Dynamic evolution of oryza genomes is revealed by comparative genomic analysis of a genus-wide vertical data set

Abstract

Oryza (23 species; 10 genome types) contains the world's most important food crop - rice. Although the rice genome serves as an essential tool for biological research, little is known about the evolution of the other Oryza genome types. They contain a historical record of genomic changes that led to diversification of this genus around the world as well as an untapped reservoir of agriculturally important traits. To investigate the evolution of the collective Oryza genome, we sequenced and compared nine orthologous genomic regions encompassing the Adh1-Adh2 genes (from six diploid genome types) with the rice reference sequence. Our analysis revealed the architectural complexities and dynamic evolution of this region that have occurred over the past approximately 15 million years. Of the 46 intact genes and four pseudogenes in the japonica genome, 38 (76%) fell into eight multigene families. Analysis of the evolutionary history of each family revealed independent and lineage-specific gain and loss of gene family members as frequent causes of synteny disruption. Transposable elements were shown to mediate massive replacement of intergenic space (>95%), gene disruption, and gene/gene fragment movement. Three cases of long-range structural variation (inversions/deletions) spanning several hundred kilobases were identified that contributed significantly to genome diversification.

Figure 1.

Comparative Phylogenomic View of the Orthologous Adh1 Vertical Data Set across the Genus Oryza. Genes from each Oryza species are denoted by the first letter of each species (i.e., J, japonica; I, indica; N, nivara; R, rufipogon; G, glaberrima, P, punctata; O, officinalis; A, australiensis, B, brachyantha; GR, granulata). Each gene family is color coded to depict dynamics of gene family evolution.

Figure 2.

Phylogenetic Relationships of Individual Conserved Core Genes across Oryza and a Consensus Tree Depicting All Topologies. (A) Consensus diploid tree with all six core genes. (B) Oryza Adh1 gene species tree. (C) Oryza Adh2 species tree. (D) Oryza RZ53 gene species tree. (E) Oryza NifS gene species tree. (F) Oryza Peroxidase gene species tree. (G) Oryza PIK gene species tree.

Figure 3.

Expanded View of Figure 1 That Depicts F-box Gene Family Dynamics.

Figure 4.

Unrooted Phylogenetic Tree Demonstrating the Evolutionary Origin and Diversification of F-box or F-box–Like Genes in the Genus-Wide Adh1 Vertical Sequence Data Set. Bootstrap values (.50%) are displayed on branches.