- Research article
- Open Access
Comparison of Genomes of Three Xanthomonas oryzae Bacteriophages
- Chia-Ni Lee†1,
- Rouh-Mei Hu†2,
- Teh-Yuan Chow3,
- Juey-Wen Lin4,
- Hui-Yi Chen5,
- Yi-Hsiung Tseng3Email author and
- Shu-Fen Weng1Email author
© Lee et al; licensee BioMed Central Ltd. 2007
- Received: 05 January 2007
- Accepted: 29 November 2007
- Published: 29 November 2007
Xp10 and OP1 are phages of Xanthomonas oryzae pv. oryzae (Xoo), the causative agent of bacterial leaf blight in rice plants, which were isolated in 1967 in Taiwan and in 1954 in Japan, respectively. We recently isolated the Xoo phage Xop411.
The linear Xop411 genome (44,520 bp, 58 ORFs) sequenced here is 147 bp longer than that of Xp10 (60 ORFs) and 735 bp longer than that of OP1 (59 ORFs). The G+C contents of OP1 (51%) and Xop411 and Xp10 (52% each) are less than that of the host (65%). The 9-bp 3'-overhangs (5'-GGACAGTCT-3') in Xop411 and Xp10 are absent from OP1. More of the deduced Xop411 proteins share higher degrees of identity with Xp10 than with OP1 proteins, while the right end of the genomes of Xp10 and OP1, containing all predicted promoters, share stronger homology. Xop411, Xp10, and OP1 contain 8, 7, and 6 freestanding HNH endonuclease genes, respectively. These genes can be classified into five groups depending on their possession of the HNH domain (HNN or HNH type) and/or AP2 domain in intact or truncated forms. While the HNN-AP2 type endonuclease genes dispersed in the genome, the HNH type endonuclease genes, each with a unique copy, were located within the same genome context. Mass spectrometry and N-terminal sequencing showed nine Xop411 coat proteins, among which three were identified, six were assigned as coat proteins (4) and conserved phage proteins (2) in Xp10. The major coat protein, in which only the N-terminal methionine is removed, appears to exist in oligomeric forms containing 2 to 6 subunits. The three phages exhibit different patterns of domain duplication in the N-terminus of the tail fiber, which are involved in determination of the host range. Many short repeated sequences are present in and around the duplicated domains.
Geographical separation may have confined lateral gene transfer among the Xoo phages. The HNN-AP2 type endonucleases were more likely to transfer their genes randomly in the genome and may degenerate after successful transmission. Some repeated sequences may be involved in duplication/loss of the domains in the tail fiber genes.
- Lateral Gene Transfer
- Bacterial Leaf Blight
- Tail Fiber
- Lysozyme Gene
- Tail Protein
Xanthomonas oryzae pv. oryzae (Xoo) is a gram-negative plant pathogenic bacterium that causes leaf blight in rice plants, thus having a serious effect on rice production in Taiwan, China, Japan, India, and South America . Agrochemicals have been somewhat effective for disease control, although biological control using bacteriophages has been considered . In addition, phages that specifically infect Xoo have been used to type Xoo hosts in the field [3, 4].
Among the Xoo phages are the lytic phages Xp10, Xp12, OP1, and OP2, and the filamentous phages Xf and phiXo [2–8]. Recently, the genomic sequences of Xp10 (44,373 bp, 60 ORFs), OP1 (43,785 bp, 59 ORFs), and OP2 (46,643 bp, 62 ORFs) were determined. Xp10 and OP1 both have linear genomes and share high degrees of similarity at both the nucleotide and amino acid levels [2, 6]. In contrast, OP2 has a circularly permuted and terminally redundant genome, which differs in sequence from those of Xp10 and OP1 [2, 6, 8]. Xp15 is a phage of X. campestris pv. pelargonii; its genomic sequence (55,770 bp) is available in the NCBI database (AY986977).
We recently isolated a Xoo bacteriophage, Xop411, from rice plants from a rice paddy near National Chung Hsing University that showed serious symptoms of bacterial leaf blight . During our sequencing of the Xop411 phage genome, the genomic sequences of Xp10 and OP1 were published [2, 6]. Since comparative analysis of several bacteriophages from a single species offers a unique opportunity to study the mechanisms that drive prokaryotic genetic diversity , we compared the sequence of Xop411 with those of Xp10, isolated in Taiwan in 1967, and OP1, isolated in Japan in 1954 [2, 4, 6, 7].
Assignments of Xop411 genes
Comparison of proteins deduced from the genes of X. oryzae phages Xop411, Xp10, and OP1.
Xop411 with Xp10
Xop411 with OP1
Xp10 with OP1
id (%)/aligned aa
id (%)/aligned aa
id (%)/aligned aa
61/134 (p17) a
65/134 (ORF31) b
64/130 (p31.1) a
55/134 (ORF58) b
61/134 (p42.1) a
63/142 (p55.1) a
100/64 (p06) a
69/56 (ORF4) b
65/49 (ORF3) b
51/35 (ORF58) b
66/171 (p17) c
62/163 (ORF31) b
64/164 (ORF31) b
65/164 (p50) c
51/168 (ORF58) b
57/169 (ORF58) b
61/166 (p58) c
61/134 (p03) c
71/157 (p50) c
68/158 (ORF31) b
69/163 (p50) c
67/157 (p58) c
56/157 (ORF58) b
69/166 (p58) c
65/155 (p17) c
64/164 (p17) c
63/124 (p03) c
65/134 (p03) c
100/112 (p41) a
97/113 (ORF41) b
100/112 (p40) c
97/113 (p40) c
68/165 (p17) c
65/163 (ORF31) b
65/164 (p58) c
58/164 (ORF58) b
66/163 (p50) c
61/134 (p03) c
65/164 (p17) a
70/162 (p31.1) a
69/163 (ORF31) b
66/163 (p42.1) a
53/163 (ORF58) b
66/168 (p55.1) a
67/64 (p53) c
74/58 (ORF53) b
75/44 (p53) c
43/55 (p17) c
42/42 (ORF31) b
50/36 (p58) c
53/26 (p58) c
50/22 (ORF50) b
52/36 (p50) c
44/43 (p50) c
45/37 (p17) c
66/168 (p50) c
64/162 (ORF31) b
66/163 (p58) c
55/163 (ORF58) b
65/169 (p17) c
63/142 (p03) c
38/104 (p17) c
35/138 (ORF31) b
39/104 (p03) c
32/103 (ORF58) b
31/173 (p50) c
37/103 (p58) c
37/114 (p17) c
34/116 (ORF31) b
57/169 (p17) c
35/122 (p50) c
35/110 (ORF58) b
56/167 (p58) c
36/98 (p58) c
53/163 (p50) c
35/98 (p03) c
55/134 (p03) c
Holin genes required for host lysis were not assigned for Xp10 and OP1 [2, 6]. These genes are usually small and adjacent to the cognate lysozyme genes, with their protein products usually containing at least one transmembrane domain (TMD) and a hydrophilic C-terminal domain . In Xop411, p27.1 (98 aa, with one TMD at aa 25–47), located upstream of the previously characterized lysozyme gene (p28) , was assigned as the putative holin gene. However, since p27.1 overlaps with p28 by 104 bp and lacks a hydrophilic C-terminal domain, it is unclear whether it encodes holin function. A corresponding ORF was identified in OP1, but the corresponding region in Xp10 was assigned to the N-terminus of the lysozyme gene (Table 1).
The next best matched ORFs other than those from Xp10 and OP1
The deduced Xop411 proteins also share similarities with proteins other than those of Xp10 and OP1, and proteins encoded in five Xop411 regions are worth noting (see Additional file 2): 1) The tail-related proteins p19 to p22, encoded in a 5.9-kb region, share 33–44% identity (55–63% similarity) with ORFs of the X. campestris pv. pelargonii phage Xp15. 2) Proteins p26 to p28, encoded in a 2.3-kb region and including tail fiber and phage lysozyme, show 33–48% identity to proteins from Chromobacterium violaceum. 3) Proteins p35 to p37, encoded in a 2.1-kb region, share 30–47% identity with proteins from Pseudomonas aeruginosa. 4) Proteins p38 to p41, encoded in a 4.3-kb region, show 38–45% identity to proteins from Burkholderia pseudomallei. 5) Protein p33 shares 60% identity with a protein from Bradyrhizobium sp. In addition, Xop411 p08 (ClpP protease), p28 (lysozyme) and p39 (DNA polymerase I) are similar to proteins from Xylella fastidiosa (25–38% identity) and X. axonopodis pv. citri (42% identity) (see Additional file 2). These data suggest that Xoo phages have actively participated in gene transfer with several organisms. In contrast, the Xoo genome did not contain homologues with significant similarity (i.e. with expected values less than e-4) to the proteins of the three phages. Since the Xoo phages are lytic, opportunities to exchange genetic material with the host may have been rare.
Gene products related to endonucleases of the HNH family
Members of the HNH endonuclease family are encoded by free-standing ORFs between genes or within introns or inteins in viruses, bacteriophages, and bacteria, as well as in eukaryotic nuclear and organellar genomes . Most of these proteins are homing endonucleases involved in the mobility of their own genes or of the introns/inteins in which they are located [13–15]. These HNH proteins are characterized by the motif His-Asn-His at the N-terminus but share little overall sequence similarity and can be classified into 8 subsets . Proteins of the second subset usually consist of an HNN domain and an adjacent DNA-binding domain, AP2 (Pfam:PF00847) or IENRI (Smart:SM00479), and are found primarily in phage genomes [17, 18]. For example, multiple copies of HNH endonuclease genes are present in the sequenced genomes of coliphages RB16 (DQ023482-7), RB43 (NC_007023), T1 , Rtp  and T5  as well as in the lactophage bIL170 .
We found that all the HNN domain-containing proteins of the Xoo phages have conserved Asp/His residues flanked by two quasi-conserved boxes (HRLAWLL and WP) at the N-terminus and three conserved boxes (DNR, NLRE and EN) at the C-terminus, but do not have either metal-binding cysteine-dyads (CX2C) or conserved GG motifs (Figure 2A). The lack of a metal-binding motif suggests that these HNN type endonucleases may not require zinc ion to function. Since most HNN-AP2/IENRI proteins are intron-encoded site-specific endonucleases , the presence of multiple HNN-AP2 endonuclease genes in all three Xoo phage genomes suggests that these genes, like the homing-endonuclease genes (HEGs), are able to self-duplicate in the genome. However, since no conserved sequences could be identified in the flanking regions of these endonuclease genes and their genomic locations varied among the three phages, it is likely that transmission of these HNN-AP2 endonuclease genes was sequence-independent.
The HNH domains of the group IV proteins, which share higher degrees of similarity with the consensus HNH domain, have two cysteine-dyads (CX2C) flanking the conserved Asp/His residues, suggesting that zinc ion is required for their function, as well as two boxes (DX2NL and CH) on the C-terminal side of each domain (Figure 2A). These group IV proteins are similar to the HNH-type protein (gp13) found in the lactophage bIL170, which has two cysteine-dyads (CX2CX36CX2C) and no DNA-binding motif . As endonucleases of this type are present as unique copies at the analogous positions of the Xoo phage genomes (the right end), they may have specific functions other than transposition, similar to the HNN-AP2 type endonucleases.
Promoters and terminators
We found that the nucleotide sequences between the end of p55 and the right end of the genome were highly variable in the three Xoo phages, with Xp10 and OP1 being more similar to each other than either were to Xop411, and segments with higher degrees of identity present at different positions (see Additional file 4). Mosaicism of the common segments suggests that these phages have undergone numerous recombination events, possibly during co-infections, resulting in gene rearrangements and insertion/deletion. In Xp10, the intergenic region between p57 and p58 separates the genes transcribed leftward and rightward and contains all six promoters [6, 29, 30]. Based on a similarity search, we located putative promoters resembling those of Xp10 in Xop411 and OP1. We found that the promoter sequences in Xp10 and OP1 were highly conserved, but shared lower degrees of identity with the Xop411 promoters (see Additional file 5). In addition, Xop411 had five sequences located between p56 and p57, and one sequence, P3, between p57.1 and p58, whereas OP1 had four sequences located between ORF57 and ORF58 and two, Pup and φP1, contained within ORF57 (see Additional file 4).
Predicted terminators in Xp10, Xop411, and OP1 genome.
CTGCCC TACTTATGGGCAG TTT
GGGAGGGGC TGGGAAACTGGCCCCTCTC TTT
GGGAGGGGC TGGGGGAACTGGCCCCTCTC TTT
GAGAGGGGC TAGGAAACTGGCCCCTCTC TTT
GGGGCAGG GTTTCCTGCCCC ATTT
GGGGCAGGG TTTCCTGCCCC ATTT
GGGGCAGG CTTTCCCTGCCC CTTT
GGGAGGG AGCTA AGCC TTAATGGC CTAGCCCCTCCC TTTTTTT
ATAGGGGACC TATTGCC TTTAATGGCA GGGTCCCCT TTTTTT
GGGAGGG AGCTA AGCC TTTAATGGC CTAGCCCCTCCC TTTTTT
CTGAACG ATCCGTTCAG TTT
CTGAACG GCTCGTTCAG TTT
CTGAACG ATCCGTTCAG TTT
Domain duplications in tail fiber and implications in host range
Japanese isolates of Xoo can be classified into four phagovars, based on their susceptibility to OP1, with host-range mutants of OP1 capable of infecting different phagovars . Sequencing of the tail fiber genes from these phage strains revealed that changes in host range are due to duplications in at least one of three domains (domains 1, 2, and 3) in ca. 118 aa at the N-terminus (see Additional file 6). This is similar to findings in other phages; for example, the host range of T4 is expanded by duplications of a small region of the tail fiber adhesin . Amino acid sequence alignments showed that OP1 possesses domains -1-2-3-, Xp10 has domains -1-2-2-2-3-  and Xop411 exhibits domains -1-2-3-3-3- (see Additional file 6). Interestingly, while OP1 and OPh1 have the same domain architecture (-1-2-3-) and no drastic changes in the surrounding amino acid residues, OP1 infects only phagovar A whereas OP1h infects only phagovar B (see Additional file 6) . This finding suggests that these related Xoo phages might use a complex structure, also containing other component(s), to determine the host range, with mutations in the latter component(s) altering the host range. Further tests are needed to understand the host ranges of Xop411 and Xp10.
In mouse minisatellite Pc-1, tandem repeats of d(GGCAG)n, which can facilitate the formation of a telomere-like intra-molecular folded-back quadruplex structure, have been shown to be hotspots of recombination during meiosis [32–34]. The genes encoding the tail fibers of the Xoo phages contain many short repeats (see Additional File 7), including i) inverted repeats that are all located outside the domains, which may be important in the acquisition/loss of domain architectures, ii) direct G-rich pentanucleotide (GGCAG) repeats at both ends of domains 1 and 2, and iii) a direct G-rich octanucleotide (CAGGCCGC) repeat flanking domain 3. It is currently unclear whether the presence of these short direct repeats can facilitate the duplication/deletion of the tail fiber domains by recombination, as observed for mouse minisatellite Pc-1. Inoue et. al. proposed that the HNH-family proteins may be involved in domain duplication via recombination using Holliday junction structures as the intermediates , but it is not clear if this is the mechanism occurring here.
Identification of virion proteins
The head portal protein, p07, with a calculated MW of 47 kDa, was found in the 47- and 31-kDa bands, suggesting that the unprocessed and processed forms co-exist in the virions. LC-MS/MS analysis showed that the 31-kDa band contained another protein, p26, which was identified as the tail fiber in Xp10 . N-terminal sequencing showed that the 22-kDa band was p14, the major tail protein in Xp10. The 13-kDa band was also a doublet, containing p10 (phage conserved protein in Xp10) and p19 (tail protein). The 160-, 105-, and 11-kDa bands were identified as p22 (tail protein), p18 (tail length tape measure protein), and p13 (phage conserved protein in Xp10), respectively. In summary, six more proteins than those identified for Xp10 were found here, and the conserved proteins p10 and p13 in Xp10 were found to be phage coat proteins.
The 5 host proteins in the 4 bands were TonB-dependent receptor FyuA (90-kDa), outer membrane protein MopB and hypothetical protein XOO0584 (33-kDa), MopB and colicin receptor protein CirA (28-kDa), and hypothetical protein XOO4199 (19-kDa). Since the experiments were repeated four times using virions freshly purified by ultracentrifugation, the consistent presence of these proteins indicates that they were rather tightly associated with the phage particles.
Our results, showing that Xop411 and Xp10 have the same G+C content and that more of the deduced Xop411 proteins share higher degrees of identity with Xp10 than with OP1 proteins, indicate that the two phages isolated in Taiwan are more closely related to each other than they are to OP1. Thus, geographical separation may have limited lateral gene transfers between phages and other sources. However, our finding that more of the DNA sequences are conserved by Xp10 and OP1 in the region between p55 and the right end of the genome, a region containing the predicted promoters, suggests that Xop411 has undergone sequence rearrangements and insertions/deletions to a greater degree. The HNN-AP2 type endonucleases may have transferred their genes randomly and begun degenerating after successful horizontal transmission, whereas the HNH type endonucleases, each with one copy, were located within the same genome context. Comparison of the host range and the architecture of the duplicated domains in the N-terminus of the tail fiber proteins suggests that the Xoo phages may need additional components for adsorption. Some of the repeated sequences in and around the domains may be involved in duplication/loss of the domains. We identified 6 more proteins than those identified for Xp10, with p10 and p13 shown to be phage coat proteins.
Bacteria, bacteriophages, and growth conditions
X. oryzae pv. oryzae (Xoo) was cultivated in Tryptic Soy Broth or Agar (Bacto™) at 28°C and Escherichia coli was grown in LB medium at 37°C. Ampicillin (50 μg/ml) was added when necessary. The procedures described previously  were used for plaque assay, phage propagation (using Xoo strain 21 as the host), purification of phage particles, and isolation and restriction enzyme digestion of phage DNA.
The purified phage DNA was treated in a HydroShear (GeneMachines, San Carlos, CA). Fragments of 1.0 to 3.0 kb were isolated and ligated into the Eco RV site of pBluescript II SK. Clones were randomly picked and subjected to nucleotide sequencing (ABI 3700). To determine the 3'-protruding terminal sequences (gap closure), the Xop411 genomic DNA was treated with or without Klenow enzyme, using its 3'→5' exonuclease activity and ligated using T4 ligase, and the ligation products were PCR-amplified separately with a pair of primers annealed close to the ends, followed by sequencing of the amplicons. Thus the extra nucleotides, obtained from the PCR product amplified on the template that had not been treated with Klenow enzyme, represented the 3'-protruding sequence. A+T content was analyzed by using the program available online . DNA sequences were assembled using the SeqMan program from the DNASTAR package (DNASTAR, Madison, WI) and analyzed with NCBI software . ORF was predicted using GeneMark. The nucleotide sequence of phage Xop411 has been deposited in GenBank under accession no. DQ777876.
HNH endonucleases were identified by searching for conserved domains as well as similarities to the endonucleases identified in Xp10 . The BLAST program was used to search for nucleotide and amino acid similarities, and phylogenetic analysis was performed using the parsimony method (Phylip package ver. 3.66). Bootstrap values were obtained for a consensus based on 1000 randomly generated trees using SEQBOOT and CONSENSE.
Sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) and LC-MS/MS analysis
Phage particles purified by ultracentrifugation were mixed with sample buffer, heated in a boiling water bath for 3 min, and subjected to SDS-PAGE separation in 12% or 6% (w/v) polyacrylamide gel. Protein bands were visualized by staining the gels with Coomassie brilliant blue, excised from the gels and subjected to LC-MS/MS (ABI Qstar System) analysis at the Biotechnology Center, National Chung Hsing University.
N-terminal amino acid sequencing of proteins
The proteins from the Xop411 particles separated in SDS-PAGE were transferred to polyvinylidene difluoride membranes and stained with Coomassie brilliant blue. Membrane strips containing the isolated protein bands were excised and subjected to Edman degradation to determine their N-terminal sequences (477A sequencer, PE Applied Biosystems).
This study was supported by grant No. NSC93-2317-B-005-007- and NSC94-2317-B-005-009- from National Science Council of Republic of China and No. 93-B-FA05-1-4 from Program for Promoting University Academic Excellence, Ministry of Education, Republic of China.
- Swings JG, Civerolo EL: Xanthomonas. 1993, London, Glasgow, New York, Tokyo, Melbourne, Madras , Chapman and Hall, 30-40.View ArticleGoogle Scholar
- Inoue Y, Matsuura T, Ohara T: Bacteriophage OP1, lytic for Xanthomonas oryzae pv. oryzae, changes its host range by duplication and deletion of the small in the deduced tail fiber gene. J Gen Plant Pathol. 2006, 72: 111-118. 10.1007/s10327-005-0252-x.View ArticleGoogle Scholar
- Kuo TT, Huang TC, Wu RY, Chen CP: Phage Xp12 of Xanthomonas oryzae (Uyeda et Ishiyama) Dowson. Can J Microbiol. 1968, 14 (10): 1139-1142.PubMedView ArticleGoogle Scholar
- Kuo TT, Huang TC, Wu RY, Yang CC: Characterization of three bacteriophages of Xanthomonas oryzae. Dowson Bot Bull Acad Sinica. 1967, 8: 246-257.Google Scholar
- Kuo TT, Huang TC, Chow TY: A filamentous bacteriophage from Xanthomonas oryzae. Virology. 1969, 39 (3): 548-555. 10.1016/0042-6822(69)90102-0.PubMedView ArticleGoogle Scholar
- Yuzenkova J, Nechaev S, Berlin J, Rogulja D, Kuznedelov K, Inman R, Mushegian A, Severinov K: Genome of Xanthomonas oryzae bacteriophage Xp10: an odd T-odd phage. J Mol Biol. 2003, 330 (4): 735-748. 10.1016/S0022-2836(03)00634-X.PubMedView ArticleGoogle Scholar
- Wakimoto SS: Classification of strains of X. oryzae on the basis of their susceptibility against bacteriophages. Ann Pytopathol pathol Soc Japan. 1960, 25: 193-198.View ArticleGoogle Scholar
- Inoue Y, Matsuura T, Ohara T: Sequence analysis of the genome of OP2, a lytic bacteriophage of Xanthomonas oryzae pv. oryzae. J Gen Plant Pathol. 2006, 72: 104-110. 10.1007/s10327-005-0259-3.View ArticleGoogle Scholar
- Lee CN, Lin JW, Chow TY, Tseng YH, Weng SF: A novel lysozyme from Xanthomonas oryzae phage varphiXo411 active against Xanthomonas and Stenotrophomonas. Protein Expr Purif. 2006, 50 (2): 229-237. 10.1016/j.pep.2006.06.013.PubMedView ArticleGoogle Scholar
- Kwan T, Liu J, DuBow M, Gros P, Pelletier J: The complete genomes and proteomes of 27 Staphylococcus aureus bacteriophages. Proc Natl Acad Sci U S A. 2005, 102 (14): 5174-5179. 10.1073/pnas.0501140102.PubMed CentralPubMedView ArticleGoogle Scholar
- Lee BM, Park YJ, Park DS, Kang HW, Kim JG, Song ES, Park IC, Yoon UH, Hahn JH, Koo BS, Lee GB, Kim H, Park HS, Yoon KO, Kim JH, Jung CH, Koh NH, Seo JS, Go SJ: The genome sequence of Xanthomonas oryzae pathovar oryzae KACC10331, the bacterial blight pathogen of rice. Nucleic Acids Res. 2005, 33 (2): 577-586. 10.1093/nar/gki206.PubMed CentralPubMedView ArticleGoogle Scholar
- Wang IN, Smith DL, Young R: Holins: the protein clocks of bacteriophage infections. Annu Rev Microbiol. 2000, 54: 799-825. 10.1146/annurev.micro.54.1.799.PubMedView ArticleGoogle Scholar
- Dalgaard JZ, Klar AJ, Moser MJ, Holley WR, Chatterjee A, Mian IS: Statistical modeling and analysis of the LAGLIDADG family of site-specific endonucleases and identification of an intein that encodes a site-specific endonuclease of the HNH family. Nucleic Acids Res. 1997, 25 (22): 4626-4638. 10.1093/nar/25.22.4626.PubMed CentralPubMedView ArticleGoogle Scholar
- Stoddard BL: Homing endonuclease structure and function. Q Rev Biophys. 2005, 38 (1): 49-95. 10.1017/S0033583505004063.PubMedView ArticleGoogle Scholar
- Shen BW, Landthaler M, Shub DA, Stoddard BL: DNA binding and cleavage by the HNH homing endonuclease I-HmuI. J Mol Biol. 2004, 342 (1): 43-56. 10.1016/j.jmb.2004.07.032.PubMedView ArticleGoogle Scholar
- Mehta P, Katta K, Krishnaswamy S: HNH family subclassification leads to identification of commonality in the His-Me endonuclease superfamily. Protein Sci. 2004, 13 (1): 295-300. 10.1110/ps.03115604.PubMed CentralPubMedView ArticleGoogle Scholar
- Magnani E, Sjolander K, Hake S: From endonucleases to transcription factors: evolution of the AP2 DNA binding domain in plants. Plant Cell. 2004, 16 (9): 2265-2277. 10.1105/tpc.104.023135.PubMed CentralPubMedView ArticleGoogle Scholar
- Shigyo M, Hasebe M, Ito M: Molecular evolution of the AP2 subfamily. Gene. 2006, 366 (2): 256-265. 10.1016/j.gene.2005.08.009.PubMedView ArticleGoogle Scholar
- Roberts MD, Martin NL, Kropinski AM: The genome and proteome of coliphage T1. Virology. 2004, 318 (1): 245-266. 10.1016/j.virol.2003.09.020.PubMedView ArticleGoogle Scholar
- Wietzorrek A, Schwarz H, Herrmann C, Braun V: The genome of the novel phage Rtp, with a rosette-like tail tip, is homologous to the genome of phage T1. J Bacteriol. 2006, 188 (4): 1419-1436. 10.1128/JB.188.4.1419-1436.2006.PubMed CentralPubMedView ArticleGoogle Scholar
- Wang J, Jiang Y, Vincent M, Sun Y, Yu H, Wang J, Bao Q, Kong H, Hu S: Complete genome sequence of bacteriophage T5. Virology. 2005, 332 (1): 45-65. 10.1016/j.virol.2004.10.049.PubMedView ArticleGoogle Scholar
- Crutz-Le Coq AM, Cesselin B, Commissaire J, Anba J: Sequence analysis of the lactococcal bacteriophage bIL170: insights into structural proteins and HNH endonucleases in dairy phages. Microbiology. 2002, 148 (Pt 4): 985-1001.PubMedView ArticleGoogle Scholar
- Crooks GE, Hon G, Chandonia JM, Brenner SE: WebLogo: a sequence logo generator. Genome Res. 2004, 14 (6): 1188-1190. 10.1101/gr.849004.PubMed CentralPubMedView ArticleGoogle Scholar
- Petrov VM, Nolan JM, Bertrand C, Levy D, Desplats C, Krisch HM, Karam JD: Plasticity of the gene functions for DNA replication in the T4-like phages. J Mol Biol. 2006, 361 (1): 46-68. 10.1016/j.jmb.2006.05.071.PubMedView ArticleGoogle Scholar
- Burt A, Koufopanou V: Homing endonuclease genes: the rise and fall and rise again of a selfish element. Curr Opin Genet Dev. 2004, 14 (6): 609-615. 10.1016/j.gde.2004.09.010.PubMedView ArticleGoogle Scholar
- Wessler SR: Homing into the origin of the AP2 DNA binding domain. Trends Plant Sci. 2005, 10 (2): 54-56. 10.1016/j.tplants.2004.12.007.PubMedView ArticleGoogle Scholar
- Goddard MR, Burt A: Recurrent invasion and extinction of a selfish gene. Proc Natl Acad Sci U S A. 1999, 96 (24): 13880-13885. 10.1073/pnas.96.24.13880.PubMed CentralPubMedView ArticleGoogle Scholar
- Sandegren L, Sjoberg BM: Distribution, sequence homology, and homing of group I introns among T-even-like bacteriophages: evidence for recent transfer of old introns. J Biol Chem. 2004, 279 (21): 22218-22227. 10.1074/jbc.M400929200.PubMedView ArticleGoogle Scholar
- Semenova E, Djordjevic M, Shraiman B, Severinov K: The tale of two RNA polymerases: transcription profiling and gene expression strategy of bacteriophage Xp10. Mol Microbiol. 2005, 55 (3): 764-777. 10.1111/j.1365-2958.2004.04442.x.PubMedView ArticleGoogle Scholar
- Djordjevic M, Semenova E, Shraiman B, Severinov K: Quantitative analysis of a virulent bacteriophage transcription strategy. Virology. 2006, 354 (2): 240-251. 10.1016/j.virol.2006.05.038.PubMedView ArticleGoogle Scholar
- Tetart F, Repoila F, Monod C, Krisch HM: Bacteriophage T4 host range is expanded by duplications of a small domain of the tail fiber adhesin. J Mol Biol. 1996, 258 (5): 726-731. 10.1006/jmbi.1996.0281.PubMedView ArticleGoogle Scholar
- Mitani K, Takahashi Y, Kominami R: A GGCAGG motif in minisatellites affecting their germline instability. J Biol Chem. 1990, 265 (25): 15203-15210.PubMedGoogle Scholar
- Tanaka E, Fukuda H, Nakashima K, Tsuchiya N, Seimiya H, Nakagama H: HnRNP A3 binds to and protects mammalian telomeric repeats in vitro. Biochem Biophys Res Commun. 2007, 358 (2): 608-614. 10.1016/j.bbrc.2007.04.177.PubMedView ArticleGoogle Scholar
- Nakagama H, Higuchi K, Tanaka E, Tsuchiya N, Nakashima K, Katahira M, Fukuda H: Molecular mechanisms for maintenance of G-rich short tandem repeats capable of adopting G4 DNA structures. Mutat Res. 2006, 598 (1-2): 120-131.PubMedView ArticleGoogle Scholar
- A. B. I. M. [http://www.iut-arles.up.univ-mrs.fr/w3bb/d_abim/riche-adn.html]
- NCBI. [http://www.ncbi.nlm.nih.gov/]
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.