Uneven chromosome contraction and expansion in the maize genome

Abstract

Maize (Zea mays or corn), both a major food source and an important cytogenetic model, evolved from a tetraploid that arose about 4.8 million years ago (Mya). As a result, maize has extensive duplicated regions within its genome. We have sequenced the two copies of one such region, generating 7.8 Mb of sequence spanning 17.4 cM of the short arm of chromosome 1 and 6.6 Mb (25.6 cM) from the long arm of chromosome 9. Rice, which did not undergo a similar whole genome duplication event, has only one orthologous region (4.9 Mb) on the short arm of chromosome 3, and can be used as reference for the maize homoeologous regions. Alignment of the three regions allowed identification of syntenic blocks, and indicated that the maize regions have undergone differential contraction in genic and intergenic regions and expansion by the insertion of retrotransposable elements. Approximately 9% of the predicted genes in each duplicated region are completely missing in the rice genome, and almost 20% have moved to other genomic locations. Predicted genes within these regions tend to be larger in maize than in rice, primarily because of the presence of predicted genes in maize with larger introns. Interestingly, the general gene methylation patterns in the maize homoeologous regions do not appear to have changed with contraction or expansion of their chromosomes. In addition, no differences in methylation of single genes and tandemly repeated gene copies have been detected. These results, therefore, provide new insights into the diploidization of polyploid species.

Figure 1.

Alignments of chromosomal regions from Zm1S, Os3S, and Zm9L. The three horizontal lines with scales in million basepairs (Mb) represent the chromosomal regions from Zm1S, Os3S, and Zm9L. On these horizontal lines, the positions of the genes are marked with a white vertical bar. Above those lines, a schematic diagram shows the alignment of these regions with respect to their chromosomal locations. Vertical lines connect syntenic genes between Zm1S and Os3S, and Zm9L and Os3S, respectively. Line color indicates syntenic arrangement of genes between Zm1S–Os3S–Zm9L (red), syntenic arrangement of tandem genes (green), and syntenic arrangements of genes either between Zm1S–Os3S or between Zm9L–Os3S (black). Syntenic blocks are labeled A, B1, B2, C, and D. Syntenic blocks are interrupted by regions without corresponding genes. The expansion grade of each syntenic block with respect to rice is shown as fold expansion.

Figure 2.

Corresponding, syntenic genes between the Zm1S, Os3S, and Zm9L chromosomal regions. Gene models for all three regions were determined as described in the text. A graphic representation is given for genes (A) that are syntenic, have homologs within the syntenic regions, have homologs in the rice genome or maize GSSs/EST collections, have a homologous counterpart in other plant EST collections, or are species-specific; and (B) that are syntenic between both maize regions and have a homolog or no homolog on the other maize chromosome. Each fraction is labeled with the number of genes and the percentage of the total within its sample.

Figure 3.

Position and density of sequence features of the maize regions Zm1S and Zm9L, and rice chromosomal region Os3S. Color-coded densities of several genomic features (repeats, coverage by filtrated GSSs and genes) are shown for Zm1S, Zm9L, and Os3S. Blue represents lowest (0%), green medium (50%), and red highest (100%) density of the respective feature. Relative density has been determined within a sliding window of 50 kb and in steps of 1000 bp. Locations of GSSs represent alignment positions by BLASTN. Note that the four high-density regions within the maize gene bars indicate four very large genes (>50 kb gene size) that were predicted by our annotation.