Evolution of DNA sequence nonhomologies among maize inbreds

Abstract

Allelic chromosomal regions totaling more than 2.8 Mb and located on maize (Zea mays) chromosomes 1L, 2S, 7L, and 9S have been sequenced and compared over distances of 100 to 350 kb between the two maize inbred lines Mo17 and B73. The alleles contain extended regions of nonhomology. On average, more than 50% of the compared sequence is noncolinear, mainly because of the insertion of large numbers of long terminal repeat (LTR)-retrotransposons. Only 27 LTR-retroelements are shared between alleles, whereas 62 are allele specific. The insertion of LTR-retrotransposons into the maize genome is statistically more recent for nonshared than shared ones. Most surprisingly, more than one-third of the genes (27/72) are absent in one of the inbreds at the loci examined. Such nonshared genes usually appear to be truncated and form clusters in which they are oriented in the same direction. However, the nonshared genome segments are gene-poor, relative to regions shared by both inbreds, with up to 12-fold difference in gene density. By contrast, miniature inverted terminal repeats (MITEs) occur at a similar frequency in the shared and nonshared fractions. Many times, MITES are present in an identical position in both LTRs of a retroelement, indicating that their insertion occurred before the replication of the retroelement in question. Maize ESTs and/or maize massively parallel signature sequencing tags were identified for the majority of the nonshared genes or homologs of them. In contrast with shared genes, which are usually conserved in gene order and location relative to rice (Oryza sativa), nonshared genes violate the maize colinearity with rice. Based on this, insertion by a yet unknown mechanism, rather than deletion events, seems to be the origin of the nonshared genes. The intergenic space between conserved genes is enlarged up to sixfold in maize compared with rice. Frequently, retroelement insertions create a different sequence environment adjacent to conserved genes.

Figure 1.

Schematic Representation of the Sequence Relationship between Maize Inbreds B73 and Mo17 at Locus9002 on Chromosome 1L (Bin 1.08; Markers bz2, An1, and umc1446). The shared sequence between the inbreds is represented by the bar labeled “Shared sequence.” The sequence segments unique to either B73 or Mo17 are represented as “Mo17-specific” and “B73-specific,” with their positions of insertion indicated by dotted arrows, relative to the shared sequence. LTR-retrotransposons are represented by colored boxes, which are also drawn in a different width if nested. Retrotransposon boxes contain labels, which are cross-referenced to the tables, and the insertion times in Myr based on LTR sequence divergence (Ma and Bennetzen, 2004a). Elements in dotted brackets were excluded from the intraspecific comparison. Predicted genes are indicated with black pentagons and transposons with pink arrows. Only nonshared and individually inserted MITE M2 is shown with a red triangle.

Figure 2.

Schematic Representation of the Sequence Relationship between Maize Inbreds B73 and Mo17 at Locus9008 on Chromosome 2S (Bin 2.04; Markers umc1326 and umc1448). The shared sequence between the inbreds is represented by the bar labeled “Shared sequence.” The sequence segments unique to either B73 or Mo17 are represented as “Mo17-specific” and “B73-specific,” with their positions of insertion indicated by dotted arrows, relative to the shared sequence. LTR-retrotransposons are represented by colored boxes, which are also drawn in a different width if nested. Retrotransposon boxes contain labels, which are cross-referenced to the tables, and the insertion times in Myr based on LTR sequence divergence (Ma and Bennetzen, 2004a). Elements in dotted brackets were excluded from the intraspecific comparison. Predicted genes are indicated with black pentagons, transposons with pink arrows, and non-LTR-retrotransposons with black triangles.

Figure 3.

Schematic Representation of the Sequence Relationship between Maize Inbreds B73 and Mo17 at Locus9009 on Chromosome 7L (Bin 7.04; Markers rpot1 and umc1295). The sequence segments unique to either B73 or Mo17 are represented as “Mo17-specific” and “B73-specific,” with their positions of insertion indicated by dotted arrows, relative to the shared sequence. LTR-retrotransposons are represented by colored boxes, which are also drawn in a different width if nested. Retrotransposon boxes contain labels, which are cross-referenced to the tables, and the insertion times in Myr based on LTR sequence divergence (Ma and Bennetzen, 2004a). Elements in dotted brackets were excluded from the intraspecific comparison. Predicted genes are indicated with black pentagons, transposons with pink arrows, and non-LTR-retrotransposons with black triangles. Only nonshared and individually inserted MITE M1 is shown with a red triangle.

Figure 4.

Schematic Representation of the Sequence Relationship between Maize Inbreds B73 and Mo17 at the adh1 Locus on Chromosome 7L (Bin 7.04; Markers rpot1 and umc1295). The sequence segments unique to either B73 or Mo17 are represented as “Mo17-specific” and “B73-specific,” with their positions of insertion indicated by dotted arrows, relative to the shared sequence. LTR-retrotransposons are represented by colored boxes, which are also drawn in a different width if nested. Retrotransposon boxes contain labels, which are cross-referenced to the tables, and the insertion times in Myr based on LTR sequence divergence (Ma and Bennetzen, 2004a). Elements in dotted brackets were excluded from the intraspecific comparison. Predicted genes are indicated with black pentagons and non-LTR-retrotransposons with black triangles.

Figure 5.

Diagram Showing the Fraction (%) of Genic and Nongenic Sequences in the Shared, Nonshared, and Total Sequence at Loci 9002, 9008, 9009, and adh1 (see Supplemental Table 5 Online for Complete Data Set).

Figure 6.

Rice–Maize Colinearity of the Analyzed Maize Genes at Locus9002, Locus9008, and Locus9009. (A) Locus9002. (B) Locus9008. (C) Locus9009. The physical distance between conserved genes is indicated for both species with brackets. Genes that are present in rice but absent in one of the maize inbreds are likely to be deletions in the other inbred. Genes absent in rice but present in one of the maize inbreds are likely to be recent insertions in maize. Genes absent in rice but present in both maize inbreds may have been deleted in the rice lineage or inserted in the common ancestor of B73 and Mo17. cen., centromere; tel., telomere.

Figure 7.

Schematic Representation of the Sequence Relationship among Maize Inbreds B73, Mo17, and McC at the bz1 Locus on Chromosome 9S (Bin 9.02) (Modified from Fu and Dooner, 2002). Dashed green lines indicate the shared sequence between all three inbred lines. Dashed gray and orange lines indicate the shared sequence regions between the inbreds B73 and Mo17 and between Mo17 and McC, respectively. Inserted and deleted regions are connected via dashed lines. The LTR-retrotransposons unique to McC or Mo17 and/or B73 are represented by different colored boxes, which are also drawn in a different width if nested, with their positions of insertion indicated by dotted arrows. Retrotransposon boxes contain labels, which are cross-referenced to the tables, and the insertion times in Myr based on LTR sequence divergence (Ma and Bennetzen, 2004a). Genes are represented as black pentagons. The location of exons 7 and 8 and intron 7 of gene hypro3 is labeled with a red line.

Figure 8.

Distribution of the Retrotransposon Insertion Times Calculated from the LTR Sequence Divergence (Ma and Bennetzen, 2004a). Open bars show the distribution of shared LTR-retrotransposons, and closed bars represent the distribution of nonshared LTR-retrotransposons.