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Research ArticleResearch Article
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Target Site Specificity of the Tos17 Retrotransposon Shows a Preference for Insertion within Genes and against Insertion in Retrotransposon-Rich Regions of the Genome

Akio Miyao, Katsuyuki Tanaka, Kazumasa Murata, Hiromichi Sawaki, Shin Takeda, Kiyomi Abe, Yoriko Shinozuka, Katsura Onosato, Hirohiko Hirochika
Akio Miyao
aMolecular Genetics Department, National Institute of Agrobiological Sciences, Tsukuba, Ibaraki 305-8602, Japan
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Katsuyuki Tanaka
bFirst Research Division, Institute of Society for Techno-Innovation of Agriculture, Forestry, and Fisheries, Tsukuba, Ibaraki 305-0854, Japan
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Kazumasa Murata
bFirst Research Division, Institute of Society for Techno-Innovation of Agriculture, Forestry, and Fisheries, Tsukuba, Ibaraki 305-0854, Japan
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Hiromichi Sawaki
bFirst Research Division, Institute of Society for Techno-Innovation of Agriculture, Forestry, and Fisheries, Tsukuba, Ibaraki 305-0854, Japan
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Shin Takeda
aMolecular Genetics Department, National Institute of Agrobiological Sciences, Tsukuba, Ibaraki 305-8602, Japan
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Kiyomi Abe
aMolecular Genetics Department, National Institute of Agrobiological Sciences, Tsukuba, Ibaraki 305-8602, Japan
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Yoriko Shinozuka
bFirst Research Division, Institute of Society for Techno-Innovation of Agriculture, Forestry, and Fisheries, Tsukuba, Ibaraki 305-0854, Japan
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Katsura Onosato
bFirst Research Division, Institute of Society for Techno-Innovation of Agriculture, Forestry, and Fisheries, Tsukuba, Ibaraki 305-0854, Japan
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Hirohiko Hirochika
aMolecular Genetics Department, National Institute of Agrobiological Sciences, Tsukuba, Ibaraki 305-8602, Japan
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Published August 2003. DOI: https://doi.org/10.1105/tpc.012559

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    Figure 1.

    Base Preferences of Tos17 Insertion Sites.

    Average base preferences at each position were calculated based on flanking sequences at 20,458 loci. From position 1 to position 5 is the TSD sequence. Numbers with minus and plus signs are base numbers upstream and downstream, respectively, from the TSD. The percentages of A (green), C (blue), G (black), and T (red) at each position were plotted.

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    Figure 2.

    Frequency Distribution of the GC Content of Tos17-Inserted Regions and Published Rice Genomic Sequences.

    The percentages of GC for 1-kb windows centered on 20,458 insertion points were calculated, and the frequency distribution was plotted in red. For continuous rice genomic sequences, derived from PAC or BAC clones with at least 70 kb of sequence, GC contents were calculated with a 1-kb sliding window, and the frequency distribution was plotted in blue. To determine the GC content distribution of CDS, all annotated CDS sequences were first joined into one large sequence. This sequence then was split into 1-kb pieces to determine the percentage of GC and the frequency distribution (green line). To generate a frequency distribution for protein kinase and defense-related genes (pink line), each 1-kb fragment of the rice genomic sequences was searched by BLASTX against an amino acid data set containing records of protein kinase and disease resistance genes. Fragments showing matches with E values of <e-10 were included in the frequency distribution. Each frequency distribution of GC content is plotted using 1% intervals.

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    Figure 3.

    Tos17 Insertion Map on Contigs of Rice Chromosome 1.

    Contigs were assembled through a combination of BLASTN searches and the EMBOSS megamerger program. Seven remaining gaps between the contigs were joined simply. The x axes represent the position on chromosome 1. The y axes show the frequency of Tos17 insertions, retrotransposons, and genes.

    (A) Tos17 insertions.

    (B) Protein kinase genes.

    (C) Disease resistance–related genes.

    (D) Retrotransposons.

    (E) Rice ESTs.

    Frequencies were calculated at 100-kb intervals along chromosome 1. The position of the centromere is shown with a box. For (B), (C), and (D), the joined sequence of chromosome 1 was split into 1-kb fragments. Each fragment was searched with BLASTX against an amino acid data set of protein kinase genes, disease resistance genes, and retrotransposons, respectively. Gene frequencies represent the number of 1-kb fragments that have matches with E values of <e-10 for BLASTX or <e-100 for BLASTN.

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    Figure 4.

    Estimation of the Window Sizes of Tos17 Hot Spots.

    All insertion points were mapped onto public PAC and BAC sequences. The distances between adjacent Tos17 insertion points on the rice genomic sequences were obtained, and the frequency distribution of the distances was plotted in 100-bp increments. Each distance was calculated from continuous genomic sequences of at least 70 kb. Red, green, and blue bars indicate Tos17 insertions in coding, intergenic, and unknown regions, respectively.

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    Table 1.

    Functional Classes of Disrupted Genes

    CategoryNumber
 (<e-4)Number
 (<e-25)Percent
    Cell growth/division3961414.7
    Cell structure2891213.4
    Disease/defense1,17566113.8
    Energy36120.4
    Intracellular trafficking3290.4
    Metabolism5982317.0
    Protein synthesis69350.8
    Protein targeting and storage138361.6
    Secondary metabolism88281.0
    Signal transduction7683579.0
    Transcription3642034.3
    Transporters3641804.3
    Transposons7044508.3
    Unclear classification3,4741,07240.9
    Total hits8,4953,536
    Total independent insertions16,784
    • A total of 42,292 sequences (from 4316 lines) were analyzed. The hit ratio in independent flanking sequences was 50.6%.

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    Table 2.

    Disrupted Genes with High Scores

    Accession NumberaEntrybPutative IdentificationOrganismcScoreE Value
    AG020730BAA24449.16-4 photolyaseArabidopsis thaliana89.74e-31
    AG020828CAB41466.1Inositol 1,4,5-trisphosphate 5-phosphataseArabidopsis thaliana69.14e-11
    AG020899CAB88264.1Callose synthase catalytic subunit–likeArabidopsis thaliana2055e-53
    AG020942AAF74563.1Heat stress transcription factor A3Lycopersicon peruvianum1193e-26
    AG020963AAF31730.1Phosphoribosylformylglycinamidine synthase–likeArabidopsis thaliana1591e-50
    AG020968BAA94795.1S-Adenosyl-l-Met:l-Met S-methyltransferaseHordeum vulgare90.51e-27
    AG021106AAD37810.1NADP-specific isocitrate dehydrogenaseOryza sativa77.65e-14
    AG021182BAB11335.1Eukaryotic release factor 1Arabidopsis thaliana1812e-45
    AG021242JDMU1DNA-directed RNA polymerase II largest chainArabidopsis thaliana3576e-98
    AG021377AAF23509.1Fructose-1,6-bisphosphatasePorteresia coarctata1012e-26
    AG021380BAA94509.1Protein kinase 1Populus nigra1845e-46
    AG021400BAB08003.1Adenine phosphoribosyltransferaseHordeum vulgare93.68e-19
    AG021445T03846Plasma membrane H+-ATPaseOryza sativa1023e-45
    AG021473T00020Bacterial blight resistance protein Xa1Oryza sativa2891e-77
    AG021543T01661DNA (cytosine-5-)-methyltransferaseZea mays90.12e-53
    AG021593CAA65053.1Pro transporter 2Arabidopsis thaliana1162e-25
    AG021694BAA35120.1NADH-dependent glutamate synthaseOryza sativa2661e-70
    AG021741S64721Protoporphyrin IX magnesium chelatase precursorHordeum vulgare433e-121
    AG021763BAB10513.1NAM (no apical meristem)–likeArabidopsis thaliana1148e-25
    AG021795CAA94437.1PDR5-like ABC transporterSpirodela polyrrhiza1366e-52
    AG021958AAC39369.1Trehalose-6-phosphate phosphataseArabidopsis thaliana65.21e-24
    AG021996BAB03631.1Putative protein kinase Xa21Oryza sativa2291e-59
    AG022284S47582High-affinity potassium uptake transporterTriticum aestivum1623e-39
    AG022440O23755Elongation factor 2Beta vulgaris1612e-39
    AG022521P30298Sucrose synthase 1Oryza sativa85.86e-17
    AG022936P17801Putative receptor protein kinase zmpk1 precursorZea mays1624e-61
    AG023034AAF26975.1Stelar K+ outward rectifying channelArabidopsis thaliana98.31e-25
    AG023207T09999Cytochrome P450Catharanthus roseus1208e-40
    AG023219P10931Phytochrome AOryza sativa2582e-68
    AG023602BAB08867.1DNA-3-methyladenine glycosylaseArabidopsis thaliana65.26e-26
    AG023738AAD40979.1Peroxisomal copper-containing amine oxidaseGlycine max1961e-49
    AG023869BAA34861.1Importin-β1Oryza sativa1323e-30
    AG023905BAB10038.1DihydropyrimidinaseArabidopsis thaliana88.52e-25
    AG023996BAA90462.1Chlorophyll a oxygenaseArabidopsis thaliana1009e-31
    AG024163P52421Phosphoribosylamine-Gly ligaseVigna unguiculata2449e-64
    AG024164T04103Sucrose phosphate synthaseOryza sativa3114e-84
    AG024224AAC18440.1Argonaute proteinArabidopsis thaliana68.71e-21
    AG024327AAC49302.1ErectaArabidopsis thaliana1574e-38
    AG024330P52711Ser carboxypeptidase II-3Hordeum vulgare1172e-25
    • ↵a Accession number of the flanking sequence.

    • ↵b Entry name of the hit protein.

    • ↵c Source of the protein showing the highest similarity score.

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    Table 3.

    Location of Tos17 Insertions in Published Rice Genomic Sequences

    LocationNumber of
 InsertionsPercentTotal Target
 Length (bp)PercentAverage
 Interval (bp)
    Exon2,26011.025,780,2874.911,407
    Intron1,8379.029,727,9485.716,182
    Intergenic1,9509.578,227,31415.040,116
    Unknown14,41270.4387,279,81474.326,872
    Total20,458521,015,36325,467
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Target Site Specificity of the Tos17 Retrotransposon Shows a Preference for Insertion within Genes and against Insertion in Retrotransposon-Rich Regions of the Genome
Akio Miyao, Katsuyuki Tanaka, Kazumasa Murata, Hiromichi Sawaki, Shin Takeda, Kiyomi Abe, Yoriko Shinozuka, Katsura Onosato, Hirohiko Hirochika
The Plant Cell Aug 2003, 15 (8) 1771-1780; DOI: 10.1105/tpc.012559

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Target Site Specificity of the Tos17 Retrotransposon Shows a Preference for Insertion within Genes and against Insertion in Retrotransposon-Rich Regions of the Genome
Akio Miyao, Katsuyuki Tanaka, Kazumasa Murata, Hiromichi Sawaki, Shin Takeda, Kiyomi Abe, Yoriko Shinozuka, Katsura Onosato, Hirohiko Hirochika
The Plant Cell Aug 2003, 15 (8) 1771-1780; DOI: 10.1105/tpc.012559
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The Plant Cell Online: 15 (8)
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