Gene loss and movement in the maize genome

Abstract

Maize (Zea mays L. ssp. mays), one of the most important agricultural crops in the world, originated by hybridization of two closely related progenitors. To investigate the fate of its genes after tetraploidization, we analyzed the sequence of five duplicated regions from different chromosomal locations. We also compared corresponding regions from sorghum and rice, two important crops that have largely collinear maps with maize. The split of sorghum and maize progenitors was recently estimated to be 11.9 Mya, whereas rice diverged from the common ancestor of maize and sorghum approximately 50 Mya. A data set of roughly 4 Mb yielded 206 predicted genes from the three species, excluding any transposon-related genes, but including eight gene remnants. On average, 14% of the genes within the aligned regions are noncollinear between any two species. However, scoring each maize region separately, the set of noncollinear genes between all four regions jumps to 68%. This is largely because at least 50% of the duplicated genes from the two progenitors of maize have been lost over a very short period of time, possibly as short as 5 million years. Using the nearly completed rice sequence, we found noncollinear genes in other chromosomal positions, frequently in more than one. This demonstrates that many genes in these species have moved to new chromosomal locations in the last 50 million years or less, most as single gene events that did not dramatically alter gene structure.

Figure 1

Graphic representation of the alignment, position, and polarity of all predicted genes within the selected chromosomal intervals of maize, sorghum, and rice. The relative positions of all predicted and known genes of the orthologous regions, defined by the six genetic markers highlighted under the bottom interval in red, are graphically presented. Each interval is drawn as a horizontal bar with the gene polarity indicated by an arrow. The origin of each region is labeled to the left of the bar. The physical length of each interval and other properties are reported in Table 1. Predicted and known genes are numbered from the left to the right for each interval. Duplicated genes are given the same number but ordered by a, b, c,.... Gene numbers with an ^* indicate gene remnants. Conservation of genes between different intervals is indicated by vertical connecting lines. A key is provided as an inset to show the conserved genes (collinear genes), and also the noncollinear genes, genes in flanking regions, and gene remnants. (A) An alignment of regions containing the zmfie1/2 and orp1/2 genes and their orthologs in sorghum and rice. (B) The r1/b1 genes and their orthologs. (C) The c1/pl1 genes and their orthologs. (D) The tb1/2 genes and their orthologs. (E) The tbp1/2 genes and their orthologs.

Figure 2