Rapid genome divergence at orthologous low molecular weight glutenin loci of the A and Am genomes of wheat - PubMed (original) (raw)

Rapid genome divergence at orthologous low molecular weight glutenin loci of the A and Am genomes of wheat

Thomas Wicker et al. Plant Cell. 2003 May.

Abstract

To study genome evolution in wheat, we have sequenced and compared two large physical contigs of 285 and 142 kb covering orthologous low molecular weight (LMW) glutenin loci on chromosome 1AS of a diploid wheat species (Triticum monococcum subsp monococcum) and a tetraploid wheat species (Triticum turgidum subsp durum). Sequence conservation between the two species was restricted to small regions containing the orthologous LMW glutenin genes, whereas >90% of the compared sequences were not conserved. Dramatic sequence rearrangements occurred in the regions rich in repetitive elements. Dating of long terminal repeat retrotransposon insertions revealed different insertion events occurring during the last 5.5 million years in both species. These insertions are partially responsible for the lack of homology between the intergenic regions. In addition, the gene space was conserved only partially, because different predicted genes were identified on both contigs. Duplications and deletions of large fragments that might be attributable to illegitimate recombination also have contributed to the differentiation of this region in both species. The striking differences in the intergenic landscape between the A and A(m) genomes that diverged 1 to 3 million years ago provide evidence for a dynamic and rapid genome evolution in wheat species.

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Figures

Figure 1.

Genetic and Physical Maps of Orthologous LMW Glutenin Loci in Diploid, Tetraploid, and Hexaploid Wheat Species. BAC libraries from T. monococcum and T. durum were screened with a probe corresponding to the coding region of the TaGlu-1D-1 gene and with SFR159, a shotgun clone of T. monococcum BAC453N11, respectively. The positions of probes on the contigs are indicated. The black dot represents the centromere position. Shaded areas indicate BAC clones that were chosen for complete sequencing. cM, centimorgan.

Figure 2.

Determination of the Copy Number and Chromosomal Location of SFR159 in Chinese Spring and T. durum cv Langdon by DNA Gel Blot Hybridization of HindIII-Digested Genomic DNA of Chinese Spring Nullitetrasomic Lines and of Langdon/Chinese Spring Substitution Lines. TaCS represents the hexaploid wheat line Chinese Spring, TdLDN represents the tetraploid T. durum cv Langdon, and TmDV92 represents diploid T. monococcum line DV92. N1A/T1B, N1B/T1A, and N1D/T1B are nullitetrasomic lines of Chinese Spring. LDN-CS-1D(1A) and LDN-CS-1D(1B) are Langdon/Chinese Spring disomic substitution lines in which chromosome 1D of Chinese Spring replaces chromosome 1A or 1B of Langdon. Arrowheads at left indicate the SFR159 loci missing in the Chinese Spring nullitetrasomic line N1A/T1B (CS 1A) and in the substitution line LDN-CS-1D(1A) (LDN 1A). These loci are attributed to chromosome 1A of Chinese Spring (CS 1A) and to chromosome 1A of T. durum cv Langdon (LDN 1A), respectively. The T. durum fragment is present on Langdon BAC 107G22. Arrowheads at right indicate the three loci detected by SFR159 in T. monococcum line DV92 (Tm 1A).

Figure 3.

Sequence Organization of the T. monococcum and T. durum LMW Glutenin Contigs. (A) T. monococcum sequence contig. a, b, and c indicate regions in which no repetitive elements were identified. (B) T. durum sequence contig. The left end of the contigs is distal on chromosome 1AS. Positions of genes, pseudogenes, and probes used for genetic mapping are indicated above the maps. Transcriptional orientations are indicated with horizontal arrows. The details shown in Figure 6 are indicated with boxes. Colored boxes and black boxes represent gene and pseudogene predictions supported by BLASTX homologies. Genes and pseudogenes are marked as follows: 1, TmGlu-A3-2 (red box); 2, TmHG-1; 3, TmGlu-A3-3 (red box); 4, TmHG-2; 5, TmPIK-1; 6, TmRGL-1 (green box); 7, TmSTF-1; 8, TdHbox-1; 9, TmGlu-A3-1 (red box); 10, TdLRR-1; 11, TdHG-1; 12, TdHG-2; 13, TdHG-3; and 14, TdRGL-1 (green box). RFLP, restriction fragment length polymorphism.

Figure 4.

Model for the Evolution of the TmGlu-A3-2 and TmGlu-A3-3 Loci after the 54-kb Duplication in T. monococcum. Nested repetitive elements are depicted raised above the elements into which they inserted (i.e., the CACTA element C1 has inserted into the CACTA element C2, producing the two fragments C2.1 and C2.2). Regions affected by deletions are indicated with braces. Step 1. A fragment of at least 54 kb is duplicated, creating the two paralogous loci TmGlu-A3-2 and TmGlu-A3-3. Step 2. A foldback element (Zeus_426K20-1) inserted ∼1 kb upstream of the coding region of the TmGlu-A3-2 gene and a CACTA transposon (SNAC_107G22-1) inserted 15 kb downstream of the gene. Two Angela elements inserted close to the left end of the contig. Step 3. The insertions were followed by three deletions (D1, D2, and D3). D1 was an unequal crossover event that resulted in a single LTR (Angela_426K20-1), whereas D2 and D3 were deletions of random fragments. Step 4. A small duplication of ∼4.5 kb resulted in a complex pattern of fragments of repetitive elements. Step 5. The insertions of two CACTA transposons, two LTR retrotransposons (WIS_453N11-1 and Daniela_453N11-1), and the unclassified XG_453N11-1 element increased the size of the TmGlu-A3-3 locus by >40 kb. At the same stage, a random deletion affected the flanking region of the originally duplicated fragment (D4), resulting in the truncated Sabrina_453N11-1 and a small 39-bp fragment of the Paula_453N11-1 element. Step 6. Two additional deletions (D5 and D6) affected two retrotransposons. D5 was a deletion of a random fragment within the internal domain of Daniela_453N11-1, and D6 was an unequal crossover between the two LTRs of WIS_453N11-1. MITE, miniature inverted-repeat transposable element.

Figure 5.

Patterns of DNA Deletions in Wheat. (A) Truncated repetitive elements resulting from random fragment deletions. The deleted regions are indicated with braces. One deletion affected Sabrina_ 453N11-2 and the 3′ region of Emil_453N11-1 as well as the sequences located between them. A second, independent event affected the 5′ region of Emil_453N11-1 as well as a non-LTR retrotransposon (Karin_453N11-1) and Angela_453N11-1, which is nested inside Karin_453N11-1. (B) Direct repeat structures in short InDels from the 54-kb duplication in T. monococcum. InDels were characterized by the alignment of the two duplicated units. Direct repeat structures that could serve as templates for illegitimate recombination are highlighted with boxes.

Figure 6.

Comparison between the Glu-A3 Loci of T. monococcum and T. durum and the TaGlu-1D-1 Locus from the D Genome of Hexaploid Wheat. The depicted regions of the T. monococcum and T. durum sequence contigs correspond to details 1, 2, and 3 in Figure 3. Regions conserved between T. monococcum and T. durum are indicated by light blue areas. Regions conserved between T. monococcum, T. durum, and the TaGlu-1D-1 locus are indicated by pink areas. Repetitive elements nested into other elements are depicted raised above the elements into which they inserted. The estimated insertion times of the repetitive elements (in million years) are shown inside the elements. The vertical arrow indicates the breakpoint of a large deletion in T. monococcum. MITE, miniature inverted-repeat transposable element.

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Rapid genome divergence at orthologous low molecular weight glutenin loci of the A and Am genomes of wheat - PubMed (original) (raw)