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Comparative Study
. 2008 Sep;148(1):25-40.
doi: 10.1104/pp.108.121491. Epub 2008 Jul 23.

Genome-wide analysis of transposon insertion polymorphisms reveals intraspecific variation in cultivated rice

Xuehui Huang  1 , Guojun Lu, Qiang Zhao, Xiaohui Liu, Bin Han
Affiliations
Comparative Study

Genome-wide analysis of transposon insertion polymorphisms reveals intraspecific variation in cultivated rice

Xuehui Huang et al. Plant Physiol. 2008 Sep.

Abstract

Insertions and precise eliminations of transposable elements generated numerous transposon insertion polymorphisms (TIPs) in rice (Oryza sativa). We observed that TIPs represent more than 50% of large insertions and deletions (>100 bp) in the rice genome. Using a comparative genomic approach, we identified 2,041 TIPs between the genomes of two cultivars, japonica Nipponbare and indica 93-11. We also identified 691 TIPs between Nipponbare and indica Guangluai 4 in the 23-Mb collinear regions of chromosome 4. Among them, retrotransposon-based insertion polymorphisms were used to reveal the evolutionary relationships of these three cultivars. Our conservative estimates suggest that the TIPs generated approximately 14% of the genomic DNA sequence differences between subspecies indica and japonica. It was also found that more than 10% of TIPs were located in expressed gene regions, representing an important source of genetic variation. Transcript evidence implies that these TIPs induced a series of genetic differences between two subspecies, including interrupting host genes, creating different expression forms, drastically changing intron length, and affecting expression levels of adjacent genes. These analyses provide genome-wide insights into evolutionary history and genetic variation of rice.

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Figures

Figure 1.
Figure 1.
Sequence comparison of an orthologous region between japonica Nipponbare and indica Guangluai 4. The region is approximately 492 kb in Nipponbare, from 31,616,657 to 32,108,476 bp on chromosome 4 (TIGR pseudomolecule 5.0), and approximately 394 kb in Guangluai 4. Light gray shading indicates the homologous regions, and the white areas show the indels of more than 100 bp. TEs are represented by bars of designated colors. All non-TE genes are indicated by dark lines with arrows. Exons are depicted as horizontal lines, and introns are depicted as the lines connecting exons.
Figure 2.
Figure 2.
Contribution of TIPs to large indels. TIPs and indels in the approximately 23-Mb orthologous regions of chromosome 4 are classified into seven groups according to their sizes, as shown at the bottom of the histograms. A, Bars show the number of TIPs and indels, in black and red, respectively. The blue line indicates the proportion of TIPs to indels. B, Bars show the coverage of TIPs and indels. The blue line denotes the ratio of TIPs to indels.
Figure 3.
Figure 3.
The phylogenetic relationship of three varieties, japonica Nipponbare, indica 93-11, and indica Guangluai 4, characterized by in silico analysis of RBIPs. The first node represents the divergence between two subspecies, while the second node denotes the radiation of ancestral indica into two gene pools, the ancestors of the 93-11 and Guangluai 4 gene pools, which are represented by the green ellipses. The dashed line represents the introgression between the two. I, II, and III are the expected patterns of RBIPs in the three varieties. Type I indicates the insertions that occurred in the Nipponbare genome after the divergence between the two subspecies. Type II occurred in the common ancestor of the Guangluai 4 and 93-11 gene pools, after the divergence. Type III happened in the Guangluai 4 gene pool, after the radiation of indica into at least two gene pools. Copy number, average length, and ratio of solo LTR to intact LTR are also listed.
Figure 4.
Figure 4.
Distribution of 2,041 TIPs in the rice genome. Individual transposon insertions are represented by horizontal lines, and different kinds of transposons are shown in different colors. The light gray bars on the chromosomes indicate the position of centromeres. Detailed information for each TIP is listed in Supplemental Table S2.
Figure 5.
Figure 5.
Densities of SNPs, TIPs, and repeats on rice chromosome 5 (approximately 30 Mb). At top, the azure bars indicate the numbers of TIPs per megabase. The red line shows SNP rate (per kilobase) after subtraction of repetitive regions, and the gray line shows the percentage of repetitive DNA. The distribution of TIPs on chromosome 5 is shown at bottom.
Figure 6.
Figure 6.
Examples of genetic variation types associated with TIPs. A, Two gene fragments were separated by a Dasheng insertion into the coding region of XIP-I. B, The insertion of copia in the 3′ UTR of OsWRKY8 created an alternative isoform in Nipponbare, which was a chimeric transcript possessing three additional exons from the TE. C, The first intron of a homolog of AtPUP11 was inserted by a hAT transposon, resulting in the loss of its original first exon and the gain of an additional exon deriving from the TE. D, Transposition of a large gypsy into a rice glucosyltransferase gene generated an intron of 15 kb. E, A 5′ upstream region of a gene was inserted by a hAT transposon. Homologous regions are indicated by light gray shading. Horizontal lines and arrows over/below the genomic region represent the corresponding Fl-cDNA or EST. LTR and internal sequences of transposons, TSDs, and coding regions are indicated by designated colors. The transcripts of indica in E are not found in the rice EST or Fl-cDNA database.
Figure 7.
Figure 7.
Phylogenetic and GeneChip expression analyses of the XIP-I gene. A, Phylogenetic relationship of wheat XIP-I and its homologous proteins in rice. Both wheat XIP-I and indica XIP-I are highlighted with red. OsXIP, riceXIP, RIXI, OsChib3a, and OsChib3b (Park et al., 2002) are proteins that have been identified and studied in rice. B, The small colored boxes represent the positions of the probes in the two probe sets of the Affymetrix GeneChip. The probes of OsAffx.27816.1.S1_at and OsAffx.27815.1.S1_s_at are shown with red and green, respectively. The insertion position in the gene is indicated with a black triangle. The transcription initiation site is also indicated. C and D, Plot and correlation of hybrid intensity between OsAffx.27816.1.S1_at and OsAffx.27815.1.S1_s_at in different samples from Nipponbare (C) or IR64 (D). The horizontal axis shows the intensity of the probe set OsAffx.27816.1.S1_at calculated based on the hybrid intensity of its 11 probes, while the vertical axis shows the intensity of OsAffx.27815.1.S1_s_at. Pearson's correlation coefficient was used in linear correlation analysis. The significance of the slope of the regression lines is determined from the t statistic.
Figure 8.
Figure 8.
Detection of the LTR insertion in the XIP-I gene using PCR. A, Small arrows indicate the locations of the primers used in PCR amplification. The expected sizes of PCR products in different patterns (insertion or no insertion) are also shown. B, RT-PCR analysis of XIP-I gene expression in japonica Nipponbare and indica Guangluai 4. C, Detection of the insertion in the genomic DNA of 10 indica, 11 japonica, and three wild rice varieties.
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