty5 retrotransposon in S. cerevisiae inserts preferentially into the heterochromatic regions. This targeting specificity is determined by interactions between the targeting domain at the C-terminus of the Ty5 integrase (IN) and the heterochromatin protein Sir4p (Zhu et al. 2003). Thus, the targeted integration of Ty5 is controlled by protein-protein interactions.
One of the most interesting retrotransposon families in plants is the centromeric retrotransposon (CR) in the grass species. CR belongs to the Ty3-gypsy group and is highly specific to the centromeric regions of grass chromosomes (Jiang et al. 2003). The CR elements are found in both monocot and dicot species and represent a distinct clade in the Metaviridae family (Gorinsek, Gubensek, and Kordis 2004). Two repetitive DNA sequences specific to grass centromeres were isolated from sorghum (Jiang et al. 1996) and Brachypodium sylvaticum (Aragon-Alcaide et al. 1996), and these sequences were later found to be derived from different parts of the CR elements (Miller et al. 1998; Presting et al. 1998; Langdon et al. 2000). The rice and maize CR subfamilies were named as CRR (CR of rice) and CRM (CR of maize), respectively (Cheng et al. 2002; Zhong et al. 2002). Both CRR and CRM elements are highly intermingled with centromere-specific satellite repeats (Cheng et al. 2002; Jin et al. 2004). Chromatin immunoprecipitation (ChIP) analysis demonstrated that CRR and CRM elements are enriched in centromeric chromatin containing the centromere-specific histone H3 variant (CenH3), suggesting that the CRR and CRM elements may play a role in centromere function (Zhong et al. 2002; Nagaki et al. 2004).
Rice chromosomes 1, 4, 8, and 10, including the centromeres of chromosomes 4 and 8, have been sequenced to high quality (Feng et al. 2002; Sasaki et al. 2002; Yu et al. 2003; Nagaki et al. 2004; Wu et al. 2004) (http://www.tigr.org/tdb/e2k1/osa1/pseudomolecules/info.shtml). We identified all of the CRR elements and their solo LTRs, which include only the LTR sequence and may be derived from illegitimate recombination within and between the CRR elements (Devos, Brown, and Bennetzen 2002), in these four chromosomes and further analyzed their structure, distribution, and divergence. Phylogenetic analysis revealed that the CRR family consists of four structurally diverged subfamilies, including two autonomous and two nonautonomous subfamilies. The autonomous and nonautonomous CRR elements show similar chromosomal distribution patterns and share substantial sequence similarities within regions required for DNA replication and integrase recognition. These results have provided new insights about the evolution and mechanism of centromeric targeting specificity of the CR retrotransposon family in grasses.
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Materials and Methods |
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Fluorescence in situ Hybridization
Oryza sativa spp. japonica cv. Nipponbare was used for cytological analyses. The fluorescence in situ hybridization (FISH) procedures on meiotic pachytene chromosomes have been described previously (Cheng et al. 2001). Primers specific to the LTRs of the four CRR subfamilies were designed. Primers include CRR1-a (AACCAGATCGCAAGCAACACTA), CRR1-b (TACATCCAAACAAAACCCAAAG), CRR2-a (CACTCGTGTTTTACTCAGGAA), CRR2-b (CAGGCAGACGGGCGGTTTAGC), noaCRR1-a (GCCACCTGCTACACTGCTGACT), noaCRR1-b (CCGACTACAACCATACGAGACG), noaCRR2-a (TCATAACTTCACACGCTCCAAT), and noaCRR2-b (TGCAATCGCTACACCACAAACG). DNA fragments corresponding to LTRs of each subfamilie were amplified from the genomic DNA of Nipponbare and were labeled as FISH probes. Polymerase chain reaction (PCR) conditions were 30 cycles at 94°C for 30 s, 55°C for 30 s, and 72°C for 1 min. Plasmid pRCS2 (Dong et al. 1998) was used as a probe to detect the rice centromere-specific satellite CentO.
ChIP-PCR
ChIP-PCR was conducted as described previously (Nagaki et al. 2004) using 1-week-old etiolated rice seedlings and purified anti-CenH3 antibody. Pre-immuno blood was used as a mock in the ChIP experiments. DNA from antibody-bound fraction and mock experiments were used as the template in PCR. PCR primers specific to each of the four CRR subfamilies were designed (table 1). Two sets of primers were designed from the 18S-25S ribosomal RNA genes (rDNA) (table 1) and were used as negative control for ChIP-PCR. PCR conditions were 30 cycles at 94°C for 30 s, 55°C for 30 s, and 72°C for 1 min. The PCR products were electrophoresed and blotted on HybondN+ membrane (Amersham Biosciences, Piscataway, NJ). The same PCR products were used as probes for Southern hybridizations. The membranes were hybridized at 65°C overnight and then washed sequentially with 2 x SSC with 0.1% SDS, 0.5 x SSC with 0.1% SDS, and 0.1 x SSC with 0.1% SDS. The signals were detected by phosphoimaging. Relative enrichment (RE) was calculated by comparing antibody-associated PCR product ratios to product ratios from mock experiments using the following formula: RE = (LTRs or rDNA1/rDNA2)antibody/(LTRs or rDNA1/rDNA2)mock. The probability (P) of the mock fractions and antibody fractions belonging to same group was analyzed by t-test.
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Results |
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Intact LTRs from the CRR elements were analyzed using ClustalX together with the previously reported CRR sequences and CR elements from maize, including CRM1 and CRM2 (Nagaki et al. 2003) and CentA (a nonautonomous CRM element) (Ananiev, Phillips, and Rines 1998). The CRR elements were clustered into four groups, with the branches having more than 97 pre-100 bootstrap test values (fig. 2). Two of the four clusters include only LTRs from the autonomous CRR elements, and the other two clusters include LTRs only from the nonautonomous CRR elements (fig. 2). We named the two autonomous clusters CRR1 and CRR2, respectively, because of their sequence similarities to CRM1 and CRM2 in maize (Nagaki et al. 2003) (fig. 2). The two nonautonomous clusters were arbitrarily named noaCRR1 and noaCRR2, respectively.
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Search for conserved domains within the polyprotein performed using RPS-Blast (Marchler-Bauer et al. 2003) allowed identification of GAG, zinc-finger, protease (PRO), reverse-transcriptase (RT), and integrase (IN) domains (table 2). The ribonuclease H (RH) domain was identified based on the presence of typical DEDD motif (Malik and Eickbush 2001). The CRR1/CRR2 elements contain all characteristic protein domains required for retrotransposition. The noaCRR1 elements contain only a partial GAG domain lacking at least part of the nucleocapsid domain defined by zinc finger. The noaCRR2 elements show heterogeneous structures. Among the six noaCRR2 elements analyzed, two of them show a similar structure to noaCRR1 elements and contain a partial GAG domain, and two elements have a complete GAG, together with the PRO domain. The remaining two elements contain no coding regions (fig. 1A). Besides these domains, putative proteins in the nonautonomous elements contain relatively large downstream regions, which have no similarity to the polyprotein of the autonomous elements. Similar to previously described CR elements (Langdon et al. 2000), the putative coding regions of newly identified CRR elements from all four groups extended into the 3' LTR.
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Age of the CRR Elements
LTR nucleotide identity was used to estimate the ages of the CRR elements using a reported nucleotide substitution rate of 6.5x109 (Gaut et al. 1996). Average age, standard deviation, youngest age, and oldest age of the CRR elements from each of the four subfamilies are listed in table 3. The average age of the two autonomous subfamilies, CRR1 and CRR2, are approximately 0.44 and 0.87 Myr, respectively. In contrast, the average age of the noaCRR1 and noaCRR2 elements are 2.13 and 3.91 Myr, respectively, which is significantly older than the autonomous elements. We did not find a correlation between the age and the chromosomal locations of the CRR elements (data not shown).
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To further confirm whether all four CRR subfamilies are associated with CenH3-associated chromatin, we conducted ChIP-PCR analysis using the rice anti-CenH3 antibody (Nagaki et al. 2004) and PCR primers designed to the LTR regions (table 1). The rDNA, which is located in the subtelomeric regions of rice chromosomes (Fukui, Ohmido, and Khush 1994), was used as controls in the ChIP-PCR analysis. A set of PCR primers was also constructed from the LTR of RIRE3, which is one of the most dominant Ty3/gypsy class of retrotransposons in the rice genome and was found in the centromeric regions of the rice chromosomes 5 (Nonomura and Kurata 2001) and 8 (Nagaki et al. 2004).
The relative enrichment (RE) of the CRR1-LTR was 3.8 (standard error [SE] = ±0.6, n = 5) on average, which is significantly higher (P < 0.003) than the RE of the rDNA control (0.9, SE = ±0.0, n = 5) (fig. 6). REs of CRR2-LTR and noaCRR1-LTR were 3.9 (SE = ±0.4, n = 5) and 7.3 (SE = ±0.7, n = 5), respectively, both significantly increased in the immunoprecipitated fraction (CRR2-LTR: P < 0.0002; noaCRR1-LTR: P < 0.00003). The RIRE3-LTR was slightly increased (RE = 1.4, SE = ±0.1, n = 5) compared with the rDNA control (P < 0.004). However, the noaCRR2-LTR was not significantly increased (RE = 0.9, SE = ±0.1, n = 5, P < 0.31) (fig. 6). These results confirmed that at least a portion of the CRR1, CRR2, and noaCRR1 elements are located within CenH3-associated chromatin. However, we failed to demonstrate the potential association of the noaCRR2 elements with CenH3-associated chromatin.
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Discussion |
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The discovery of autonomous and nonautonomous CRR elements provides another example of evolution of nonautonomous retrotransposon families. The full-size CRR elements encode for a polyprotein with all characteristic domains. Although some of the CRR1/CRR2 elements seem to be slightly mutated within the coding region, others seem to have the region intact, implying that they could be still capable of autonomous transposition, which is in agreement with the young age estimated for these elements (table 3). The noaCRR elements have different structures (fig. 1A). Most noaCRR elements contain the gag or a gag-pro gene, which is different from LARDs and TRIMs, which contain no open reading frames. The CRR and noaCRR elements share substantial sequence similarity of the LTRs and have fully conserved PBS and PPT regions (fig. 1B). There is also a strongly conserved heptanucleotide inverted repeat at the termini of LTRs (fig. 1B). The inverted repeats differ in sequence and length among different retroelements and are important for recognition by integrase (Hindmarsh and Leis 1999). Thus, the conservation of these sites suggests that autonomous and nonautonomous elements use the same or very similar enzyme machinery. The presence of young noaCRR elements in the rice genome (table 3) coupled with similar chromosomal distribution between noaCRR1 and CRR1/CRR2 elements further suggest that the noaCRR elements are likely mobilized through the retrotransposition machinery from CRR elements, a similar scenario as Dasheng and RIRE2.
It is interesting to note that most noaCRR elements contain the gag or gag-pro genes, a feature different from LARDs and TRIMs. As reverse transcription takes place only in the VLPs, nonautonomous elements must have a mechanism that allows their RNA to be packaged during the assembly of VLPs. This can be achieved by the presence of encapsidation signals that should be conserved among autonomous and nonautonomous elements. Several candidate regions could be identified within LTR, 5' UTR, and gag (data not shown). However, it remains unclear which of them, if any, serve as an actual encapsidation signal. An alternative scenario can be envisioned for some of the noaCRR2 elements. These elements encode for a protein with the GAG and PRO domains, which alone should be capable of RNA packaging, as was demonstrated in the case of retroviruses (Swanstrom and Wills 1997). The remaining enzymes supplied by autonomous elements could be assembled into VLPs by a virtue of protein-protein interactions between the GAG-PRO and GAG-PRO-POL polyproteins. Such interactions are well documented in retroviruses and are very important in the process of the virion assembly (Swanstrom and Wills 1997; Freed 1998). This scenario cannot be readily applied to noaCRR1 elements, as they lack portion of the nucleocapsid domain responsible for RNA binding. However, even the noaCRR1 proteins are likely to play some roles during the assembly process, as the appropriate coding region appears to have evolved under selection constraints. Alternatively, the discovery of several noaCRR2 elements lacking the whole coding region suggests that all necessary enzymes could be supplied in trans, like in the Dasheng and RIRE2 elements (Jiang, Jordan, and Wessler 2002).
Targeting Specificity of the CRR Elements
The CRR elements are highly concentrated in the centromeric and pericentromeric regions (fig. 5). In the centromere of rice chromosome 8, the CRR elements are highly enriched within the chromatin domain containing CenH3 (Nagaki et al. 2004). In maize, CRM elements are highly intermingled with a centromeric satellite repeat CentC, suggesting that CRM transposed preferentially into CentC satellite arrays or into other CRM elements. Maize CenH3 is almost exclusively associated with intermingled CRM/CentC sequences (Jin et al. 2004). These results suggest that CR elements in both rice and maize transposed preferentially into CenH3-associated chromatin domains.
In yeast, the Ty3 element integrates only in DNA encoding the 5' end of genes transcribed by RNA polymerase III. The mechanism of Ty3 integration appears to involve the interaction between integration complex and the TFIIIB component of the PolIII transcription apparatus (Kirchner, Connolly, and Sandmeyer 1995). The targeting of the Ty5 element into the heterochromatin domains is determined by interactions between the targeting domain of the integrase and the heterochromatin protein Sir4p (Zhu et al. 2003). The preferential integration of CRR elements within and near the CenH3-associated DNA domain suggests that the targeting mechanism of CRR elements may involve an interaction with centromeric proteins. CenH3, a histone H3 variant, would be a good candidate because it is a constitutive component of the centromeric chromatin. The Tf1 element of Schizosaccharomyces pombe preferentially inserts in intergenic regions (Behrens, Hayles, and Nurse 2000; Singleton and Levin 2002). It has recently been proposed that the Tf1 integration may be controlled by an interaction of the chromodomain located at the C terminal of the integrase with histone H3 methylated at lysine 4 (Sandmeyer 2003). The N terminal of CenH3 is significantly diverged from the N terminal of histone H3 (Henikoff, Ahmad, and Malik 2001), which would provide the specificity for recognition by the CRR elements. Gorinsek, Gubensek, and Kordis (2004) recently reported that the CR family shows clear differences in the integrase sequences from other plant LTR retrotransposons. They differ in the otherwise conserved sequence motifs in the C-terminal region of the integrase, such as in the HPVFHS motif and in two motifs of the chromodomain. It will be of great interest to test whether the chromodomain of the CRR integrase interacts with CenH3 in rice.
Interestingly, the nonautonomous CRR elements are less specific to the centromeric regions compared with the autonomous CRR elements (figs. 4 and 5). Furthermore, the LTRs of the noaCRR1 element share more sequence similarity with the LTRs of autonomous elements than with the LTRs of the noaCRR2 element (fig. 3). In parallel, noaCRR1 elements appear to target the centromeres more frequently than the noaCRR2 elements (fig. 4), especially considering the fact that we were not able to reveal an association between the noaCRR2 elements with CenH3-associated chromatin (fig. 6). These results support the hypothesis that the LTR sequences may play a role in centromere specificity of the CR family (Nagaki et al. 2003). Recognition of centromeric chromatin during noaCRR1 retrotransposition may be error prone, resulting in a less centromeric specificity of the noaCRR1 elements compared with the CRR1/CRR2 elements. Alternatively, but less likely, noaCRR1 elements may transpose using the retrotransposition machinery from other retrotransposon families, which would result in the loss of the centromeric specificity.
CRR Elements and Grass Centromere Function
It has been well documented that retrotransposition within or near genes will generate mutations or alter gene expression (Kumar and Bennetzen 1999; Hirochika 2001). However, few retrotransposons have been associated with specific structural and/or functional roles. For example, the telomeres of Drosophila chromosomes consist of long tandem arrays of two non-LTR retrotransposons, HeT-A and TART. These telomeric retrotransposons have a functional role in preventing the shortening of the chromosome ends (Pardue and DeBaryshe 2003). The putative role of the CR elements in centromere function was speculated mostly because of their centromere specificity (Miller et al. 1998; Presting et al. 1998). In maize, the core of the centromeres consist of primarily intermingled CRM/CentC sequences (Jin et al. 2004). Maize CenH3 is associated exclusively with such intermingled CentC/CRM sequences (Zhong et al. 2002; Jin et al. 2004). Association of CR elements with CenH3 has also been demonstrated in rice (Nagaki et al. 2004) (fig. 5). These recent results strongly suggest a structural and/or functional role of the CR elements in grass centromere function.
Jiang et al. (2003) recently proposed that deposition of CenH3 in centromeres is possibly a transcription-mediated event. Incorporation of CenH3 into centromeric chromatin is independent of DNA replication (Shelby, Monier, and Sullivan 2000; Ahmad and Henikoff 2001; Sullivan and Karpen 2001). DNA transcription can result in displacement of histone molecules, which may provide an opportunity for CenH3 deposition/replacement (Jiang et al. 2003). DNA transcription in CenH3-associated chromatin has been reported in a human neocentromere (Saffery et al. 2003) and in the centromere of rice chromosome 8 (Nagaki et al. 2004). Nakano et al. (2003) recently showed that activation of centromeric function of ectopically integrated alpha satellite sites on human chromosomes can be achieved by treatment with histone deacetylase inhibitors, which also increases the acetylation level of histone H3 and the transcription level of a marker gene within the ectopic centromeres. This result supports the hypothesis on the relationship between DNA transcription and centromere assembly.
LTRs usually diverge faster than the other parts of the retrotransposons. Even closely related retrotransposon families often have LTRs with no detectable sequence similarity. In contrast, the CR elements from different grass species share substantial homology in the LTR sequences. Highly conserved DNA motifs were found in the LTRs of both autonomous and nonautonomous CR elements from rice, maize, and barley (Nagaki et al. 2003). which were diverged more than 55 Myr ago (Kellogg 2001). The conservation of LTRs of CR elements from distantly related grass species suggests a selective pressure at the nucleotide level. Because the transcriptional regulatory sequences reside in the LTRs, the selection pressure of LTRs of CR elements has probably been on their capacity to initiate transcription. Transcription of CR elements and/or the flanking centromeric satellite may be an important component of centromeric chromatin assembly in the grass species (Jiang et al. 2003).
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Acknowledgements |
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Footnotes |
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