Massive gene losses in Asian cultivated rice unveiled by comparative genome analysis

Abstract

Background: Rice is one of the most important food crops in the world. With increasing world demand for food crops, there is an urgent need to develop new cultivars that have enhanced performance with regard to yield, disease resistance, and so on. Wild rice is expected to provide useful genetic resources that could improve the present cultivated species. However, the quantity and quality of these unexplored resources remain unclear. Recent accumulation of the genomic information of both cultivated and wild rice species allows for their comparison at the molecular level. Here, we compared the genome sequence of Oryza sativa ssp. japonica with sets of bacterial artificial chromosome end sequences (BESs) from two wild rice species, O. rufipogon and O. nivara, and an African rice species, O. glaberrima.

Results: We found that about four to five percent of the BESs of the two wild rice species and about seven percent of the African rice could not be mapped to the japonica genome, suggesting that a substantial number of genes have been lost in the japonica rice lineage; however, their close relatives still possess their counterpart genes. We estimated that during evolution, O. sativa has lost at least one thousand genes that are still preserved in the genomes of the other species. In addition, our BLASTX searches against the non-redundant protein sequence database showed that disease resistance-related proteins were significantly overrepresented in the close relative-specific genomic portions. In total, 235 unmapped BESs of the three relatives matched 83 non-redundant proteins that contained a disease resistance protein domain, most of which corresponded to an NBS-LRR domain.

Conclusion: We found that the O. sativa lineage appears to have recently experienced massive gene losses following divergence from its wild ancestor. Our results imply that the domestication process accelerated large-scale genomic deletions in the lineage of Asian cultivated rice and that the close relatives of cultivated rice have the potential to restore the lost traits.

Figure 1

Phylogenetic tree of the five Oryza species used in this study: Oj, O. sativa L. ssp. japonica; Oi, O. sativa L. ssp. indica; On, O. nivara; Or, O. rufipogon; and Og, O. glaberrima. We employed the maximum-parsimony method using the third positions of 15,053 codons. Bootstrap values are shown above the internal branches. The scale indicates the branch length.

Figure 2

Shared and unique genomic portions in four Oryza species. Although the Oj-specific portion is unknown, the size of the shared region in Oj is expected to be nearly equal to that in On or Or.

Figure 3

Relationship between the numbers of synonymous substitutions and unique genes. Black circles represent the numbers of unique genes that are missing from the Oj genome, and black triangles represent the numbers of unique genes that are missing from the Oi genome. A white circle represents the number of Oi-specific genes missing from the Oj genome, and a white triangle represents the number of Oj-specific genes missing from the Oi genome. The regression line indicates a constant rate of gene deletion over time.

Figure 4

Functional classifications of Oj and Or proteins. The classifications of mapped and unmapped BESs of Or were derived from the nr database proteins that were homologous to the mapped and unmapped BESs (see Materials and Methods). Protein categories are based on the molecular functions of the Gene Ontology (GO) hierarchy.

Figure 5

Phylogenetic tree of possible disease resistance proteins. CL716448 is a newly found homologue of O. nivara (On). Accession numbers and species names are shown. Oj stands for O. sativa L. ssp. japonica and Oi for indica. The tree was reconstructed by the neighbour-joining method [59]. The interior branches were tested by 1,000 bootstrap replicates, and bootstrap values of 50% or more are shown above the branches. The scale indicates the branch length.